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The nematophagous fungus Monacrosporium thaumasium and its nematicidal activity on Angiostrongylus vasorum
El hongo nematófago Monacrosporium thaumasium y su actividad nematicida frente a Angiostrongylus vasorum
Filippe Elias de Freitas Soaresc,
, Fabio Ribeiro Bragaa,b, Jackson Victor de Araújoa,1, Walter dos Santos Limad, José Humberto de Queirozc
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a Departamento de Veterinária, Universidade Federal de Viçosa, Viçosa, MG, Brazil
b Departamento de Veterinária, Universidade Vila Velha, ES, Brazil
c Departamento de Bioquímica e Biologia Molecular, Universidade Federal de Viçosa, Viçosa, MG, Brazil
d Departamento de Parasitologia Animal, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
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White arrows: protease with molecular weight of approximately 40<span class="elsevierStyleHsp" style=""></span>kDa.</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0005" class="elsevierStylePara elsevierViewall">Nematophagous fungi have been successfully used on <span class="elsevierStyleItalic">in vitro</span> studies of biological control. These organisms called “eaters of helminths” stand out for their availability and easy maintenance under laboratory conditions. However, after many years, little is known about the real mechanism of their infection <span class="elsevierStyleItalic">versus</span> nematodes.<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1,13</span></a> In this context, researches about the production of primary metabolites, such as proteolytic enzymes, are performed; these enzymes have been studied in biological assays of nematicidal activity.<a class="elsevierStyleCrossRefs" href="#bib0045"><span class="elsevierStyleSup">9,17</span></a> On the other hand, nematophagous fungi have been pointed out, especially due to the promising results observed in laboratory conditions through the interaction between fungi and the first-stage larvae of <span class="elsevierStyleItalic">Angiostrongylus vasorum</span>.<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">Species of the genus <span class="elsevierStyleItalic">Angiostrongylus</span> (<span class="elsevierStyleItalic">Angiostrongylus costaricensis</span>, <span class="elsevierStyleItalic">Angiostrongylus cantonensis</span> and <span class="elsevierStyleItalic">Angiostrongylus vasorum</span>) can cause problems for the definitive host (dogs) and eventually parasitize man.<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a> The literature has reported some work that have aimed to seek alternative measures, such as biological control, to be used in combat of angiostrongyliasis.</p><p id="par0015" class="elsevierStylePara elsevierViewall">The role of the dog as a reservoir and environmental disseminator of potentially zoonotic parasites was reported long ago. Moreover, it is known that in many places this important aspect of transmission of zoonotic agents is present, especially in poorer regions of Asia, South America, Africa and Australia.<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">18</span></a> In Brazil,<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">16</span></a> the risk of human infection through contaminated feces of dogs may be significantly higher than in developed countries where a similar prevalence is observed. In this context,<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">15</span></a> the fecal environment is the favorable place for the development of helminths that parasitize domestic animals and may also be zoonotic, since in this environment most genera of helminth pass from the egg stage to infective larvae stage. On the other hand, there is a need for studies aimed at discovering the action of substances produced by these fungi in environments that mimic the natural condition of infection, for example, contaminated feces, so they can eventually be used in environmental control of larvae of this nematoda. Among those substances, the use of proteases produced by nematophagous fungi stands out.<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a></p><p id="par0020" class="elsevierStylePara elsevierViewall">The aim of this work was to study the proteolytic profile of the nematophagous fungus <span class="elsevierStyleItalic">Monacrosporium thaumasium</span> and its activity against <span class="elsevierStyleItalic">A. vasorum</span> larvae.</p><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Materials and methods</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Organisms</span><p id="par0025" class="elsevierStylePara elsevierViewall">Positive feces of dogs were used for <span class="elsevierStyleItalic">A. vasorum</span> previously maintained in the Parasitology Department, Federal University of Minas Gerais.