Growth, tolerance, and enzyme activities of Trichoderma strains in culture media added with a pyrethroids-based insecticide

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GS20: 10% w/v gelatin+10% w/v pregelled starch; GS7.5: 10% w/v gelatin+5% w/v pregelled starch." ] ] ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "Jorge Alberto Zimmermann, Noelí Sirini, Carolina Raquel Olivero, María Sol Renna, Marcelo Lisandro Signorini, María Virginia Zbrun, Laureano Sebastián Frizzo, Lorena Paola Soto" "autores" => array:8 [ 0 => array:2 [ "nombre" => "Jorge Alberto" "apellidos" => "Zimmermann" ] 1 => array:2 [ "nombre" => "Noelí" "apellidos" => "Sirini" ] 2 => array:2 [ "nombre" => "Carolina Raquel" "apellidos" => "Olivero" ] 3 => array:2 [ "nombre" => "María Sol" "apellidos" => "Renna" ] 4 => array:2 [ "nombre" => "Marcelo Lisandro" "apellidos" => "Signorini" ] 5 => array:2 [ "nombre" => "María Virginia" "apellidos" => "Zbrun" ] 6 => array:2 [ "nombre" => "Laureano Sebastián" "apellidos" => "Frizzo" ] 7 => array:2 [ "nombre" => "Lorena Paola" "apellidos" => "Soto" ] ] ] ] "resumen" => array:1 [ 0 => array:3 [ "titulo" => "Highlights" "clase" => "author-highlights" "resumen" => "<ul class="elsevierStyleList" id="lis0005"><li class="elsevierStyleListItem" id="lsti0005">•Capsules designed with industrial materials are effective as probiotic carrier for pigs.</li><li class="elsevierStyleListItem" id="lsti0010">•Whey permeate protects the inoculum during lyophilization process.</li><li class="elsevierStyleListItem" id="lsti0015">•Freezing and vacuum condition maintain the viability of the inoculum for 210 days.</li><li class="elsevierStyleListItem" id="lsti0020">•Encapsulation protect the inoculum under simulated gastrointestinal conditions.</li><li class="elsevierStyleListItem" id="lsti0025">•Macrocapsules ensure delivery to the site of action in the gastrointestinal tract.</li></ul>" ] ] ] "idiomaDefecto" => "en" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S0325754123000822?idApp=UINPBA00004N" "url" => "/03257541/0000005600000001/v1_202403171031/S0325754123000822/v1_202403171031/en/main.assets" ] 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"en" => true "es" => true ] "contieneTextoCompleto" => array:1 [ "en" => true ] "contienePdf" => array:1 [ "en" => true ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0010" "etiqueta" => "Figure 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 599 "Ancho" => 755 "Tamanyo" => 100363 ] ] "descripcion" => array:1 [ "en" => "Microscope photography of epilated eyelashes showing adults and eggs of Demodex folliculorum (100×)." ] ] ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "Viviana Flores, Marina Ruf, Silvia Paola Abad Farfan, Andrea Vanessa Suárez Echávez, Dolores Pilar Bastard, Maria Celeste Puga, Luis Daniel Mazzuoccolo" "autores" => array:7 [ 0 => array:2 [ "nombre" => "Viviana" "apellidos" => "Flores" ] 1 => array:2 [ "nombre" => "Marina" "apellidos" => "Ruf" ] 2 => array:2 [ "nombre" => "Silvia Paola" "apellidos" => "Abad Farfan" ] 3 => array:2 [ "nombre" => "Andrea Vanessa" "apellidos" => "Suárez Echávez" ] 4 => array:2 [ "nombre" => "Dolores Pilar" "apellidos" => "Bastard" ] 5 => array:2 [ "nombre" => "Maria Celeste" "apellidos" => "Puga" ] 6 => array:2 [ "nombre" => "Luis Daniel" "apellidos" => "Mazzuoccolo" ] ] ] ] "resumen" => array:1 [ 0 => array:3 [ "titulo" => "Highlights" "clase" => "author-highlights" "resumen" => "<ul class="elsevierStyleList" id="lis0015"><li class="elsevierStyleListItem" id="lsti0005">•High prevalence of Demodex spp. blepharitis in patients older than 60 years old.</li><li class="elsevierStyleListItem" id="lsti0010">•Meibomitis, dandruff, itching, epiphora were associated with blepharitis by Demodex spp.</li><li class="elsevierStyleListItem" id="lsti0015">•Diagnosis of blepharitis by Demodex spp. allows for an adequate treatment.</li></ul>" ] ] ] "idiomaDefecto" => "en" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S032575412300055X?idApp=UINPBA00004N" "url" => "/03257541/0000005600000001/v1_202403171031/S032575412300055X/v1_202403171031/en/main.assets" ] "en" => array:21 [ "idiomaDefecto" => true "cabecera" => "Original article" "titulo" => "Growth, tolerance, and enzyme activities of Trichoderma strains in culture media added with a pyrethroids-based insecticide" "tieneTextoCompleto" => true "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "79" "paginaFinal" => "89" ] ] "autores" => array:1 [ 0 => array:4 [ "autoresLista" => "Caliope Mendarte-Alquisira, Alejandro Alarcón, Ronald Ferrera-Cerrato" "autores" => array:3 [ 0 => array:2 [ "nombre" => "Caliope" "apellidos" => "Mendarte-Alquisira" ] 1 => array:2 [ "nombre" => "Alejandro" "apellidos" => "Alarcón" ] 2 => array:4 [ "nombre" => "Ronald" "apellidos" => "Ferrera-Cerrato" "email" => array:1 [ 0 => "rferreracerrato@gmail.com" ] "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "*" "identificador" => "cor0005" ] ] ] ] "afiliaciones" => array:1 [ 0 => array:2 [ "entidad" => "Área de Microbiología, Posgrado de Edafología, Colegio de Postgraduados, Carretera Federal México-Texcoco km 36.5, Montecillo 56264, Estado de México, Mexico" "identificador" => "aff0005" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Crecimiento, tolerancia y actividades enzimáticas de cepas de Trichoderma en medios de cultivo adicionados con un insecticida a base de piretroides" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0010" "etiqueta" => "Figure 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 2895 "Ancho" => 2091 "Tamanyo" => 275621 ] ] "descripcion" => array:1 [ "en" => "(a) Radial growth rate (mm/h) and (b) radial growth rate inhibition (RGRI%) of Trichoderma strains and Phanerochaete chrysosporium-ATCC34540 in solid medium (PDA) with 0, 50, 100, 150, and 200mg/l of commercial insecticide H24® with three active ingredients (permethrin, prallethrin, and propoxur). Means±standard error (n=4)." ] ] ] "textoCompleto" => "IntroductionAfter the prohibition of using the highly toxic and persistent dichloro diphenyl trichloroethane (DDT), alternate insecticides based on carbamates and pyrethroids (single or combined) began to be utilized for controlling insect pests<a class="elsevierStyleCrossRef" href="#bib0335">17</a>. However, these insecticides may also represent potential issues for human and environmental health<a class="elsevierStyleCrossRef" href="#bib0485">47</a>. Some carbamates such as propoxur or pyrethroids such as permethrin and prallethrin may have carcinogenic and mutagenic properties, and inflammatory effects in the stomach; in addition, they are also associated with alterations in functional sodium channels and poor motor development in children<a class="elsevierStyleCrossRefs" href="#bib0375">25,30,44</a>. Furthermore, several studies reported the effect of carbamates and pyrethroids on beneficial bacteria and communities in the rhizosphere<a class="elsevierStyleCrossRefs" href="#bib0300">10,35,36,38,47</a>. Therefore, research focused on improving strategies for integrated pest management, which includes the combination of organically-derived pesticides and the application of antagonist microorganisms to reduce chemical damage induced by insecticides in the environment<a class="elsevierStyleCrossRef" href="#bib0440">38</a>.Trichoderma genus includes worldwide ubiquitous fungi commonly found in soils and possesses a powerful and versatile enzymatic machinery (including cellulases, chitinases, peroxidases, and proteases, among others) which may degrade a wide range of organic recalcitrant compounds in soil<a class="elsevierStyleCrossRefs" href="#bib0265">3,29,41</a>. Commonly, Trichoderma is one of the widest fungi directed to control plant pathogens since they produce enzymes with hydrolytic capacity and secondary metabolites related to processes such as antibiosis, space competition, plant growth improvement, and resistance against biotic and abiotic stresses<a class="elsevierStyleCrossRefs" href="#bib0385">27,32,37</a>. Furthermore, Trichoderma spp. are tolerant to many agrochemicals and have the potential to degrade chemical pesticides because they possess specific enzymes to metabolize such compounds<a class="elsevierStyleCrossRef" href="#bib0290">8</a>.Therefore, the aims of this research were (1) to determine the tolerance of several strains of Trichoderma to solid culture medium contaminated with commercial insecticide H24® (composed of pyrethroids, permethrin and prallethrin, and carbamate propoxur) and (2) to evaluate the effect of this insecticide on the release of enzymes such as chitinases, peroxidases, and endoglucanases by selected Trichoderma strains grown in liquid culture medium.Materials and methodsMicrobiological materialsThis research utilized ten strains of Trichoderma: Trich CP01 (T. virens), Trich CP03 (T. koningii), Trich CP04 (T. viride), Trich CP022 (T. virens), Trich CP023 (T. koningii), Trich CP037 (T. virens) Trich CP038 (T. harzianum), Trich CP056 (T. viride), Trich CP0X (T. atroviride), Trich CP0TGC (T. viride), and one strain of Phanerochaete chrysosporium-ATCC 34540 (CDBB 686) as referential fungus able to degrade toxic organic contaminants.All Trichoderma strains are part of the microbial collection of the Microbiology Laboratory (Colegio de Postgraduados), which were reported as tolerant to crude oil, and to high concentrations of naphthalene, phenanthrene, and benzo[a]pyrene<a class="elsevierStyleCrossRef" href="#bib0260">2</a>. The strain of P. chrysosporium-ATCC 34540 (CDBB 686) was acquired from the CINVESTAV microbial repository and reported as tolerant and degrader of persistent organic pollutants, including insecticides<a class="elsevierStyleCrossRef" href="#bib0370">24</a>.Chemical reagents and culture mediaThe commercial insecticide H24® contains permethrin (360mg/kg), propoxur (890mg/kg) and prallethrin (50mg/kg) as active ingredients; thus, the total of active ingredients yields up to 1300mg/kg, which are dissolved in an organic solvent. This commercial insecticide is commonly applied for controlling flying and crawling insects that attack cotton crops due to its active ingredient permethrin. Potato dextrose agar (PDA) medium (BD Bioxon®) was prepared according to the manufacturer's specifications and different concentrations of the commercial insecticide (0, 50, 100, 150, and 200ppm) were added to it.The liquid culture consisted of a mineral medium (MM) prepared in accordance with Gao et al. with some modifications<a class="elsevierStyleCrossRef" href="#bib0315">13</a>. The MM contained (g/l): 1.0 K2HPO4, 0.5 KCl, 0.5 MgSO4·7H2O, 0.01 FeSO4, pH 7.0. The nitrogen source was meat peptone (CAS 91079-38-8, Merck), considering a nitrogen content of ∼12.5% and nitrogen in the insecticide (propoxur), the carbon source was sucrose and that carbon derived from the insecticide. The final C/N ratio was ∼20/1, considering 100ppm of active ingredients (permethrin, prallethrin, and propoxur) in commercial insecticide H24®. Both media were autoclaved at 121°C for 15min; afterwards, the H24® insecticide was added using filtration.Bioassay 1. Fungal growth and tolerance to increased concentrations of commercial insecticideAgar disks of 5mm in diameter with fungal mycelium were sown in Petri dishes containing solid PDA medium with or without the commercial insecticide (four replicates per treatment); all fungal cultures were incubated at 28°C for 96h. The growth diameter was measured every 24h, for 4 days. The results were used to estimate the radial growth, radial growth rate, radial growth rate inhibition (%) (RGRI%), and the inhibitory dose 50 (ID50)<a class="elsevierStyleCrossRefs" href="#bib0390">28,34</a>. The radial growth rate was calculated with the quadratic equation that was fitted to the dose–response curve for each strain. The radial growth rate was used to estimate the (ID50) for each strain and the RGRI%<a class="elsevierStyleCrossRefs" href="#bib0390">28,34</a>. The ID50 was also utilized as a reference to define a sub-ID50 without inhibiting the growth and further estimations<a class="elsevierStyleCrossRef" href="#bib0415">33</a>.Bioassay 2. Fungal protein content and induced peroxidase, chitinase, and glucanase activities in a liquid medium containing/contaminated with 100ppm of commercial insecticideFour tolerant strains of Trichoderma sp. (a consortium of Trichoderma sp.) selected from Bioassay 1, and P. chrysosporium-ATCC 34540 were used for evaluating the effect of a sub-ID50 of commercial insecticide H24® on the enzymatic activities of interest.The initial fungal inoculum was adjusted for applying 1×106 spores ml of the Trichoderma consortium (adding the same number of spores per each fungal strain), and 1×106 spores ml of P. chrysosporium-ATCC 34540. Fungal cultures were maintained for 8 days at 200rpm and 28°C. Afterwards, protein analysis and enzyme tests were performed.Protein content was determined with the Biuret method by using bovine albumin as standard<a class="elsevierStyleCrossRef" href="#bib0320">14</a>. The reaction mixture contained 100μl of fungal supernatant and 1000μl of Biuret reagent. This mixture was incubated for 30min at room temperature (20–25°C). Then, absorbance readings at 540nm were taken by using a spectrophotometer (Synergy 2, Biotek®).Non-specific peroxidase (POX, EC 1.11.1.7) activity was measured in 96-well microplates by mixing 20μl of the fungal supernatant with 190μl of phosphate buffer (50mM, pH 7.0), 10μl of guaiacol 1%, and 20μl of H2O2 in phosphate buffer (50mM, pH 7.0). Absorbance readings at 450nm were taken from this mixture every 15s for 5min, by using a spectrophotometer (Synergy 2, Biotek®). POX activity was calculated using a molar extinction coefficient (ɛ) of 16.8/mMcm. One unit of POX activity is defined as the amount of enzyme that catalyzes the formation of 1μmol of tetraguaiacol per min at 25°C and pH 7.0<a class="elsevierStyleCrossRef" href="#bib0285">7</a>.Chitinase activity (GlcNAc activity) was measured by using the method proposed by Vargas-Hoyos and Gilchrist-Ramelli, using N-acetyl-d-glucosamine (GlcNAc) as standard<a class="elsevierStyleCrossRefs" href="#bib0360">22,42</a>. Thus, 500μl of fungal supernatant was mixed with 100μl of colloidal chitin in sodium citrate buffer (50mM, pH 5.2), and incubated for 30min at 40°C; then, the mixture was cooled at ambient temperature (20–25°C), and 2000μl of dinitrosalicylic acid (DNS) were added, for further incubation at 90°C for 5min. The reaction mixture was cooled with iced water, and absorbance readings were measured at 540nm in a Synergy 2, Biotek® spectrophotometer. One unit of GlcNAc activity was defined as the amount of the enzyme necessary to liberate 1μmol/min of reducing sugar (glucose). Enzyme activity was expressed in units per mg of protein.β-1,4-Glucanase activity (CMCase activity) was quantified by the DNS technique using d-glucose as standard<a class="elsevierStyleCrossRefs" href="#bib0325">15,22</a>. The reaction mixture consisted of 500μl of carboxymethyl cellulose (2%) in sodium citrate buffer (50mM, pH 4.8) and 500μl of fungal supernatant. The mixture was incubated for 30min at 50°C and cooled at room temperature. Then, 5000μl of DNS solution was added and incubated at 90°C for 5min; the reaction was stopped by adding iced water. Absorbance readings were taken at 540nm in a spectrophotometer (Synergy 2, Biotek®). One unit of CMCase activity was defined as the amount of the enzyme necessary to liberate 1μmol/min of glucose, and the enzyme activity was expressed in terms of units per mg of protein.Statistical analysisData were analyzed by one-way ANOVA and by the mean comparison test (Tukey, α=0.05). Data represents the values of the means±standard error (SE), from four replicates for each treatment. Analyses were performed using SPSS software, version PASW 18 (IBM SPSS-IBM Corp).ResultsBioassay 1. Fungal growth and tolerance to three concentrations of commercial insecticideIn general, all Trichoderma strains tolerated the presence of the commercial insecticide H24® when applied at 50, 100, and 150ppm. Nevertheless, the strains CP01 (Trichoderma virens), CP04 (T. viride), CP038 (T. harzianum), CP056 (T. viride), and CP0TGC (T. viride) stopped their growth after 72h of exposure to 150ppm of the commercial insecticide (<a class="elsevierStyleCrossRef" href="#fig0005">Figs. 1b–d</a>). Only four Trichoderma strains (CP03 T. koningii, CP022 T. virens, CP037 T. virens, and CP0X T. atroviride) tolerated the application of the insecticide at 200ppm (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>e). Fungal adaptation to the insecticide occurred after 24h when all Trichoderma strains exposed to 50, 100, 150, and 200ppm showed visible mycelial growth (<a class="elsevierStyleCrossRef" href="#fig0005">Figs. 1b–e</a>).<elsevierMultimedia ident="fig0005"></elsevierMultimedia>The growth rate of Trichoderma strains and P. chrysosporium-ATCC 34540 in a solid medium (PDA) containing 0, 50, 100, 150, and 200ppm of active ingredients (permethrin, prallethrin, and propoxur) of the commercial insecticide was determined. The tested concentrations had a negative effect on the radial growth rate of all Trichoderma strains and P. chrysosporium-ATCC 34540 when compared to their respective control without insecticide. The radial growth rate achieved at 150ppm oscillated between ∼0.50 and ∼0.09mm/h, while the radial growth rate for tolerant strains at 200ppm was between ∼0.53 and ∼0.17mm/h (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>a). Trich CP037 (T. virens) showed the lowest radial growth rate when exposed to 200ppm of the commercial insecticide (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>).<elsevierMultimedia ident="fig0010"></elsevierMultimedia>Data from radial growth rate and radial growth rate inhibition (%) were used to obtain the inhibitory dose 50 (ID50) of the commercial insecticide (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>). ID50 showed variations among all fungal strains. The values of the ID50 for those tolerant strains (Trich CP01; Trich CP04; Trich CP023; Trich CP038; Trich CP056; Trich CP0TGC) exposed to 150ppm ranged from 77.27 to 107.66ppm. Moreover, the values of the ID50 for those tolerant strains (Trich CP03; Trich CP022; Trich CP037; Trich CP0X; and P. chrysosporium-ATCC 34540) exposed to 200ppm ranged between 131.64 and 219.04ppm; of these strains, Trich CP037 showed the highest ID50 value (219.04ppm) when compared to that from P. chrysosporium-ATCC 34540 (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>).<elsevierMultimedia ident="tbl0005"></elsevierMultimedia>In addition, ID50 was used for a proposed sub-ID50 for those fungal strains that tolerated 200ppm of the commercial insecticide. This sub-ID50 was utilized for Bioassay 2 to determine the enzyme activities from a Trichoderma sp. consortium and P. chrysosporium-ATCC 34540.Bioassay 2. Fungal growth, protein content, and induced peroxidase, chitinase, and glucanase activities in a liquid medium containing 100mg/l of commercial insecticideThe Trichoderma consortium [Trich CP03 (T. koningii), Trich CP022 (T. virens), Trich CP037 (T. virens), and Trich CP0X (T. atroviride)], and P. chrysosporium-ATCC 34540, were exposed to 100ppm of the active ingredient of the commercial insecticide. After eight days, either the Trichoderma sp. consortium or P. chrysosporium grew and released proteins and enzymes into the contaminated liquid culture (<a class="elsevierStyleCrossRefs" href="#fig0015">Figs. 3 and 4</a>).<elsevierMultimedia ident="fig0015"></elsevierMultimedia><elsevierMultimedia ident="fig0020"></elsevierMultimedia>In the present study, we observed that the growth of the Trichoderma consortium and P. chrysosporium was not affected by the active ingredients contained in the commercial insecticide (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>a). However, in the absence and presence of insecticides, the biomass of the Trichoderma sp. consortium was significantly higher (∼7-fold) than that of P. chrysosporium.The strain of P. chrysosporium-ATCC 34540 produced more protein than the Trichoderma consortium in the absence or presence of the insecticide. The insecticide significantly influenced the protein production in the Trichoderma consortium and P. chrysosporium, whose protein content increased by ∼1.3-fold under the contaminated culture (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>b).On the other hand, without the insecticide, the Trichoderma consortium had significantly higher (∼1.8-fold) POX activity than P. chrysosporium, reaching levels of ∼6000U/μg protein when compared to P. chrysosporium (∼3250U/μg protein) (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>c). Under insecticide contamination, POX activity increased in both fungal cultures; for the Trichoderma consortium, an increase of POX was achieved (∼1.4-fold), whereas for P. chrysosporium the increase of POX was about ∼2.1-fold than that of the respective control in the absence of the insecticide. Overall, the POX activity of the Trichoderma consortium was slightly higher (∼1.2-fold) but not significant, as determined for P. chrysosporium (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>c).The chitinase activity (GlcNAc activity) for the Trichoderma consortium was higher (∼1.2-fold) than that achieved for P. chrysosporium, either in the absence or presence of the insecticide (<a class="elsevierStyleCrossRef" href="#fig0020">Fig. 4</a>a). Overall, the application of the insecticide caused a 25% decrease in the GlcNAc activity of both fungal cultures; however, the GlcNAc activity in the Trichoderma consortium was always significantly higher (∼1.2-fold) than that in P. chrysosporium (<a class="elsevierStyleCrossRef" href="#fig0020">Fig. 4</a>a).In the absence of the insecticide, the CMCase activity for the Trichoderma consortium was significantly higher (∼1.4-fold) than the CMCase activity achieved by P. chrysosporium. The insecticide significantly decreased the CMCase activity of both fungal cultures; overall, the enzyme activity of the Trichoderma consortium was significantly higher (∼1.3-fold) than that of P. chrysosporium (<a class="elsevierStyleCrossRef" href="#fig0020">Fig. 4</a>b).DiscussionMany microorganisms grow in the presence of pesticides, and this ability is influenced by chemical, physical, biochemical, and environmental conditions, and also depends on the amount and type of pesticides<a class="elsevierStyleCrossRef" href="#bib0430">36</a>. The initial fungal response to contaminants reflects the initial adaptation to stressful cultural conditions and/or to contaminated environments<a class="elsevierStyleCrossRef" href="#bib0350">20</a>. Synthetic pyrethroids (cypermethrin, deltamethrin, permethrin, and others) and carbamates such as propoxur may reduce the growth of bacteria and filamentous fungi such as T. viride, T. harzianum, and P. chrysosporium strains<a class="elsevierStyleCrossRefs" href="#bib0255">1,10,23,36,47</a>. Conversely to our results, Schumacher and Poheling did not find negative effects of permethrin on the growth of Metarhiziumanisopliae<a class="elsevierStyleCrossRef" href="#bib0425">35</a>. On the other hand, pyrethroids such as allethrin (50mg/l) did not affect the growth of Fusarium proliferatum CF2<a class="elsevierStyleCrossRef" href="#bib0270">4</a>. Consistently to our results, Deng et al. observed that pyrethroids such as β-cypermethrin (100mg/l) did not affect the final biomass produced by Aspergillus niger YAT; however, its radial growth was delayed<a class="elsevierStyleCrossRef" href="#bib0300">10</a>.The mixture of pyrethroids, β-cypermethrin, deltamethrin, fenvalerate, and α-cyhalothrin (100–1000mg/l), reduced the growth in T. viride and P.chrysosporium<a class="elsevierStyleCrossRef" href="#bib0430">36</a>. In soils, the application of cypermethrin and chlorpyrifos alone and in combination dramatically decreased both bacterial and fungal populations<a class="elsevierStyleCrossRef" href="#bib0445">39</a>. The latter indicates that microorganisms require a certain period of adaptation to toxic contaminants to produce those necessary molecules for tolerating such compounds<a class="elsevierStyleCrossRef" href="#bib0255">1</a>. In the present study, the commercial product has a mixture of two pyrethroids (permethrin, prallethrin) with carbamate (propoxur), and this combination exerts certain toxicity which significantly delayed the growth of all fungal strains. This effect could be due to the synergy between carbamates and pyrethroids by which the toxicity to microbes may increase<a class="elsevierStyleCrossRef" href="#bib0335">17</a>.Some studies have demonstrated the ability of Trichoderma strains for tolerating and growing in the presence of organic compounds such as petroleum hydrocarbons and pyrethroids<a class="elsevierStyleCrossRefs" href="#bib0260">2,6,36</a>. Furthermore, these fungi may use organic molecules as carbon and energy source since they have the enzymes necessary to perform such metabolism<a class="elsevierStyleCrossRefs" href="#bib0340">18,45</a>. The fungus identified as part of the genus Cladosporium was reported as tolerant to pyrethroids, including β-cypermethrin, deltamethrin, bifenthrin and permethrin (100mg/l)<a class="elsevierStyleCrossRef" href="#bib0290">8</a>. Other studies include fungi such as Aspergillus oryzae and Cunninghamella elegans, exposed to pyrethroids, cyhalothrin and 3-phenoxybenzoic acid, an intermediate in the degradation of permethrin<a class="elsevierStyleCrossRefs" href="#bib0405">31,49</a>.Consortium cultures are better than individual cultures because there are complementary physiological and biochemical functions among microorganisms, i.e., while some microorganisms perform specific enzymatic activity, other microorganisms can perform some different enzyme activities, by which all the involved organisms may be benefited<a class="elsevierStyleCrossRef" href="#bib0450">40</a>. Enzyme activities include superoxide dismutases (SOD), peroxidases (POXs), catalases (CAT), chitinases, glucanases, and many others.In nature, microorganisms coexist in consortia and interact with each other to transform organic materials<a class="elsevierStyleCrossRefs" href="#bib0380">26,40</a>. Artificial and natural microbial consortia are being studied for assessing tolerance, removal, and degradation of inorganic and organic compounds<a class="elsevierStyleCrossRef" href="#bib0450">40</a>. However, little attention is given to filamentous fungi and their tolerance to insecticides as accounted for bacteria<a class="elsevierStyleCrossRef" href="#bib0295">9</a>. Moreover, research about fungal consortia exposed to pyrethroids and carbamates utilized as substitutes for DDT is scant. Furthermore, many fungi may remove or degrade inorganic and organic compounds from polluted systems through several biochemical processes which include antioxidant molecules and enzymes such as POXs. In this regard, POXs have antioxidant activity and are involved in the detoxification of reactive oxygen species (ROS) such as H2O2 accumulation in cells because these enzymes oxidize H2O2 and are involved in the detoxification processes of organic pollutants<a class="elsevierStyleCrossRefs" href="#bib0345">19,46</a>. Other extracellular fungal POXs (lignin peroxidase, manganese peroxidase, and versatile peroxidase VP) are involved in the removal and degradation of pollutants such as polycyclic aromatic hydrocarbons (PAHs), dye-based textile effluents, polychlorinated biphenyls, fungicides, and pesticides<a class="elsevierStyleCrossRef" href="#bib0480">46</a>.Our results concur with those findings in white-rot fungi such as Polyporus tricholoma, Cilindrobasidium leave, and Deconica citrispora