<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">14</span></a></p><p id="par0030" class="elsevierStylePara elsevierViewall">To obtain a crude extract, it was used an isolate of the nematophagous fungus <span class="elsevierStyleItalic">M. thaumasium</span> (NF34a), isolated from soil in Brazil and maintained through continuous transfer to solid culture media (corn meal agar 2%) in the Laboratory of the Department of Veterinary Parasitology, Federal University of Viçosa. For the production of crude extract, mycelia of this fungus were obtained by transferring culture discs (about 5<span class="elsevierStyleHsp" style=""></span>mm in diameter) to flasks previously autoclaved and containing 50<span class="elsevierStyleHsp" style=""></span>ml of liquid medium. The liquid medium was composed of: glucose (10<span class="elsevierStyleHsp" style=""></span>g/l), casein (10<span class="elsevierStyleHsp" style=""></span>g/l), K<span class="elsevierStyleInf">2</span>HPO<span class="elsevierStyleInf">4</span> (5.0<span class="elsevierStyleHsp" style=""></span>g/l), MgSO<span class="elsevierStyleInf">4</span> (0.10<span class="elsevierStyleHsp" style=""></span>g/l), ZnSO<span class="elsevierStyleInf">4</span> (0.0050<span class="elsevierStyleHsp" style=""></span>g/l); FeSO<span class="elsevierStyleInf">4</span> (0.001<span class="elsevierStyleHsp" style=""></span>g/l) and CuSO<span class="elsevierStyleInf">4</span> (0.50<span class="elsevierStyleHsp" style=""></span>mg/l). Next, the flasks containing the fungal inoculum grown in shaker under agitation of 120<span class="elsevierStyleHsp" style=""></span>×<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">g</span> and after six days, the supernatant was collected and filtered using Whatman no. 1 filter paper at 4<span class="elsevierStyleHsp" style=""></span>°C. The methodology for production and obtaining of the crude extract was based on the work of Braga et al.<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a></p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Assays</span><p id="par0035" class="elsevierStylePara elsevierViewall">The <span class="elsevierStyleItalic">in vitro</span> test was carried out through two assays (A and B). In assay A, 1000 conidia of the fungus N34a were added in positive coprocultures for <span class="elsevierStyleItalic">A. vasorum</span>, constituting the treated group. The control group was constituted by coprocultures of positive feces, without fungus. In assay B, 5<span class="elsevierStyleHsp" style=""></span>ml of crude extract produced by NF34a were added to coprocultures, constituting the treated group; coprocultures with only the addition of distilled water (5<span class="elsevierStyleHsp" style=""></span>ml) constituted the control group. In both assays, coprocultures were incubated at 25<span class="elsevierStyleHsp" style=""></span>°C in the dark for 8 days. Six replicates were carried for each assay.</p><p id="par0040" class="elsevierStylePara elsevierViewall">At the end of this period, first-stage larvae (L<span class="elsevierStyleInf">1</span>) were obtained using the modified method of Baermann in both assays (A and B), and the total amount of larvae was obtained by a simple rule of three.<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a> Then, data were interpreted by analysis of variance and the efficiency of predation of L<span class="elsevierStyleInf">1</span> in relation to the control groups was assessed by the Tukey test at 1% probability.<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> Subsequently, the average percentage reduction of larvae was calculated according to the following equation:<elsevierMultimedia ident="eq0010"></elsevierMultimedia></p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Proteolytic profile</span><p id="par0045" class="elsevierStylePara elsevierViewall">Next, the proteolytic profile of crude extract of the nematophagous fungus <span class="elsevierStyleItalic">M. thaumasium</span> (NF34a) was revealed by performing a zymogram, using casein as substrate (Casein-SDS-PAGE), as described by Hummel et al.<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a> with some modifications. The action of the enzyme can be observed by the formation of white halos.</p></span></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Results and discussion</span><p id="par0050" class="elsevierStylePara elsevierViewall">After eight days, it was demonstrated in assays A and B that the conidia and the crude extract of <span class="elsevierStyleItalic">M. thaumasium</span> (NF34a) were effective in reducing the number of <span class="elsevierStyleItalic">A. vasorum</span> L<span class="elsevierStyleInf">1</span>. In addition, at the end of the assays, it was noted a statistical difference (<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>0.01) between the means of larvae recovered from the treated groups and those from the control groups with the following percentages: 40% and 52% for the assays A and B, respectively. Via the zymogram performed, it was revealed the proteolytic profile of the crude extract produced by NF34, <a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>, where the presence of a halo of digestion of casein can be observed, revealing the presence of a protease of approximately 40<span class="elsevierStyleHsp" style=""></span>kDa.