that increased POX activity (especially MnP) when exposed to paraquat, a widely applied herbicide in agriculture whose chemical structure resembles that of lignin<a class="elsevierStyleCrossRef" href="#bib0275">5</a>. In addition, P. chrysosporium can degrade a wide variety of organic pollutants due to the activity of non-specific extracellular POXs<a class="elsevierStyleCrossRef" href="#bib0370">24</a>. Furthermore, non-ligninolytic fungi such as Aspergillus, Fusarium, and Trichoderma may transform environmental pollutants such as PAHs, pesticides, and dyes, releasing POX enzymes<a class="elsevierStyleCrossRef" href="#bib0355">21</a>. Zhao et al. proposed that A. oryzae M4 uses some POXs in the presence of NADPH and O2, for degrading 3-phenoxybenzoic acid, a subproduct of permethrin degradation<a class="elsevierStyleCrossRef" href="#bib0490">48</a>. Trichoderma asperellum H15 was exposed to PAHs with 3–5 rings (phenanthrene, pyrene, and benzo[a]pyrene), and the fungal POX activity increased after 4 days of exposure<a class="elsevierStyleCrossRef" href="#bib0480">46</a>. Many POXs were identified in T. asperellum, including cytochrome C peroxidases, catalases, glutathione peroxidase, and dye-decolorizing peroxidases<a class="elsevierStyleCrossRef" href="#bib0480">46</a>. Most fungi, including P. chrysosporium and Trichoderma sp., are studied for degrading or removing PAHs, organochloride pesticides, organophosphates, carbamates, and pyrethroids such as β-cypermethrin and deltamethrin, by means of the oxidative effects of POXs<a class="elsevierStyleCrossRefs" href="#bib0305">11,12,24,43</a>. In our results, the POX activity detected in the Trichoderma consortium was higher than that of P. chrysosporium, which may be explained in part, by the fact that the Trichoderma consortium was integrated by four fungal strains, and thus, all strains may have released more POX enzymes.The studies of POXs involved in either the removal or degradation of pyrethroids such as permethrin and prallethrin, and carbamates such as propoxur, are still little explored. Our results suggest that the Trichoderma consortium and P. chrysosporium increase their POX activities for tolerating the commercial insecticide in liquid culture. However, further studies are needed to identify specific POXs that participate during this process, and to determine whether these enzymes act on both the degradation and detoxification of insecticides and byproducts, as well.On the other hand, chitinases play a key role in the transformation of chitin and are widely distributed in nature with a wider range of biotechnological applications, including the biocontrol of fungal phytopathogens, harmful insects, bioconversion of chitin wastes, to single-cell protein, biopesticides, among others<a class="elsevierStyleCrossRef" href="#bib0435">37</a>. Moreover, chitinases are important for maintaining the balance of carbon and nitrogen ratio in ecosystems<a class="elsevierStyleCrossRefs" href="#bib0385">27,32,37</a>. Regarding chitin degradation, the chitinase family includes three enzymes that act separately, (1) endochitinases that recognize o-glycosyl bonds between chito-saccharide residues for catalysis and produce multimers of oligosaccharides, especially diacetylchitobiose; (2) exochitinases that release soluble low molecular weight dimers, and (3) chitobiose that hydrolyses diacetylchitobiose to N-acetyl-glucosamine (GlcNAc)<a class="elsevierStyleCrossRef" href="#bib0455">41</a>. Both bacteria and fungi use chitin as a carbon and energy source, and the production of chitinolytic enzymes is related to carbon sources in synthetic culture media<a class="elsevierStyleCrossRefs" href="#bib0410">32,41</a>.Chitinases produced by Trichoderma correspond to enzymes that function as biological control agents and are responsible for the lysis and degradation of fungal cell walls and insect cuticles<a class="elsevierStyleCrossRef" href="#bib0330">16</a>. Furthermore, the exposure of Paenibacillus sp. to pyrethroids (cypermethrin) at concentrations recommended for field applications, caused the total inhibition of chitinase production, whereas insecticides such as methyl parathion and endosulfan significantly decreased (30–40%) the activity and stability of chitinases<a class="elsevierStyleCrossRef" href="#bib0440">38</a>. Organic molecules such as PAHs, with four or more aromatic rings, inhibited chitinase activities from Aeromonas hydrophila subsp. anaerogenes A52 and from T.harzianum<a class="elsevierStyleCrossRefs" href="#bib0395">29,41</a>. To our knowledge, GlcNAc-activity has not been reported as being involved in the removal or degradation of organic pollutants such as pyrethroid and carbamate insecticides; however, this enzyme may serve as a biomarker for assessing detoxification processes of systems polluted with these compounds.Endoglucanases (EGs) represent a group of dynamic cellulases that randomly attack internal O-glycosidic bonds of the cellulose chain, releasing glucan chains with different lengths, to generate new reducing and non-reducing ends; thus, EGs are the most important cellulases that contribute to the hydrolysis of cellulose<a class="elsevierStyleCrossRef" href="#bib0500">50</a>. EGs have many biotechnological applications for the industry, including animal food, textiles, laundry, pulp and paper, brewery and wine, food, and agriculture, among others. These enzymes are globally marketed from fungi such as Aspergillus and Trichoderma<a class="elsevierStyleCrossRef" href="#bib0265">3</a>.Overall, most studies are limited to reporting the degradation percentages of insecticides but not emphasizing the effects of insecticides on microbial biomolecules. The production of a high number of enzymes, and the optimal activity of these enzymes may depend on culture media and microorganisms. The use of pyrethroids and carbamates increased as a result of the prohibition of DDT, and these insecticides can disturb agricultural soils and may lead to several issues related to environmental and human health pollution. Furthermore, these organic chemicals may exert toxic effects on microorganisms and higher organisms. The present study highlights that a commercial organic pesticide based on pyrethroids and carbamates may inhibit both the growth of filamentous fungi and the activity of important fungal enzymes involved in either chitin or cellulose degradation.Overall, increasing the concentrations of the active ingredient of the commercial insecticide H24® decreased the radial growth rate in ten strains of Trichoderma sp. and P. chrysosporium. Four prominent strains of Trichoderma [T. koningii (Trich CP03), T. virens (Trich CP022), T. virens (Trich CP037), and T. atroviride (Trich CP0X)] were able to tolerate 200ppm of this commercial insecticide. These four fungal strains grew in a liquid culture medium contaminated with 100ppm of the commercial insecticide and showed increased protein production and high POX enzyme activity. Moreover, this commercial insecticide had negative effects on chitinase and endoglucanase activities derived from the Trichoderma consortium; therefore, it should be considered when using these microorganisms in combination with organic insecticides addressed to integrated pest management, and for assessing tolerance, detoxification, or degradation of organic insecticides based on permethrin, prallethrin and propoxur, for instance.Conflict of interestThe authors declare that they have no conflicts of interest." "textoCompletoSecciones" => array:1 [ "secciones" => array:12 [ 0 => array:3 [ "identificador" => "xres2109221" "titulo" => "Highlights" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:3 [ "identificador" => "xres2109223" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0010" ] ] ] 2 => array:2 [ "identificador" => "xpalclavsec1796971" "titulo" => "Keywords" ] 3 => array:3 [ "identificador" => "xres2109222" "titulo" => "Resumen" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0015" ] ] ] 4 => array:2 [ "identificador" => "xpalclavsec1796970" "titulo" => "Palabras clave" ] 5 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 6 => array:3 [ "identificador" => "sec0010" "titulo" => "Materials and methods" "secciones" => array:5 [ 0 => array:2 [ "identificador" => "sec0015" "titulo" => "Microbiological materials" ] 1 => array:2 [ "identificador" => "sec0020" "titulo" => "Chemical reagents and culture media" ] 2 => array:2 [ "identificador" => "sec0025" "titulo" => "Bioassay 1. Fungal growth and tolerance to increased concentrations of commercial insecticide" ] 3 => array:2 [ "identificador" => "sec0030" "titulo" => "Bioassay 2. Fungal protein content and induced peroxidase, chitinase, and glucanase activities in a liquid medium containing/contaminated with 100 ppm of commercial insecticide" ] 4 => array:2 [ "identificador" => "sec0035" "titulo" => "Statistical analysis" ] ] ] 7 => array:3 [ "identificador" => "sec0040" "titulo" => "Results" "secciones" => array:2 [ 0 => array:2 [ "identificador" => "sec0045" "titulo" => "Bioassay 1. Fungal growth and tolerance to three concentrations of commercial insecticide" ] 1 => array:2 [ "identificador" => "sec0050" "titulo" => "Bioassay 2. Fungal growth, protein content, and induced peroxidase, chitinase, and glucanase activities in a liquid medium containing 100 mg/l of commercial insecticide" ] ] ] 8 => array:2 [ "identificador" => "sec0055" "titulo" => "Discussion" ] 9 => array:2 [ "identificador" => "sec0060" "titulo" => "Conflict of interest" ] 10 => array:2 [ "identificador" => "xack734799" "titulo" => "Acknowledgments" ] 11 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2022-07-13" "fechaAceptado" => "2023-06-13" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec1796971" "palabras" => array:6 [ 0 => "Permethrin" 1 => "Prallethrin" 2 => "Propoxur" 3 => "Peroxidases" 4 => "Chitinases" 5 => "Endoglucanases" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec1796970" "palabras" => array:6 [ 0 => "Permetrina" 1 => "Praletrina" 2 => "Propoxur" 3 => "Peroxidasas" 4 => "Quitinasas" 5 => "Endoglucanasas" ] ] ] ] "tieneResumen" => true "highlights" => array:2 [ "titulo" => "Highlights" "resumen" => "<ul class="elsevierStyleList" id="lis0005"><li class="elsevierStyleListItem" id="lsti0005">•Trichoderma spp. strains tolerate 200ppm of pyrethroids and carbamate insecticides.</li><li class="elsevierStyleListItem" id="lsti0010">•Trichoderma spp. consortium growth in liquid culture with 100ppm of insecticide.</li><li class="elsevierStyleListItem" id="lsti0015">•Insecticide promotes the release of proteins and peroxidases by Trichoderma spp.</li><li class="elsevierStyleListItem" id="lsti0020">•Insecticide decreases chitinase and endoglucanase produced by Trichoderma spp.</li></ul>" ] "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "The application of pyrethroids and carbamates represents an environmental risk and may exert adverse effects on beneficial microorganisms such as Trichoderma, which contribute to the biocontrol of several fungal phytopathogens. This research evaluated the tolerance of several strains of Trichoderma to a selected culture medium contaminated with a commercial insecticide (H24®) composed of pyrethroids, permethrin and prallethrin, and carbamate propoxur, and determined the influence of this insecticide on the release of enzymes such as chitinases, peroxidases, and endoglucanases by a consortium of selected Trichoderma strains grown in liquid culture medium. Four out of 10 Trichoderma strains showed tolerance to 200ppm (∼48.3% of growth) of the commercial insecticide after 96h of exposure to a contaminated solid medium. After eight days of growth in liquid culture, the insecticide enhanced extracellular protein content and peroxidase activities in the Trichoderma consortium but decreased both chitinase and glucanase activities. These fungal responses should be considered when implementing strategies that combine alternative pesticides and fungal biocontrollers for managing fungal phytopathogens." ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "La aplicación de piretroides y carbamatos representa un riesgo ambiental y puede ejercer efectos adversos sobre microorganismos benéficos, como el Trichoderma, que contribuyen al biocontrol de varios fitopatógenos. Por un lado, esta investigación evaluó la tolerancia de varias cepas de Trichoderma a un medio de cultivo sólido contaminado con un insecticida comercial (H24®) compuesto por piretroides (permetrina y praletrina) y carbamato propoxur; por el otro, determinó la influencia de este insecticida en la liberación de enzimas como quitinasas, peroxidasas y endoglucanasas por un consorcio de cepas seleccionadas de Trichoderma cultivadas en medio líquido. Cuatro de 10 cepas de Trichoderma mostraron tolerancia a 200 ppm (∼48,3% de crecimiento) del insecticida comercial después de 96 horas en un medio sólido contaminado. Tras ocho días de crecimiento en cultivo líquido, el insecticida aumentó el contenido de proteínas y la actividad peroxidasa del consorcio Trichoderma, pero redujo las actividades quitinasa y glucanasa. Estas respuestas fúngicas podrían ser consideradas al implementar estrategias para el biocontrol y el manejo de hongos fitopatógenos." ] ] "multimedia" => array:5 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 3792 "Ancho" => 3341 "Tamanyo" => 392177 ] ] "descripcion" => array:1 [ "en" => "Growth rate of Trichoderma strains and Phanerochaete chrysosporium-ATCC 34540 in solid medium (PDA) with (a) 0mg/l, (b) 50mg/l, (c) 100mg/l, (d) 150mg/l, and (e) 200mg/l of commercial insecticide H24® with three active ingredients (permethrin, prallethrin, and propoxur). Means±standard error (n=4)." ] ] 1 => array:7 [ "identificador" => "fig0010" "etiqueta" => "Figure 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 2895 "Ancho" => 2091 "Tamanyo" => 275621 ] ] "descripcion" => array:1 [ "en" => "(a) Radial growth rate (mm/h) and (b) radial growth rate inhibition (RGRI%) of Trichoderma strains and Phanerochaete chrysosporium-ATCC34540 in solid medium (PDA) with 0, 50, 100, 150, and 200mg/l of commercial insecticide H24® with three active ingredients (permethrin, prallethrin, and propoxur). Means±standard error (n=4)." ] ] 2 => array:7 [ "identificador" => "fig0015" "etiqueta" => "Figure 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr3.jpeg" "Alto" => 2663 "Ancho" => 1675 "Tamanyo" => 119116 ] ] "descripcion" => array:1 [ "en" => "(a) Biomass (DWg), (b) extracellular protein content (μg/l), and (c) extracellular peroxidase activity (POX activity, U/μg protein) of Trichoderma sp. and P. chrysosporium-ATCC 34540 in liquid culture in the absence (SC) and presence (SC+I) of sub-ID50 (100mg/l) of commercial insecticide H24® with three active ingredients (permethrin, prallethrin and propoxur), after 8 days in liquid culture. Different letters indicate significant differences among means for medium culture; asterisks indicate significant differences among means for microorganisms (Tukey, α=0.05). Means±standard error (n=4)." ] ] 3 => array:7 [ "identificador" => "fig0020" "etiqueta" => "Figure 4" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr4.jpeg" "Alto" => 2343 "Ancho" => 2091 "Tamanyo" => 122620 ] ] "descripcion" => array:1 [ "en" => "(a) Chitinase activity (GlcNAc, U/mg protein) and (b) endoglucanase activity (CMCase, U/μg protein) of Trichoderma sp. and P. chrysosporium-ATCC 34540 in liquid culture in the absence (SC) and presence (SC+I) of sub-ID50 (100mg/l) of commercial insecticide H24® with three active ingredients (permethrin, prallethrin, and propoxur), after 8 days in liquid culture. Different letters indicate significant differences among means for medium culture; the asterisk indicates significant differences among means for microorganisms (Tukey, α=0.05). Means±standard error (n=4)." ] ] 4 => array:8 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at1" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:2 [ "leyenda" => "Active ingredients in the commercial product (H24®) are permethrin, prallethrin, and propoxur. Means±standard error (n=4)." "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Fungal strain \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">ID50 (mg/l) of commercial insecticide \t\t\t\t\t\t\n \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Trich CP01 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">104.34±1.47 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Trich CP03 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">131.64±15.80 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Trich CP04 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">107.66±3.56 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Trich CP022 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">143.76±3.45 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Trich CP023 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">77.27±0.99 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Trich CP037 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">219.04±3.16 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Trich CP038 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">91.59±2.15 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Trich CP056 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">87.32±4.58 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Trich CP0X \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">167.10±8.82 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Trich CP0TGC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">85.58±0.32 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">P. chrysosporium-ATCC 34540 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">134.61±1.34 \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab3489002.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Inhibitory dose 50 (ID50) of commercial insecticide H24® with three active ingredients (permethrin, prallethrin, and propoxur) on the growth rate of ten strains of Trichoderma sp. and Phanerochaete chrysosporium-ATCC 34540 grown on solid culture medium." ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0015" "bibliografiaReferencia" => array:50 [ 0 => array:3 [ "identificador" => "bib0255" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "A study on biodegradation of propoxur by bacteria isolated from municipal solid waste" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:5 [ 0 => "J. 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Crecimiento, tolerancia y actividades enzimáticas de cepas de Trichoderma en medios de cultivo adicionados con un insecticida a base de piretroides

Caliope Mendarte-Alquisira, Alejandro Alarcón, Ronald Ferrera-Cerrato

Corresponding author

rferreracerrato@gmail.com

Corresponding author.

Área de Microbiología, Posgrado de Edafología, Colegio de Postgraduados, Carretera Federal México-Texcoco km 36.5, Montecillo 56264, Estado de México, Mexico

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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Introduction</span><p id="par0025" class="elsevierStylePara elsevierViewall">After the prohibition of using the highly toxic and persistent dichloro diphenyl trichloroethane &#40;DDT&#41;&#44; alternate insecticides based on carbamates and pyrethroids &#40;single or combined&#41; began to be utilized for controlling insect pests<a class="elsevierStyleCrossRef" href="#bib0335"><span class="elsevierStyleSup">17</span></a>&#46; However&#44; these insecticides may also represent potential issues for human and environmental health<a class="elsevierStyleCrossRef" href="#bib0485"><span class="elsevierStyleSup">47</span></a>&#46; Some carbamates such as propoxur or pyrethroids such as permethrin and prallethrin may have carcinogenic and mutagenic properties&#44; and inflammatory effects in the stomach&#59; in addition&#44; they are also associated with alterations in functional sodium channels and poor motor development in children<a class="elsevierStyleCrossRefs" href="#bib0375"><span class="elsevierStyleSup">25&#44;30&#44;44</span></a>&#46; Furthermore&#44; several studies reported the effect of carbamates and pyrethroids on beneficial bacteria and communities in the rhizosphere<a class="elsevierStyleCrossRefs" href="#bib0300"><span class="elsevierStyleSup">10&#44;35&#44;36&#44;38&#44;47</span></a>&#46; Therefore&#44; research focused on improving strategies for integrated pest management&#44; which includes the combination of organically-derived pesticides and the application of antagonist microorganisms to reduce chemical damage induced by insecticides in the environment<a class="elsevierStyleCrossRef" href="#bib0440"><span class="elsevierStyleSup">38</span></a>&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Trichoderma</span> genus includes worldwide ubiquitous fungi commonly found in soils and possesses a powerful and versatile enzymatic machinery &#40;including cellulases&#44; chitinases&#44; peroxidases&#44; and proteases&#44; among others&#41; which may degrade a wide range of organic recalcitrant compounds in soil<a class="elsevierStyleCrossRefs" href="#bib0265"><span class="elsevierStyleSup">3&#44;29&#44;41</span></a>&#46; Commonly&#44; <span class="elsevierStyleItalic">Trichoderma</span> is one of the widest fungi directed to control plant pathogens since they produce enzymes with hydrolytic capacity and secondary metabolites related to processes such as antibiosis&#44; space competition&#44; plant growth improvement&#44; and resistance against biotic and abiotic stresses<a class="elsevierStyleCrossRefs" href="#bib0385"><span class="elsevierStyleSup">27&#44;32&#44;37</span></a>&#46; Furthermore&#44; <span class="elsevierStyleItalic">Trichoderma</span> spp&#46; are tolerant to many agrochemicals and have the potential to degrade chemical pesticides because they possess specific enzymes to metabolize such compounds<a class="elsevierStyleCrossRef" href="#bib0290"><span class="elsevierStyleSup">8</span></a>&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">Therefore&#44; the aims of this research were &#40;1&#41; to determine the tolerance of several strains of <span class="elsevierStyleItalic">Trichoderma</span> to solid culture medium contaminated with commercial insecticide H24&#174; &#40;composed of pyrethroids&#44; permethrin and prallethrin&#44; and carbamate propoxur&#41; and &#40;2&#41; to evaluate the effect of this insecticide on the release of enzymes such as chitinases&#44; peroxidases&#44; and endoglucanases by selected <span class="elsevierStyleItalic">Trichoderma</span> strains grown in liquid culture medium&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Materials and methods</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Microbiological materials</span><p id="par0040" class="elsevierStylePara elsevierViewall">This research utilized ten strains of <span class="elsevierStyleItalic">Trichoderma</span>&#58; Trich CP01 &#40;<span class="elsevierStyleItalic">T&#46; virens</span>&#41;&#44; Trich CP03 &#40;<span class="elsevierStyleItalic">T&#46; koningii</span>&#41;&#44; Trich CP04 &#40;<span class="elsevierStyleItalic">T&#46; viride</span>&#41;&#44; Trich CP022 &#40;<span class="elsevierStyleItalic">T&#46; virens</span>&#41;&#44; Trich CP023 &#40;<span class="elsevierStyleItalic">T&#46; koningii</span>&#41;&#44; Trich CP037 &#40;<span class="elsevierStyleItalic">T&#46; virens</span>&#41; Trich CP038 &#40;<span class="elsevierStyleItalic">T&#46; harzianum</span>&#41;&#44; Trich CP056 &#40;<span class="elsevierStyleItalic">T&#46; viride</span>&#41;&#44; Trich CP0X &#40;<span class="elsevierStyleItalic">T&#46; atroviride</span>&#41;&#44; Trich CP0TGC &#40;<span class="elsevierStyleItalic">T&#46; viride</span>&#41;&#44; and one strain of <span class="elsevierStyleItalic">Phanerochaete chrysosporium</span>-ATCC 34540 &#40;CDBB 686&#41; as referential fungus able to degrade toxic organic contaminants&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">All <span class="elsevierStyleItalic">Trichoderma</span> strains are part of the microbial collection of the Microbiology Laboratory &#40;Colegio de Postgraduados&#41;&#44; which were reported as tolerant to crude oil&#44; and to high concentrations of naphthalene&#44; phenanthrene&#44; and benzo&#91;<span class="elsevierStyleItalic">a</span>&#93;pyrene<a class="elsevierStyleCrossRef" href="#bib0260"><span class="elsevierStyleSup">2</span></a>&#46; The strain of <span class="elsevierStyleItalic">P&#46; chrysosporium</span>-ATCC 34540 &#40;CDBB 686&#41; was acquired from the CINVESTAV microbial repository and reported as tolerant and degrader of persistent organic pollutants&#44; including insecticides<a class="elsevierStyleCrossRef" href="#bib0370"><span class="elsevierStyleSup">24</span></a>&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Chemical reagents and culture media</span><p id="par0050" class="elsevierStylePara elsevierViewall">The commercial insecticide H24&#174; contains permethrin &#40;360<span class="elsevierStyleHsp" style=""></span>mg&#47;kg&#41;&#44; propoxur &#40;890<span class="elsevierStyleHsp" style=""></span>mg&#47;kg&#41; and prallethrin &#40;50<span class="elsevierStyleHsp" style=""></span>mg&#47;kg&#41; as active ingredients&#59; thus&#44; the total of active ingredients yields up to 1300<span class="elsevierStyleHsp" style=""></span>mg&#47;kg&#44; which are dissolved in an organic solvent&#46; This commercial insecticide is commonly applied for controlling flying and crawling insects that attack cotton crops due to its active ingredient permethrin&#46; Potato dextrose agar &#40;PDA&#41; medium &#40;BD Bioxon&#174;&#41; was prepared according to the manufacturer&#39;s specifications and different concentrations of the commercial insecticide &#40;0&#44; 50&#44; 100&#44; 150&#44; and 200<span class="elsevierStyleHsp" style=""></span>ppm&#41; were added to it&#46;</p><p id="par0055" class="elsevierStylePara elsevierViewall">The liquid culture consisted of a mineral medium &#40;MM&#41; prepared in accordance with Gao et al&#46; with some modifications<a class="elsevierStyleCrossRef" href="#bib0315"><span class="elsevierStyleSup">13</span></a>&#46; The MM contained &#40;g&#47;l&#41;&#58; 1&#46;0 K<span class="elsevierStyleInf">2</span>HPO<span class="elsevierStyleInf">4</span>&#44; 0&#46;5 KCl&#44; 0&#46;5 MgSO<span class="elsevierStyleInf">4</span>&#183;7H<span class="elsevierStyleInf">2</span>O&#44; 0&#46;01 FeSO<span class="elsevierStyleInf">4</span>&#44; pH 7&#46;0&#46; The nitrogen source was meat peptone &#40;CAS 91079-38-8&#44; Merck&#41;&#44; considering a nitrogen content of &#8764;12&#46;5&#37; and nitrogen in the insecticide &#40;propoxur&#41;&#44; the carbon source was sucrose and that carbon derived from the insecticide&#46; The final C&#47;N ratio was &#8764;20&#47;1&#44; considering 100<span class="elsevierStyleHsp" style=""></span>ppm of active ingredients &#40;permethrin&#44; prallethrin&#44; and propoxur&#41; in commercial insecticide H24&#174;&#46; Both media were autoclaved at 121<span class="elsevierStyleHsp" style=""></span>&#176;C for 15<span class="elsevierStyleHsp" style=""></span>min&#59; afterwards&#44; the H24&#174; insecticide was added using filtration&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Bioassay 1&#46; Fungal growth and tolerance to increased concentrations of commercial insecticide</span><p id="par0060" class="elsevierStylePara elsevierViewall">Agar disks of 5<span class="elsevierStyleHsp" style=""></span>mm in diameter with fungal mycelium were sown in Petri dishes containing solid PDA medium with or without the commercial insecticide &#40;four replicates per treatment&#41;&#59; all fungal cultures were incubated at 28<span