</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0055" class="elsevierStylePara elsevierViewall">The soil contaminated with infective stages (eggs and/or larvae) has been appointed as one of the major sources of contamination by geohelminths.<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a> Fungal structures, such as conidia, have proven to be effective in controlled trials against <span class="elsevierStyleItalic">A. vasorum</span> L<span class="elsevierStyleInf">1</span>.<a class="elsevierStyleCrossRefs" href="#bib0025"><span class="elsevierStyleSup">5,7</span></a> On the other hand, the use of crude extract is also a artifice, although recent, that has been used to combat eggs and/or larvae of geohelminths.<a class="elsevierStyleCrossRefs" href="#bib0035"><span class="elsevierStyleSup">7,8</span></a> In the present work, the fecal environment was mimetized by use of coprocultures and the results were very promising.</p><p id="par0060" class="elsevierStylePara elsevierViewall">In assay A, conidia of the fungus NF34 poured in the coprocultures decreased the number of L<span class="elsevierStyleInf">1</span> recovered (40%). This result is interesting and confirms previous reports about the predatory activity of conidia of this fungus after the interaction in culture medium containing agar-water and <span class="elsevierStyleItalic">A. vasorum</span> L<span class="elsevierStyleInf">1</span> at the end of seven days (74.5%).<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a> However, some comparisons can be made between the respective works: (1) in this study coprocultures (poor medium) were utilized to mimic the real condition of contamination, while in the work cited above agar-water was used, which although is also poor in nutrients probably gives a larger pattern of control, especially in relation to contamination by other agents; (2) the agar-water medium routinely used in laboratory tests has not yet presented the results achieved under natural conditions, an important information for the use of fecal material.</p><p id="par0065" class="elsevierStylePara elsevierViewall">In relation to assay B, the results obtained can be compared also with the same report5 of the use of crude extract of the predatory fungus <span class="elsevierStyleItalic">Duddingtonia flagrans</span> on <span class="elsevierStyleItalic">A. vasorum</span> L<span class="elsevierStyleInf">1</span>. However, even belonging <span class="elsevierStyleItalic">M. thaumasium</span> to the same group of fungi (predators), this information is important because the concentrated crude extract of <span class="elsevierStyleItalic">D. flagrans</span> was evaluated directly on the L1 in a short period of time, 24 and 48 h, demonstrating a percentage reduction of 53.5% and 71.3%, respectively. In the present work, the crude extract of NF34 showed a percentage of reduction of 52% when recovering after eight days L<span class="elsevierStyleInf">1</span> larvae obtained from treated coprocultures.</p><p id="par0070" class="elsevierStylePara elsevierViewall">This result suggests that possibly the crude extracts produced by predatory nematophagous fungi contains hydrolytic enzymes such as proteases, which maintains its biological activity even under non-optimal pH, temperature, humidity and salt concentrations. On the other hand, the zymogram demonstrated a proteolytic profile of the crude extract of NF34a that points to the presence of one protease with molecular weight similar to the proteases described from predatory nematophagous fungi.<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">11</span></a> Moreover, the zymogram suggested the presence of one protease (Mt1) of approximately 40<span class="elsevierStyleHsp" style=""></span>kDa, which is in according to the recent work of Soares et al.<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">17</span></a> These results may eventually contribute to the discovery of new methodologies that can help in environmental decontamination of geohelminths.</p><p id="par0075" class="elsevierStylePara elsevierViewall">The results of this work confirm that the conidia, as well as the crude extract of the fungus <span class="elsevierStyleItalic">M. thaumasium</span>, may be used to control <span class="elsevierStyleItalic">A. vasorum</span> L<span class="elsevierStyleInf">1</span>. The proteolytic profile suggested the presence of one protease (Mt1) of approximately 40<span class="elsevierStyleHsp" style=""></span>kDa that in the future may be used in biological control of L<span class="elsevierStyleInf">1</span> of this nematode.</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0100">Authors’ declaration</span><p id="par0080" class="elsevierStylePara elsevierViewall">We declare that: (a) the content of the article is original and was not published previously; (b) there is no conflict of interests, related to financial aspects; (c) all the authors have read and approved this manuscript.