class="elsevierStyleHsp" style=""></span>&#176;C for 96<span class="elsevierStyleHsp" style=""></span>h&#46; The growth diameter was measured every 24<span class="elsevierStyleHsp" style=""></span>h&#44; for 4 days&#46; The results were used to estimate the radial growth&#44; radial growth rate&#44; radial growth rate inhibition &#40;&#37;&#41; &#40;RGRI&#37;&#41;&#44; and the inhibitory dose 50 &#40;ID<span class="elsevierStyleInf">50</span>&#41;<a class="elsevierStyleCrossRefs" href="#bib0390"><span class="elsevierStyleSup">28&#44;34</span></a>&#46; The radial growth rate was calculated with the quadratic equation that was fitted to the dose&#8211;response curve for each strain&#46; The radial growth rate was used to estimate the &#40;ID<span class="elsevierStyleInf">50</span>&#41; for each strain and the RGRI&#37;<a class="elsevierStyleCrossRefs" href="#bib0390"><span class="elsevierStyleSup">28&#44;34</span></a>&#46; The ID<span class="elsevierStyleInf">50</span> was also utilized as a reference to define a sub-ID<span class="elsevierStyleInf">50</span> without inhibiting the growth and further estimations<a class="elsevierStyleCrossRef" href="#bib0415"><span class="elsevierStyleSup">33</span></a>&#46;</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Bioassay 2&#46; Fungal protein content and induced peroxidase&#44; chitinase&#44; and glucanase activities in a liquid medium containing&#47;contaminated with 100<span class="elsevierStyleHsp" style=""></span>ppm of commercial insecticide</span><p id="par0065" class="elsevierStylePara elsevierViewall">Four tolerant strains of <span class="elsevierStyleItalic">Trichoderma</span> sp&#46; &#40;a consortium of <span class="elsevierStyleItalic">Trichoderma</span> sp&#46;&#41; selected from Bioassay 1&#44; and <span class="elsevierStyleItalic">P&#46; chrysosporium</span>-ATCC 34540 were used for evaluating the effect of a sub-ID<span class="elsevierStyleInf">50</span> of commercial insecticide H24&#174; on the enzymatic activities of interest&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall">The initial fungal inoculum was adjusted for applying 1<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">6</span> spores ml of the <span class="elsevierStyleItalic">Trichoderma</span> consortium &#40;adding the same number of spores per each fungal strain&#41;&#44; and 1<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">6</span> spores ml of <span class="elsevierStyleItalic">P&#46; chrysosporium</span>-ATCC 34540&#46; Fungal cultures were maintained for 8 days at 200<span class="elsevierStyleHsp" style=""></span>rpm and 28<span class="elsevierStyleHsp" style=""></span>&#176;C&#46; Afterwards&#44; protein analysis and enzyme tests were performed&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall">Protein content was determined with the Biuret method by using bovine albumin as standard<a class="elsevierStyleCrossRef" href="#bib0320"><span class="elsevierStyleSup">14</span></a>&#46; The reaction mixture contained 100<span class="elsevierStyleHsp" style=""></span>&#956;l of fungal supernatant and 1000<span class="elsevierStyleHsp" style=""></span>&#956;l of Biuret reagent&#46; This mixture was incubated for 30<span class="elsevierStyleHsp" style=""></span>min at room temperature &#40;20&#8211;25<span class="elsevierStyleHsp" style=""></span>&#176;C&#41;&#46; Then&#44; absorbance readings at 540<span class="elsevierStyleHsp" style=""></span>nm were taken by using a spectrophotometer &#40;Synergy 2&#44; Biotek&#174;&#41;&#46;</p><p id="par0080" class="elsevierStylePara elsevierViewall">Non-specific peroxidase &#40;POX&#44; EC 1&#46;11&#46;1&#46;7&#41; activity was measured in 96-well microplates by mixing 20<span class="elsevierStyleHsp" style=""></span>&#956;l of the fungal supernatant with 190<span class="elsevierStyleHsp" style=""></span>&#956;l of phosphate buffer &#40;50<span class="elsevierStyleHsp" style=""></span>mM&#44; pH 7&#46;0&#41;&#44; 10<span class="elsevierStyleHsp" style=""></span>&#956;l of guaiacol 1&#37;&#44; and 20<span class="elsevierStyleHsp" style=""></span>&#956;l of H<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">2</span> in phosphate buffer &#40;50<span class="elsevierStyleHsp" style=""></span>mM&#44; pH 7&#46;0&#41;&#46; Absorbance readings at 450<span class="elsevierStyleHsp" style=""></span>nm were taken from this mixture every 15<span class="elsevierStyleHsp" style=""></span>s for 5<span class="elsevierStyleHsp" style=""></span>min&#44; by using a spectrophotometer &#40;Synergy 2&#44; Biotek&#174;&#41;&#46; POX activity was calculated using a molar extinction coefficient &#40;<span class="elsevierStyleItalic">&#603;</span>&#41; of 16&#46;8&#47;mM<span class="elsevierStyleHsp" style=""></span>cm&#46; One unit of POX activity is defined as the amount of enzyme that catalyzes the formation of 1<span class="elsevierStyleHsp" style=""></span>&#956;mol of tetraguaiacol per min at 25<span class="elsevierStyleHsp" style=""></span>&#176;C and pH 7&#46;0<a class="elsevierStyleCrossRef" href="#bib0285"><span class="elsevierStyleSup">7</span></a>&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">Chitinase activity &#40;GlcNAc activity&#41; was measured by using the method proposed by Vargas-Hoyos and Gilchrist-Ramelli&#44; using N-acetyl-<span class="elsevierStyleSmallCaps">d</span>-glucosamine &#40;GlcNAc&#41; as standard<a class="elsevierStyleCrossRefs" href="#bib0360"><span class="elsevierStyleSup">22&#44;42</span></a>&#46; Thus&#44; 500<span class="elsevierStyleHsp" style=""></span>&#956;l of fungal supernatant was mixed with 100<span class="elsevierStyleHsp" style=""></span>&#956;l of colloidal chitin in sodium citrate buffer &#40;50<span class="elsevierStyleHsp" style=""></span>mM&#44; pH 5&#46;2&#41;&#44; and incubated for 30<span class="elsevierStyleHsp" style=""></span>min at 40<span class="elsevierStyleHsp" style=""></span>&#176;C&#59; then&#44; the mixture was cooled at ambient temperature &#40;20&#8211;25<span class="elsevierStyleHsp" style=""></span>&#176;C&#41;&#44; and 2000<span class="elsevierStyleHsp" style=""></span>&#956;l of dinitrosalicylic acid &#40;DNS&#41; were added&#44; for further incubation at 90<span class="elsevierStyleHsp" style=""></span>&#176;C for 5<span class="elsevierStyleHsp" style=""></span>min&#46; The reaction mixture was cooled with iced water&#44; and absorbance readings were measured at 540<span class="elsevierStyleHsp" style=""></span>nm in a Synergy 2&#44; Biotek&#174; spectrophotometer&#46; One unit of GlcNAc activity was defined as the amount of the enzyme necessary to liberate 1<span class="elsevierStyleHsp" style=""></span>&#956;mol&#47;min of reducing sugar &#40;glucose&#41;&#46; Enzyme activity was expressed in units per mg of protein&#46;</p><p id="par0090" class="elsevierStylePara elsevierViewall">&#946;-1&#44;4-Glucanase activity &#40;CMCase activity&#41; was quantified by the DNS technique using <span class="elsevierStyleSmallCaps">d</span>-glucose as standard<a class="elsevierStyleCrossRefs" href="#bib0325"><span class="elsevierStyleSup">15&#44;22</span></a>&#46; The reaction mixture consisted of 500<span class="elsevierStyleHsp" style=""></span>&#956;l of carboxymethyl cellulose &#40;2&#37;&#41; in sodium citrate buffer &#40;50<span class="elsevierStyleHsp" style=""></span>mM&#44; pH 4&#46;8&#41; and 500<span class="elsevierStyleHsp" style=""></span>&#956;l of fungal supernatant&#46; The mixture was incubated for 30<span class="elsevierStyleHsp" style=""></span>min at 50<span class="elsevierStyleHsp" style=""></span>&#176;C and cooled at room temperature&#46; Then&#44; 5000<span class="elsevierStyleHsp" style=""></span>&#956;l of DNS solution was added and incubated at 90<span class="elsevierStyleHsp" style=""></span>&#176;C for 5<span class="elsevierStyleHsp" style=""></span>min&#59; the reaction was stopped by adding iced water&#46; Absorbance readings were taken at 540<span class="elsevierStyleHsp" style=""></span>nm in a spectrophotometer &#40;Synergy 2&#44; Biotek&#174;&#41;&#46; One unit of CMCase activity was defined as the amount of the enzyme necessary to liberate 1<span class="elsevierStyleHsp" style=""></span>&#956;mol&#47;min of glucose&#44; and the enzyme activity was expressed in terms of units per mg of protein&#46;</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Statistical analysis</span><p id="par0095" class="elsevierStylePara elsevierViewall">Data were analyzed by one-way ANOVA and by the mean comparison test &#40;Tukey&#44; <span class="elsevierStyleItalic">&#945;</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41;&#46; Data represents the values of the means<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>standard error &#40;SE&#41;&#44; from four replicates for each treatment&#46; Analyses were performed using SPSS software&#44; version PASW 18 &#40;IBM SPSS-IBM Corp&#41;&#46;</p></span></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Results</span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Bioassay 1&#46; Fungal growth and tolerance to three concentrations of commercial insecticide</span><p id="par0100" class="elsevierStylePara elsevierViewall">In general&#44; all <span class="elsevierStyleItalic">Trichoderma</span> strains tolerated the presence of the commercial insecticide H24&#174; when applied at 50&#44; 100&#44; and 150<span class="elsevierStyleHsp" style=""></span>ppm&#46; Nevertheless&#44; the strains CP01 &#40;<span class="elsevierStyleItalic">Trichoderma virens</span>&#41;&#44; CP04 &#40;<span class="elsevierStyleItalic">T&#46; viride</span>&#41;&#44; CP038 &#40;<span class="elsevierStyleItalic">T&#46; harzianum</span>&#41;&#44; CP056 &#40;<span class="elsevierStyleItalic">T&#46; viride</span>&#41;&#44; and CP0TGC &#40;<span class="elsevierStyleItalic">T&#46; viride</span>&#41; stopped their growth after 72<span class="elsevierStyleHsp" style=""></span>h of exposure to 150<span class="elsevierStyleHsp" style=""></span>ppm of the commercial insecticide &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Figs&#46; 1b&#8211;d</a>&#41;&#46; Only four <span class="elsevierStyleItalic">Trichoderma</span> strains &#40;CP03 <span class="elsevierStyleItalic">T&#46; koningii</span>&#44; CP022 <span class="elsevierStyleItalic">T&#46; virens</span>&#44; CP037 <span class="elsevierStyleItalic">T&#46; virens</span>&#44; and CP0X <span class="elsevierStyleItalic">T&#46; atroviride</span>&#41; tolerated the application of the insecticide at 200<span class="elsevierStyleHsp" style=""></span>ppm &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>e&#41;&#46; Fungal adaptation to the insecticide occurred after 24<span class="elsevierStyleHsp" style=""></span>h when all <span class="elsevierStyleItalic">Trichoderma</span> strains exposed to 50&#44; 100&#44; 150&#44; and 200<span class="elsevierStyleHsp" style=""></span>ppm showed visible mycelial growth &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Figs&#46; 1b&#8211;e</a>&#41;&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0105" class="elsevierStylePara elsevierViewall">The growth rate of <span class="elsevierStyleItalic">Trichoderma</span> strains and <span class="elsevierStyleItalic">P&#46; chrysosporium</span>-ATCC 34540 in a solid medium &#40;PDA&#41; containing 0&#44; 50&#44; 100&#44; 150&#44; and 200<span class="elsevierStyleHsp" style=""></span>ppm of active ingredients &#40;permethrin&#44; prallethrin&#44; and propoxur&#41; of the commercial insecticide was determined&#46; The tested concentrations had a negative effect on the radial growth rate of all <span class="elsevierStyleItalic">Trichoderma</span> strains and <span class="elsevierStyleItalic">P&#46; chrysosporium</span>-ATCC 34540 when compared to their respective control without insecticide&#46; The radial growth rate achieved at 150<span class="elsevierStyleHsp" style=""></span>ppm oscillated between &#8764;0&#46;50 and &#8764;0&#46;09<span class="elsevierStyleHsp" style=""></span>mm&#47;h&#44; while the radial growth rate for tolerant strains at 200<span class="elsevierStyleHsp" style=""></span>ppm was between &#8764;0&#46;53 and &#8764;0&#46;17<span class="elsevierStyleHsp" style=""></span>mm&#47;h &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>a&#41;&#46; Trich CP037 &#40;<span class="elsevierStyleItalic">T&#46; virens</span>&#41; showed the lowest radial growth rate when exposed to 200<span class="elsevierStyleHsp" style=""></span>ppm of the commercial insecticide &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0110" class="elsevierStylePara elsevierViewall">Data from radial growth rate and radial growth rate inhibition &#40;&#37;&#41; were used to obtain the inhibitory dose 50 &#40;ID<span class="elsevierStyleInf">50</span>&#41; of the commercial insecticide &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; ID<span class="elsevierStyleInf">50</span> showed variations among all fungal strains&#46; The values of the ID<span class="elsevierStyleInf">50</span> for those tolerant strains &#40;Trich CP01&#59; Trich CP04&#59; Trich CP023&#59; Trich CP038&#59; Trich CP056&#59; Trich CP0TGC&#41; exposed to 150<span class="elsevierStyleHsp" style=""></span>ppm ranged from 77&#46;27 to 107&#46;66<span class="elsevierStyleHsp" style=""></span>ppm&#46; Moreover&#44; the values of the ID<span class="elsevierStyleInf">50</span> for those tolerant strains &#40;Trich CP03&#59; Trich CP022&#59; Trich CP037&#59; Trich CP0X&#59; and <span class="elsevierStyleItalic">P&#46; chrysosporium</span>-ATCC 34540&#41; exposed to 200<span class="elsevierStyleHsp" style=""></span>ppm ranged between 131&#46;64 and 219&#46;04<span class="elsevierStyleHsp" style=""></span>ppm&#59; of these strains&#44; Trich CP037 showed the highest ID<span class="elsevierStyleInf">50</span> value &#40;219&#46;04<span class="elsevierStyleHsp" style=""></span>ppm&#41; when compared to that from <span class="elsevierStyleItalic">P&#46; chrysosporium</span>-ATCC 34540 &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0115" class="elsevierStylePara elsevierViewall">In addition&#44; ID<span class="elsevierStyleInf">50</span> was used for a proposed sub-ID<span class="elsevierStyleInf">50</span> for those fungal strains that tolerated 200<span class="elsevierStyleHsp" style=""></span>ppm of the commercial insecticide&#46; This sub-ID<span class="elsevierStyleInf">50</span> was utilized for Bioassay 2 to determine the enzyme activities from a <span class="elsevierStyleItalic">Trichoderma</span> sp&#46; consortium and <span class="elsevierStyleItalic">P&#46; chrysosporium</span>-ATCC 34540&#46;</p></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Bioassay 2&#46; Fungal growth&#44; protein content&#44; and induced peroxidase&#44; chitinase&#44; and glucanase activities in a liquid medium containing 100<span class="elsevierStyleHsp" style=""></span>mg&#47;l of commercial insecticide</span><p id="par0120" class="elsevierStylePara elsevierViewall">The <span class="elsevierStyleItalic">Trichoderma</span> consortium &#91;Trich CP03 &#40;<span class="elsevierStyleItalic">T&#46; koningii</span>&#41;&#44; Trich CP022 &#40;<span class="elsevierStyleItalic">T&#46; virens</span>&#41;&#44; Trich CP037 &#40;<span class="elsevierStyleItalic">T&#46; virens</span>&#41;&#44; and Trich CP0X &#40;<span class="elsevierStyleItalic">T&#46; atroviride</span>&#41;&#93;&#44; and <span class="elsevierStyleItalic">P&#46; chrysosporium</span>-ATCC 34540&#44; were exposed to 100<span class="elsevierStyleHsp" style=""></span>ppm of the active ingredient of the commercial insecticide&#46; After eight days&#44; either the <span class="elsevierStyleItalic">Trichoderma</span> sp&#46; consortium or <span class="elsevierStyleItalic">P&#46; chrysosporium</span> grew and released proteins and enzymes into the contaminated liquid culture &#40;<a class="elsevierStyleCrossRefs" href="#fig0015">Figs&#46; 3 and 4</a>&#41;&#46;</p><elsevierMultimedia ident="fig0015"></elsevierMultimedia><elsevierMultimedia ident="fig0020"></elsevierMultimedia><p id="par0125" class="elsevierStylePara elsevierViewall">In the present study&#44; we observed that the growth of the <span class="elsevierStyleItalic">Trichoderma</span> consortium and <span class="elsevierStyleItalic">P&#46; chrysosporium</span> was not affected by the active ingredients contained in the commercial insecticide &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>a&#41;&#46; However&#44; in the absence and presence of insecticides&#44; the biomass of the <span class="elsevierStyleItalic">Trichoderma</span> sp&#46; consortium was significantly higher &#40;&#8764;7-fold&#41; than that of <span class="elsevierStyleItalic">P&#46; chrysosporium</span>&#46;</p><p id="par0130" class="elsevierStylePara elsevierViewall">The strain of <span class="elsevierStyleItalic">P&#46; chrysosporium</span>-ATCC 34540 produced more protein than the <span class="elsevierStyleItalic">Trichoderma</span> consortium in the absence or presence of the insecticide&#46; The insecticide significantly influenced the protein production in the <span class="elsevierStyleItalic">Trichoderma</span> consortium and <span class="elsevierStyleItalic">P&#46; chrysosporium</span>&#44; whose protein content increased by &#8764;1&#46;3-fold under the contaminated culture &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>b&#41;&#46;</p><p id="par0135" class="elsevierStylePara elsevierViewall">On the other hand&#44; without the insecticide&#44; the <span class="elsevierStyleItalic">Trichoderma</span> consortium had significantly higher &#40;&#8764;1&#46;8-fold&#41; POX activity than <span class="elsevierStyleItalic">P&#46; chrysosporium</span>&#44; reaching levels of &#8764;6000<span class="elsevierStyleHsp" style=""></span>U&#47;&#956;g protein when compared to <span class="elsevierStyleItalic">P&#46; chrysosporium</span> &#40;&#8764;3250<span class="elsevierStyleHsp" style=""></span>U&#47;&#956;g protein&#41; &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>c&#41;&#46; Under insecticide contamination&#44; POX activity increased in both fungal cultures&#59; for the <span class="elsevierStyleItalic">Trichoderma</span> consortium&#44; an increase of POX was achieved &#40;&#8764;1&#46;4-fold&#41;&#44; whereas for <span class="elsevierStyleItalic">P&#46; chrysosporium</span> the increase of POX was about &#8764;2&#46;1-fold than that of the respective control in the absence of the insecticide&#46; Overall&#44; the POX activity of the <span class="elsevierStyleItalic">Trichoderma</span> consortium was slightly higher &#40;&#8764;1&#46;2-fold&#41; but not significant&#44; as determined for <span class="elsevierStyleItalic">P&#46; chrysosporium</span> &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>c&#41;&#46;</p><p id="par0140" class="elsevierStylePara elsevierViewall">The chitinase activity &#40;GlcNAc activity&#41; for the <span class="elsevierStyleItalic">Trichoderma</span> consortium was higher &#40;&#8764;1&#46;2-fold&#41; than that achieved for <span class="elsevierStyleItalic">P&#46; chrysosporium</span>&#44; either in the absence or presence of the insecticide &#40;<a class="elsevierStyleCrossRef" href="#fig0020">Fig&#46; 4</a>a&#41;&#46; Overall&#44; the application of the insecticide caused a 25&#37; decrease in the GlcNAc activity of both fungal cultures&#59; however&#44; the GlcNAc activity in the <span class="elsevierStyleItalic">Trichoderma</span> consortium was always significantly higher &#40;&#8764;1&#46;2-fold&#41; than that in <span class="elsevierStyleItalic">P&#46; chrysosporium</span> &#40;<a class="elsevierStyleCrossRef" href="#fig0020">Fig&#46; 4</a>a&#41;&#46;</p><p id="par0145" class="elsevierStylePara elsevierViewall">In the absence of the insecticide&#44; the CMCase activity for the <span class="elsevierStyleItalic">Trichoderma</span> consortium was significantly higher &#40;&#8764;1&#46;4-fold&#41; than the CMCase activity achieved by <span class="elsevierStyleItalic">P&#46; chrysosporium</span>&#46; The insecticide significantly decreased the CMCase activity of both fungal cultures&#59; overall&#44; the enzyme activity of the <span class="elsevierStyleItalic">Trichoderma</span> consortium was significantly higher &#40;&#8764;1&#46;3-fold&#41; than that of <span class="elsevierStyleItalic">P&#46; chrysosporium</span> &#40;<a class="elsevierStyleCrossRef" href="#fig0020">Fig&#46; 4</a>b&#41;&#46;</p></span></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Discussion</span><p id="par0150" class="elsevierStylePara elsevierViewall">Many microorganisms grow in the presence of pesticides&#44; and this ability is influenced by chemical&#44; physical&#44; biochemical&#44; and environmental conditions&#44; and also depends on the amount and type of pesticides<a class="elsevierStyleCrossRef" href="#bib0430"><span class="elsevierStyleSup">36</span></a>&#46; The initial fungal response to contaminants reflects the initial adaptation to stressful cultural conditions and&#47;or to contaminated environments<a class="elsevierStyleCrossRef" href="#bib0350"><span class="elsevierStyleSup">20</span></a>&#46; Synthetic pyrethroids &#40;cypermethrin&#44; deltamethrin&#44; permethrin&#44; and others&#41; and carbamates such as propoxur may reduce the growth of bacteria and filamentous fungi such as <span class="elsevierStyleItalic">T&#46; viride</span>&#44; <span class="elsevierStyleItalic">T&#46; harzianum</span>&#44; and <span class="elsevierStyleItalic">P&#46; chrysosporium</span> strains<a class="elsevierStyleCrossRefs" href="#bib0255"><span class="elsevierStyleSup">1&#44;10&#44;23&#44;36&#44;47</span></a>&#46; Conversely to our results&#44; Schumacher and Poheling did not find negative effects of permethrin on the growth of <span class="elsevierStyleItalic">Metarhizium</span><span class="elsevierStyleItalic">anisopliae</span><a class="elsevierStyleCrossRef" href="#bib0425"><span class="elsevierStyleSup">35</span></a>&#46; On the other hand&#44; pyrethroids such as allethrin &#40;50<span class="elsevierStyleHsp" style=""></span>mg&#47;l&#41; did not affect the growth of <span class="elsevierStyleItalic">Fusarium proliferatum</span> CF2<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">4</span></a>&#46; Consistently to our results&#44; Deng et al&#46; observed that pyrethroids such as &#946;-cypermethrin &#40;100<span class="elsevierStyleHsp" style=""></span>mg&#47;l&#41; did not affect the final biomass produced by <span class="elsevierStyleItalic">Aspergillus niger</span> YAT&#59; however&#44; its radial growth was delayed<a class="elsevierStyleCrossRef" href="#bib0300"><span class="elsevierStyleSup">10</span></a>&#46;</p><p id="par0155" class="elsevierStylePara elsevierViewall">The mixture of pyrethroids&#44; &#946;-cypermethrin&#44; deltamethrin&#44; fenvalerate&#44; and &#945;-cyhalothrin &#40;100&#8211;1000<span class="elsevierStyleHsp" style=""></span>mg&#47;l&#41;&#44; reduced the growth in <span class="elsevierStyleItalic">T&#46; viride</span> and <span class="elsevierStyleItalic">P&#46;</span><span class="elsevierStyleItalic">chrysosporium</span><a class="elsevierStyleCrossRef" href="#bib0430"><span class="elsevierStyleSup">36</span></a>&#46; In soils&#44; the application of cypermethrin and chlorpyrifos alone and in combination dramatically decreased both bacterial and fungal populations<a class="elsevierStyleCrossRef" href="#bib0445"><span class="elsevierStyleSup">39</span></a>&#46; The latter indicates that microorganisms require a certain period of adaptation to toxic contaminants to produce those necessary molecules for tolerating such compounds<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">1</span></a>&#46; In the present study&#44; the commercial product has a mixture of two pyrethroids &#40;permethrin&#44; prallethrin&#41; with carbamate &#40;propoxur&#41;&#44; and this combination exerts certain toxicity which significantly delayed the growth of all fungal strains&#46; This effect could be due to the synergy between carbamates and pyrethroids by which the toxicity to microbes may increase<a class="elsevierStyleCrossRef" href="#bib0335"><span class="elsevierStyleSup">17</span></a>&#46;</p><p id="par0160" class="elsevierStylePara elsevierViewall">Some studies have demonstrated the ability of <span class="elsevierStyleItalic">Trichoderma</span> strains for tolerating and growing in the presence of organic compounds such as petroleum hydrocarbons and pyrethroids<a class="elsevierStyleCrossRefs" href="#bib0260"><span class="elsevierStyleSup">2&#44;6&#44;36</span></a>&#46; Furthermore&#44; these fungi may use organic molecules as carbon and energy source since they have the enzymes necessary to perform such metabolism<a class="elsevierStyleCrossRefs" href="#bib0340"><span class="elsevierStyleSup">18&#44;45</span></a>&#46; The fungus identified as part of the genus <span class="elsevierStyleItalic">Cladosporium</span> was reported as tolerant to pyrethroids&#44; including &#946;-cypermethrin&#44; deltamethrin&#44; bifenthrin and permethrin &#40;100<span class="elsevierStyleHsp" style=""></span>mg&#47;l&#41;<a class="elsevierStyleCrossRef" href="#bib0290"><span class="elsevierStyleSup">8</span></a>&#46; Other studies include fungi such as <span class="elsevierStyleItalic">Aspergillus oryzae</span> and <span class="elsevierStyleItalic">Cunninghamella elegans</span>&#44; exposed to pyrethroids&#44; cyhalothrin and 3-phenoxybenzoic acid&#44; an intermediate in the degradation of permethrin<a class="elsevierStyleCrossRefs" href="#bib0405"><span class="elsevierStyleSup">31&#44;49</span></a>&#46;</p><p id="par0165" class="elsevierStylePara elsevierViewall">Consortium cultures are better than individual cultures because there are complementary physiological and biochemical functions among microorganisms&#44; i&#46;e&#46;&#44; while some microorganisms perform specific enzymatic activity&#44; other microorganisms can perform some different enzyme activities&#44; by which all the involved organisms may be benefited<a class="elsevierStyleCrossRef" href="#bib0450"><span class="elsevierStyleSup">40</span></a>&#46; Enzyme activities include superoxide dismutases &#40;SOD&#41;&#44; peroxidases &#40;POXs&#41;&#44; catalases &#40;CAT&#41;&#44; chitinases&#44; glucanases&#44; and many others&#46;</p><p id="par0170" class="elsevierStylePara elsevierViewall">In nature&#44; microorganisms coexist in consortia and interact with each other to transform organic materials<a class="elsevierStyleCrossRefs" href="#bib0380"><span class="elsevierStyleSup">26&#44;40</span></a>&#46; Artificial and natural microbial consortia are being studied for assessing tolerance&#44; removal&#44; and degradation of inorganic and organic compounds<a class="elsevierStyleCrossRef" href="#bib0450"><span class="elsevierStyleSup">40</span></a>&#46; However&#44; little attention is given to filamentous fungi and their tolerance to insecticides as accounted for bacteria<a class="elsevierStyleCrossRef" href="#bib0295"><span class="elsevierStyleSup">9</span></a>&#46; Moreover&#44; research about fungal consortia exposed to pyrethroids and carbamates utilized as substitutes for DDT is scant&#46; Furthermore&#44; many fungi may remove or degrade inorganic and organic compounds from polluted systems through several biochemical processes which include antioxidant molecules and enzymes such as POXs&#46; In this regard&#44; POXs have antioxidant activity and are involved in the detoxification of reactive oxygen species &#40;ROS&#41; such as H<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">2</span> accumulation in cells because these enzymes oxidize H<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">2</span> and are involved in the detoxification processes of organic pollutants<a