</p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0105">Conflicts of interest</span><p id="par0085" class="elsevierStylePara elsevierViewall">All authors declare no conflict of interest.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:10 [ 0 => array:3 [ "identificador" => "xres848052" "titulo" => "Abstract" "secciones" => array:5 [ 0 => array:2 [ "identificador" => "abst0005" "titulo" => "Background" ] 1 => array:2 [ "identificador" => "abst0010" "titulo" => "Aims" ] 2 => array:2 [ "identificador" => "abst0015" "titulo" => "Methods" ] 3 => array:2 [ "identificador" => "abst0020" "titulo" => "Results" ] 4 => array:2 [ "identificador" => "abst0025" "titulo" => "Conclusions" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec843084" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres848053" "titulo" => "Resumen" "secciones" => array:5 [ 0 => array:2 [ "identificador" => "abst0030" "titulo" => "Antecedentes" ] 1 => array:2 [ "identificador" => "abst0035" "titulo" => "Objetivos" ] 2 => array:2 [ "identificador" => "abst0040" "titulo" => "Métodos" ] 3 => array:2 [ "identificador" => "abst0045" "titulo" => "Resultados" ] 4 => array:2 [ "identificador" => "abst0050" "titulo" => "Conclusiones" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec843085" "titulo" => "Palabras clave" ] 4 => array:3 [ "identificador" => "sec0010" "titulo" => "Materials and methods" "secciones" => array:3 [ 0 => array:2 [ "identificador" => "sec0015" "titulo" => "Organisms" ] 1 => array:2 [ "identificador" => "sec0020" "titulo" => "Assays" ] 2 => array:2 [ "identificador" => "sec0025" "titulo" => "Proteolytic profile" ] ] ] 5 => array:2 [ "identificador" => "sec0030" "titulo" => "Results and discussion" ] 6 => array:2 [ "identificador" => "sec0040" "titulo" => "Authors’ declaration" ] 7 => array:2 [ "identificador" => "sec0045" "titulo" => "Conflicts of interest" ] 8 => array:2 [ "identificador" => "xack284485" "titulo" => "Acknowledgements" ] 9 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2013-01-13" "fechaAceptado" => "2013-09-03" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec843084" "palabras" => array:4 [ 0 => "Nematophagous fungi" 1 => "<span class="elsevierStyleItalic">Angiostrongylus vasorum</span>" 2 => "<span class="elsevierStyleItalic">Monacrosporium thaumasium</span>" 3 => "Protease" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec843085" "palabras" => array:4 [ 0 => "Hongos nematófagos" 1 => "<span class="elsevierStyleItalic">Angiostrongylus vasorum</span>" 2 => "<span class="elsevierStyleItalic">Monacrosporium thaumasium</span>" 3 => "Proteasa" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:3 [ "titulo" => "Abstract" "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Background</span><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">The dog acts as a reservoir and environmental disseminator of potentially zoonotic parasites.</p></span> <span id="abst0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Aims</span><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">The objective of this work was to study the fungus <span class="elsevierStyleItalic">Monacrosporium thaumasium</span> regarding its nematicidal potential in laboratory trials and its proteolytic profile.</p></span> <span id="abst0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Methods</span><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">The <span class="elsevierStyleItalic">in vitro</span> test was carried out through two assays (A and B). In assay A, conidia of the fungus N34a were added in positive coprocultures for <span class="elsevierStyleItalic">Angiostrongylus vasorum</span>. In assay B, crude extract (treated group) and distilled water (control group) were added to coprocultures. Next, the proteolytic profile of crude extract of the nematophagous fungus <span class="elsevierStyleItalic">M. thaumasium</span> (NF34a) was revealed by performing a zymogram.</p></span> <span id="abst0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Results</span><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">There was a reduction (<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>0.01) in the averages of larvae recovered from the treated groups (conidia and crude extract) in relation to control groups. The zymogram suggested that the nematophagous fungus <span class="elsevierStyleItalic">M. thaumasium</span> produces a protease of approximately 40<span class="elsevierStyleHsp" style=""></span>kDa.</p></span> <span id="abst0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Conclusions</span><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">The results of this work confirm that the conidia as well as the crude extract of the fungus <span class="elsevierStyleItalic">M. thaumasium</span> may be used to control <span class="elsevierStyleItalic">A. vasorum</span> L<span class="elsevierStyleInf">1</span>. The proteolytic profile suggested the presence of one protease (Mt1) of approximately 40<span class="elsevierStyleHsp" style=""></span>kDa that in the future may be used in biological control of L<span class="elsevierStyleInf">1</span> of this nematode.