class="elsevierStyleCrossRefs" href="#bib0345"><span class="elsevierStyleSup">19&#44;46</span></a>&#46; Other extracellular fungal POXs &#40;lignin peroxidase&#44; manganese peroxidase&#44; and versatile peroxidase VP&#41; are involved in the removal and degradation of pollutants such as polycyclic aromatic hydrocarbons &#40;PAHs&#41;&#44; dye-based textile effluents&#44; polychlorinated biphenyls&#44; fungicides&#44; and pesticides<a class="elsevierStyleCrossRef" href="#bib0480"><span class="elsevierStyleSup">46</span></a>&#46;</p><p id="par0175" class="elsevierStylePara elsevierViewall">Our results concur with those findings in white-rot fungi such as <span class="elsevierStyleItalic">Polyporus tricholoma</span>&#44; <span class="elsevierStyleItalic">Cilindrobasidium leave</span>&#44; and <span class="elsevierStyleItalic">Deconica citrispora</span> that increased POX activity &#40;especially MnP&#41; when exposed to paraquat&#44; a widely applied herbicide in agriculture whose chemical structure resembles that of lignin<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">5</span></a>&#46; In addition&#44; <span class="elsevierStyleItalic">P&#46; chrysosporium</span> can degrade a wide variety of organic pollutants due to the activity of non-specific extracellular POXs<a class="elsevierStyleCrossRef" href="#bib0370"><span class="elsevierStyleSup">24</span></a>&#46; Furthermore&#44; non-ligninolytic fungi such as <span class="elsevierStyleItalic">Aspergillus</span>&#44; <span class="elsevierStyleItalic">Fusarium</span>&#44; and <span class="elsevierStyleItalic">Trichoderma</span> may transform environmental pollutants such as PAHs&#44; pesticides&#44; and dyes&#44; releasing POX enzymes<a class="elsevierStyleCrossRef" href="#bib0355"><span class="elsevierStyleSup">21</span></a>&#46; Zhao et al&#46; proposed that <span class="elsevierStyleItalic">A&#46; oryzae</span> M4 uses some POXs in the presence of NADPH and O<span class="elsevierStyleInf">2</span>&#44; for degrading 3-phenoxybenzoic acid&#44; a subproduct of permethrin degradation<a class="elsevierStyleCrossRef" href="#bib0490"><span class="elsevierStyleSup">48</span></a>&#46; <span class="elsevierStyleItalic">Trichoderma asperellum</span> H15 was exposed to PAHs with 3&#8211;5 rings &#40;phenanthrene&#44; pyrene&#44; and benzo&#91;<span class="elsevierStyleItalic">a</span>&#93;pyrene&#41;&#44; and the fungal POX activity increased after 4 days of exposure<a class="elsevierStyleCrossRef" href="#bib0480"><span class="elsevierStyleSup">46</span></a>&#46; Many POXs were identified in <span class="elsevierStyleItalic">T&#46; asperellum</span>&#44; including cytochrome C peroxidases&#44; catalases&#44; glutathione peroxidase&#44; and dye-decolorizing peroxidases<a class="elsevierStyleCrossRef" href="#bib0480"><span class="elsevierStyleSup">46</span></a>&#46; Most fungi&#44; including <span class="elsevierStyleItalic">P&#46; chrysosporium</span> and <span class="elsevierStyleItalic">Trichoderma</span> sp&#46;&#44; are studied for degrading or removing PAHs&#44; organochloride pesticides&#44; organophosphates&#44; carbamates&#44; and pyrethroids such as &#946;-cypermethrin and deltamethrin&#44; by means of the oxidative effects of POXs<a class="elsevierStyleCrossRefs" href="#bib0305"><span class="elsevierStyleSup">11&#44;12&#44;24&#44;43</span></a>&#46; In our results&#44; the POX activity detected in the <span class="elsevierStyleItalic">Trichoderma</span> consortium was higher than that of <span class="elsevierStyleItalic">P&#46; chrysosporium</span>&#44; which may be explained in part&#44; by the fact that the <span class="elsevierStyleItalic">Trichoderma</span> consortium was integrated by four fungal strains&#44; and thus&#44; all strains may have released more POX enzymes&#46;</p><p id="par0180" class="elsevierStylePara elsevierViewall">The studies of POXs involved in either the removal or degradation of pyrethroids such as permethrin and prallethrin&#44; and carbamates such as propoxur&#44; are still little explored&#46; Our results suggest that the <span class="elsevierStyleItalic">Trichoderma</span> consortium and <span class="elsevierStyleItalic">P&#46; chrysosporium</span> increase their POX activities for tolerating the commercial insecticide in liquid culture&#46; However&#44; further studies are needed to identify specific POXs that participate during this process&#44; and to determine whether these enzymes act on both the degradation and detoxification of insecticides and byproducts&#44; as well&#46;</p><p id="par0185" class="elsevierStylePara elsevierViewall">On the other hand&#44; chitinases play a key role in the transformation of chitin and are widely distributed in nature with a wider range of biotechnological applications&#44; including the biocontrol of fungal phytopathogens&#44; harmful insects&#44; bioconversion of chitin wastes&#44; to single-cell protein&#44; biopesticides&#44; among others<a class="elsevierStyleCrossRef" href="#bib0435"><span class="elsevierStyleSup">37</span></a>&#46; Moreover&#44; chitinases are important for maintaining the balance of carbon and nitrogen ratio in ecosystems<a class="elsevierStyleCrossRefs" href="#bib0385"><span class="elsevierStyleSup">27&#44;32&#44;37</span></a>&#46; Regarding chitin degradation&#44; the chitinase family includes three enzymes that act separately&#44; &#40;1&#41; endochitinases that recognize <span class="elsevierStyleItalic">o</span>-glycosyl bonds between chito-saccharide residues for catalysis and produce multimers of oligosaccharides&#44; especially diacetylchitobiose&#59; &#40;2&#41; exochitinases that release soluble low molecular weight dimers&#44; and &#40;3&#41; chitobiose that hydrolyses diacetylchitobiose to N-acetyl-glucosamine &#40;GlcNAc&#41;<a class="elsevierStyleCrossRef" href="#bib0455"><span class="elsevierStyleSup">41</span></a>&#46; Both bacteria and fungi use chitin as a carbon and energy source&#44; and the production of chitinolytic enzymes is related to carbon sources in synthetic culture media<a class="elsevierStyleCrossRefs" href="#bib0410"><span class="elsevierStyleSup">32&#44;41</span></a>&#46;</p><p id="par0190" class="elsevierStylePara elsevierViewall">Chitinases produced by <span class="elsevierStyleItalic">Trichoderma</span> correspond to enzymes that function as biological control agents and are responsible for the lysis and degradation of fungal cell walls and insect cuticles<a class="elsevierStyleCrossRef" href="#bib0330"><span class="elsevierStyleSup">16</span></a>&#46; Furthermore&#44; the exposure of <span class="elsevierStyleItalic">Paenibacillus</span> sp&#46; to pyrethroids &#40;cypermethrin&#41; at concentrations recommended for field applications&#44; caused the total inhibition of chitinase production&#44; whereas insecticides such as methyl parathion and endosulfan significantly decreased &#40;30&#8211;40&#37;&#41; the activity and stability of chitinases<a class="elsevierStyleCrossRef" href="#bib0440"><span class="elsevierStyleSup">38</span></a>&#46; Organic molecules such as PAHs&#44; with four or more aromatic rings&#44; inhibited chitinase activities from <span class="elsevierStyleItalic">Aeromonas hydrophila</span> subsp&#46; <span class="elsevierStyleItalic">anaerogenes</span> A52 and from <span class="elsevierStyleItalic">T&#46;</span><span class="elsevierStyleItalic">harzianum</span><a class="elsevierStyleCrossRefs" href="#bib0395"><span class="elsevierStyleSup">29&#44;41</span></a>&#46; To our knowledge&#44; GlcNAc-activity has not been reported as being involved in the removal or degradation of organic pollutants such as pyrethroid and carbamate insecticides&#59; however&#44; this enzyme may serve as a biomarker for assessing detoxification processes of systems polluted with these compounds&#46;</p><p id="par0195" class="elsevierStylePara elsevierViewall">Endoglucanases &#40;EGs&#41; represent a group of dynamic cellulases that randomly attack internal <span class="elsevierStyleItalic">O</span>-glycosidic bonds of the cellulose chain&#44; releasing glucan chains with different lengths&#44; to generate new reducing and non-reducing ends&#59; thus&#44; EGs are the most important cellulases that contribute to the hydrolysis of cellulose<a class="elsevierStyleCrossRef" href="#bib0500"><span class="elsevierStyleSup">50</span></a>&#46; EGs have many biotechnological applications for the industry&#44; including animal food&#44; textiles&#44; laundry&#44; pulp and paper&#44; brewery and wine&#44; food&#44; and agriculture&#44; among others&#46; These enzymes are globally marketed from fungi such as <span class="elsevierStyleItalic">Aspergillus</span> and <span class="elsevierStyleItalic">Trichoderma</span><a class="elsevierStyleCrossRef" href="#bib0265"><span class="elsevierStyleSup">3</span></a>&#46;</p><p id="par0200" class="elsevierStylePara elsevierViewall">Overall&#44; most studies are limited to reporting the degradation percentages of insecticides but not emphasizing the effects of insecticides on microbial biomolecules&#46; The production of a high number of enzymes&#44; and the optimal activity of these enzymes may depend on culture media and microorganisms&#46; The use of pyrethroids and carbamates increased as a result of the prohibition of DDT&#44; and these insecticides can disturb agricultural soils and may lead to several issues related to environmental and human health pollution&#46; Furthermore&#44; these organic chemicals may exert toxic effects on microorganisms and higher organisms&#46; The present study highlights that a commercial organic pesticide based on pyrethroids and carbamates may inhibit both the growth of filamentous fungi and the activity of important fungal enzymes involved in either chitin or cellulose degradation&#46;</p><p id="par0205" class="elsevierStylePara elsevierViewall">Overall&#44; increasing the concentrations of the active ingredient of the commercial insecticide H24&#174; decreased the radial growth rate in ten strains of <span class="elsevierStyleItalic">Trichoderma</span> sp&#46; and <span class="elsevierStyleItalic">P&#46; chrysosporium</span>&#46; Four prominent strains of <span class="elsevierStyleItalic">Trichoderma</span> &#91;<span class="elsevierStyleItalic">T&#46; koningii</span> &#40;Trich CP03&#41;&#44; <span class="elsevierStyleItalic">T&#46; virens</span> &#40;Trich CP022&#41;&#44; <span class="elsevierStyleItalic">T&#46; virens</span> &#40;Trich CP037&#41;&#44; and <span class="elsevierStyleItalic">T&#46; atroviride</span> &#40;Trich CP0X&#41;&#93; were able to tolerate 200<span class="elsevierStyleHsp" style=""></span>ppm of this commercial insecticide&#46; These four fungal strains grew in a liquid culture medium contaminated with 100<span class="elsevierStyleHsp" style=""></span>ppm of the commercial insecticide and showed increased protein production and high POX enzyme activity&#46; Moreover&#44; this commercial insecticide had negative effects on chitinase and endoglucanase activities derived from the <span class="elsevierStyleItalic">Trichoderma</span> consortium&#59; therefore&#44; it should be considered when using these microorganisms in combination with organic insecticides addressed to integrated pest management&#44; and for assessing tolerance&#44; detoxification&#44; or degradation of organic insecticides based on permethrin&#44; prallethrin and propoxur&#44; for instance&#46;</p></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Conflict of interest</span><p id="par0210" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflicts of interest&#46;</p></span></span>"
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              "titulo" => "Bioassay 1&#46; Fungal growth and tolerance to increased concentrations of commercial insecticide"
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              "titulo" => "Bioassay 2&#46; Fungal protein content and induced peroxidase&#44; chitinase&#44; and glucanase activities in a liquid medium containing&#47;contaminated with 100 ppm of commercial insecticide"
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              "titulo" => "Bioassay 1&#46; Fungal growth and tolerance to three concentrations of commercial insecticide"
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              "titulo" => "Bioassay 2&#46; Fungal growth&#44; protein content&#44; and induced peroxidase&#44; chitinase&#44; and glucanase activities in a liquid medium containing 100 mg&#47;l of commercial insecticide"
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          "titulo" => "Acknowledgments"
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        11 => array:1 [
          "titulo" => "References"
        ]
      ]
    ]
    "pdfFichero" => "main.pdf"
    "tienePdf" => true
    "fechaRecibido" => "2022-07-13"
    "fechaAceptado" => "2023-06-13"
    "PalabrasClave" => array:2 [
      "en" => array:1 [
        0 => array:4 [
          "clase" => "keyword"
          "titulo" => "Keywords"
          "identificador" => "xpalclavsec1796971"
          "palabras" => array:6 [
            0 => "Permethrin"
            1 => "Prallethrin"
            2 => "Propoxur"
            3 => "Peroxidases"
            4 => "Chitinases"
            5 => "Endoglucanases"
          ]
        ]
      ]
      "es" => array:1 [
        0 => array:4 [
          "clase" => "keyword"
          "titulo" => "Palabras clave"
          "identificador" => "xpalclavsec1796970"
          "palabras" => array:6 [
            0 => "Permetrina"
            1 => "Praletrina"
            2 => "Propoxur"
            3 => "Peroxidasas"
            4 => "Quitinasas"
            5 => "Endoglucanasas"
          ]
        ]
      ]
    ]
    "tieneResumen" => true
    "highlights" => array:2 [
      "titulo" => "Highlights"
      "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall"><ul class="elsevierStyleList" id="lis0005"><li class="elsevierStyleListItem" id="lsti0005"><span class="elsevierStyleLabel">&#8226;</span><p id="par0005" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Trichoderma</span> spp&#46; strains tolerate 200<span class="elsevierStyleHsp" style=""></span>ppm of pyrethroids and carbamate insecticides&#46;</p></li><li class="elsevierStyleListItem" id="lsti0010"><span class="elsevierStyleLabel">&#8226;</span><p id="par0010" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Trichoderma</span> spp&#46; consortium growth in liquid culture with 100<span class="elsevierStyleHsp" style=""></span>ppm of insecticide&#46;</p></li><li class="elsevierStyleListItem" id="lsti0015"><span class="elsevierStyleLabel">&#8226;</span><p id="par0015" class="elsevierStylePara elsevierViewall">Insecticide promotes the release of proteins and peroxidases by <span class="elsevierStyleItalic">Trichoderma</span> spp&#46;</p></li><li class="elsevierStyleListItem" id="lsti0020"><span class="elsevierStyleLabel">&#8226;</span><p id="par0020" class="elsevierStylePara elsevierViewall">Insecticide decreases chitinase and endoglucanase produced by <span class="elsevierStyleItalic">Trichoderma</span> spp&#46;</p></li></ul></p></span>"
    ]
    "resumen" => array:2 [
      "en" => array:2 [
        "titulo" => "Abstract"
        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">The application of pyrethroids and carbamates represents an environmental risk and may exert adverse effects on beneficial microorganisms such as <span class="elsevierStyleItalic">Trichoderma</span>&#44; which contribute to the biocontrol of several fungal phytopathogens&#46; This research evaluated the tolerance of several strains of <span class="elsevierStyleItalic">Trichoderma</span> to a selected culture medium contaminated with a commercial insecticide &#40;H24&#174;&#41; composed of pyrethroids&#44; permethrin and prallethrin&#44; and carbamate propoxur&#44; and determined the influence of this insecticide on the release of enzymes such as chitinases&#44; peroxidases&#44; and endoglucanases by a consortium of selected <span class="elsevierStyleItalic">Trichoderma</span> strains grown in liquid culture medium&#46; Four out of 10 <span class="elsevierStyleItalic">Trichoderma</span> strains showed tolerance to 200<span class="elsevierStyleHsp" style=""></span>ppm &#40;&#8764;48&#46;3&#37; of growth&#41; of the commercial insecticide after 96<span class="elsevierStyleHsp" style=""></span>h of exposure to a contaminated solid medium&#46; After eight days of growth in liquid culture&#44; the insecticide enhanced extracellular protein content and peroxidase activities in the <span class="elsevierStyleItalic">Trichoderma</span> consortium but decreased both chitinase and glucanase activities&#46; These fungal responses should be considered when implementing strategies that combine alternative pesticides and fungal biocontrollers for managing fungal phytopathogens&#46;</p></span>"
      ]
      "es" => array:2 [
        "titulo" => "Resumen"
        "resumen" => "<span id="abst0015" class="elsevierStyleSection elsevierViewall"><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">La aplicaci&#243;n de piretroides y carbamatos representa un riesgo ambiental y puede ejercer efectos adversos sobre microorganismos ben&#233;ficos&#44; como el <span class="elsevierStyleItalic">Trichoderma</span>&#44; que contribuyen al biocontrol de varios fitopat&#243;genos&#46; Por un lado&#44; esta investigaci&#243;n evalu&#243; la tolerancia de varias cepas de <span class="elsevierStyleItalic">Trichoderma</span> a un medio de cultivo s&#243;lido contaminado con un insecticida comercial &#40;H24&#174;&#41; compuesto por piretroides &#40;permetrina y praletrina&#41; y carbamato propoxur&#59; por el otro&#44; determin&#243; la influencia de este insecticida en la liberaci&#243;n de enzimas como quitinasas&#44; peroxidasas y endoglucanasas por un consorcio de cepas seleccionadas de <span class="elsevierStyleItalic">Trichoderma</span> cultivadas en medio l&#237;quido&#46; Cuatro de 10 cepas de <span class="elsevierStyleItalic">Trichoderma</span> mostraron tolerancia a 200 ppm &#40;&#8764;48&#44;3&#37; de crecimiento&#41; del insecticida comercial despu&#233;s de 96 horas en un medio s&#243;lido contaminado&#46; Tras ocho d&#237;as de crecimiento en cultivo l&#237;quido&#44; el insecticida aument&#243; el contenido de prote&#237;nas y la actividad peroxidasa del consorcio <span class="elsevierStyleItalic">Trichoderma</span>&#44; pero redujo las actividades quitinasa y glucanasa&#46; Estas respuestas f&#250;ngicas podr&#237;an ser consideradas al implementar estrategias para el biocontrol y el manejo de hongos fitopat&#243;genos&#46;</p></span>"
      ]
    ]
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        "mostrarDisplay" => false
        "figura" => array:1 [
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          "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Growth rate of <span class="elsevierStyleItalic">Trichoderma</span> strains and <span class="elsevierStyleItalic">Phanerochaete chrysosporium</span>-ATCC 34540 in solid medium &#40;PDA&#41; with &#40;a&#41; 0<span class="elsevierStyleHsp" style=""></span>mg&#47;l&#44; &#40;b&#41; 50<span class="elsevierStyleHsp" style=""></span>mg&#47;l&#44; &#40;c&#41; 100<span class="elsevierStyleHsp" style=""></span>mg&#47;l&#44; &#40;d&#41; 150<span class="elsevierStyleHsp" style=""></span>mg&#47;l&#44; and &#40;e&#41; 200<span class="elsevierStyleHsp" style=""></span>mg&#47;l of commercial insecticide H24&#174; with three active ingredients &#40;permethrin&#44; prallethrin&#44; and propoxur&#41;&#46; Means<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>standard error &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>4&#41;&#46;</p>"
        ]
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      1 => array:7 [
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        "etiqueta" => "Figure 2"
        "tipo" => "MULTIMEDIAFIGURA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "figura" => array:1 [
          0 => array:4 [
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        "descripcion" => array:1 [
          "en" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">&#40;a&#41; Radial growth rate &#40;mm&#47;h&#41; and &#40;b&#41; radial growth rate inhibition &#40;RGRI&#37;&#41; of <span class="elsevierStyleItalic">Trichoderma</span> strains and <span class="elsevierStyleItalic">Phanerochaete chrysosporium</span>-ATCC34540 in solid medium &#40;PDA&#41; with 0&#44; 50&#44; 100&#44; 150&#44; and 200<span class="elsevierStyleHsp" style=""></span>mg&#47;l of commercial insecticide H24&#174; with three active ingredients &#40;permethrin&#44; prallethrin&#44; and propoxur&#41;&#46; Means<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>standard error &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>4&#41;&#46;</p>"
        ]
      ]
      2 => array:7 [
        "identificador" => "fig0015"
        "etiqueta" => "Figure 3"
        "tipo" => "MULTIMEDIAFIGURA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "figura" => array:1 [
          0 => array:4 [
            "imagen" => "gr3.jpeg"
            "Alto" => 2663
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        ]
        "descripcion" => array:1 [
          "en" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">&#40;a&#41; Biomass &#40;DW<span class="elsevierStyleHsp" style=""></span>g&#41;&#44; &#40;b&#41; extracellular protein content &#40;&#956;g&#47;l&#41;&#44; and &#40;c&#41; extracellular peroxidase activity &#40;POX activity&#44; U&#47;&#956;g protein&#41; of <span class="elsevierStyleItalic">Trichoderma</span> sp&#46; and <span class="elsevierStyleItalic">P&#46; chrysosporium</span>-ATCC 34540 in liquid culture in the absence &#40;SC&#41; and presence &#40;SC<span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span>I&#41; of sub-ID<span class="elsevierStyleInf">50</span> &#40;100<span class="elsevierStyleHsp" style=""></span>mg&#47;l&#41; of commercial insecticide H24&#174; with three active ingredients &#40;permethrin&#44; prallethrin and propoxur&#41;&#44; after 8 days in liquid culture&#46; Different letters indicate significant differences among means for medium culture&#59; asterisks indicate significant differences among means for microorganisms &#40;Tukey&#44; <span class="elsevierStyleItalic">&#945;</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41;&#46; Means<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>standard error &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>4&#41;&#46;</p>"
        ]
      ]
      3 => array:7 [
        "identificador" => "fig0020"
        "etiqueta" => "Figure 4"
        "tipo" => "MULTIMEDIAFIGURA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "figura" => array:1 [
          0 => array:4 [
            "imagen" => "gr4.jpeg"
            "Alto" => 2343
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            "Tamanyo" => 122620
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        "descripcion" => array:1 [
          "en" => "<p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">&#40;a&#41; Chitinase activity &#40;GlcNAc&#44; U&#47;mg protein&#41; and &#40;b&#41; endoglucanase activity &#40;CMCase&#44; U&#47;&#956;g protein&#41; of <span class="elsevierStyleItalic">Trichoderma</span> sp&#46; and <span class="elsevierStyleItalic">P&#46; chrysosporium</span>-ATCC 34540 in liquid culture in the absence &#40;SC&#41; and presence &#40;SC<span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span>I&#41; of sub-ID<span class="elsevierStyleInf">50</span> &#40;100<span class="elsevierStyleHsp" style=""></span>mg&#47;l&#41; of commercial insecticide H24&#174; with three active ingredients &#40;permethrin&#44; prallethrin&#44; and propoxur&#41;&#44; after 8 days in liquid culture&#46; Different letters indicate significant differences among means for medium culture&#59; the asterisk indicates significant differences among means for microorganisms &#40;Tukey&#44; <span class="elsevierStyleItalic">&#945;</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41;&#46; Means<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>standard error &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>4&#41;&#46;</p>"
        ]
      ]
      4 => array:8 [
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        "etiqueta" => "Table 1"
        "tipo" => "MULTIMEDIATABLA"
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        "detalles" => array:1 [
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            "identificador" => "at1"
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        "tabla" => array:2 [
          "leyenda" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">Active ingredients in the commercial product &#40;H24&#174;&#41; are permethrin&#44; prallethrin&#44; and propoxur&#46; Means<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>standard error &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>4&#41;&#46;</p>"
          "tablatextoimagen" => array:1 [
            0 => array:2 [
              "tabla" => array:1 [
                0 => """
                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Fungal strain&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">ID<span class="elsevierStyleInf">50</span> &#40;mg&#47;l&#41; of commercial insecticide&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Trich CP01&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">104&#46;34<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;47&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Trich CP03&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">131&#46;64<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>15&#46;80&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Trich CP04&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">107&#46;66<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>3&#46;56&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Trich CP022&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">143&#46;76<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>3&#46;45&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Trich CP023&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">77&#46;27<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;99&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Trich CP037&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">219&#46;04<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>3&#46;16&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Trich CP038&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">91&#46;59<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>2&#46;15&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Trich CP056&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">87&#46;32<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>4&#46;58&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Trich CP0X&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">167&#46;10<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>8&#46;82&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Trich CP0TGC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">85&#46;58<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;32&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">P&#46; chrysosporium</span>-ATCC 34540&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">134&#46;61<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;34&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
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              ]
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Article information

ISSN: 03257541
Original language: English

DOI:10.1016/j.ram.2023.06.004

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