</p></span>" "secciones" => array:5 [ 0 => array:2 [ "identificador" => "abst0005" "titulo" => "Background" ] 1 => array:2 [ "identificador" => "abst0010" "titulo" => "Aims" ] 2 => array:2 [ "identificador" => "abst0015" "titulo" => "Methods" ] 3 => array:2 [ "identificador" => "abst0020" "titulo" => "Results" ] 4 => array:2 [ "identificador" => "abst0025" "titulo" => "Conclusions" ] ] ] "es" => array:3 [ "titulo" => "Resumen" "resumen" => "<span id="abst0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Antecedentes</span><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">El perro actúa como reservorio y propagador ambiental de los parásitos potencialmente zoonóticos.</p></span> <span id="abst0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Objetivos</span><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">El objetivo del presente estudio fue examinar el potencial nematicida del hongo <span class="elsevierStyleItalic">Monacrosporium thaumasium</span> en pruebas de laboratorio, al igual que su perfil proteolítico.</p></span> <span id="abst0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Métodos</span><p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">El examen <span class="elsevierStyleItalic">in vitro</span> se efectuó mediante 2 ensayos (A y B). En el análisis A, se añadieron conidias del hongo N34a a coprocultivos positivos para <span class="elsevierStyleItalic">Angiostrongylus vasorum</span>. En el ensayo B, se añadieron extracto bruto (grupo tratado) y agua destilada (grupo de control) a los coprocultivos. A continuación, se puso de relieve el perfil proteolítico de extracto bruto del hongo nematófago <span class="elsevierStyleItalic">M. thaumasium</span> (NF34a) mediante la realización de un zimograma.</p></span> <span id="abst0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Resultados</span><p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">Se observó una reducción (p<span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>0,01) en el número medio de larvas recuperadas de los grupos tratados (conidias y extracto bruto) en relación con los grupos de control. El zimograma evidenció que el hongo nematófago <span class="elsevierStyleItalic">M. thaumasium</span> produce una proteasa de aproximadamente 40<span class="elsevierStyleHsp" style=""></span>kDa.</p></span> <span id="abst0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Conclusiones</span><p id="spar0050" class="elsevierStyleSimplePara elsevierViewall">Los resultados del presente estudio confirman que las conidias, así como el extracto bruto del hongo <span class="elsevierStyleItalic">M. thaumasium</span>, pueden utilizarse para el control de <span class="elsevierStyleItalic">A. vasorum</span> L<span class="elsevierStyleInf">1</span>. El perfil proteolítico mostró la presencia de una proteasa (Mt1) de alrededor de 40<span class="elsevierStyleHsp" style=""></span>kDa que, en el futuro, se puede utilizar en el control biológico de L<span class="elsevierStyleInf">1</span> de este nematodo.</p></span>" "secciones" => array:5 [ 0 => array:2 [ "identificador" => "abst0030" "titulo" => "Antecedentes" ] 1 => array:2 [ "identificador" => "abst0035" "titulo" => "Objetivos" ] 2 => array:2 [ "identificador" => "abst0040" "titulo" => "Métodos" ] 3 => array:2 [ "identificador" => "abst0045" "titulo" => "Resultados" ] 4 => array:2 [ "identificador" => "abst0050" "titulo" => "Conclusiones" ] ] ] ] "NotaPie" => array:1 [ 0 => array:3 [ "etiqueta" => "1" "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Scholarship CNPq.</p>" "identificador" => "fn0005" ] ] "multimedia" => array:2 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1137 "Ancho" => 585 "Tamanyo" => 30070 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0055" class="elsevierStyleSimplePara elsevierViewall">Proteolytic profile of the crude extract produced by the fungus <span class="elsevierStyleItalic">Monacrosporium thaumasium</span> (NF34a). White arrows: protease with molecular weight of approximately 40<span class="elsevierStyleHsp" style=""></span>kDa.</p>" ] ] 1 => array:5 [ "identificador" => "eq0010" "tipo" => "MULTIMEDIAFORMULA" "mostrarFloat" => false "mostrarDisplay" => true "Formula" => array:5 [ "Matematica" => "%Reduction=(x¯ of control larvae−x¯ of treatment larvae)x¯ of control larvae×100" "Fichero" => "si1.jpeg" "Tamanyo" => 5300 "Alto" => 35 "Ancho" => 434 ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:18 [ 0 => array:3 [ "identificador" => "bib0005" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Controle biológico de helmintos parasitos de animais por fungos nematófagos" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:3 [ 0 => "J.V. Araújo" 1 => "M.A. Mota" 2 => "A.K. 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| Year/Month | Html | Total | |
|---|---|---|---|
| 2024 November | 2 | 0 | 2 |
| 2024 October | 32 | 6 | 38 |
| 2024 September | 31 | 2 | 33 |
| 2024 August | 27 | 3 | 30 |
| 2024 July | 22 | 4 | 26 |
| 2024 June | 20 | 3 | 23 |
| 2024 May | 25 | 7 | 32 |
| 2024 April | 22 | 5 | 27 |
| 2024 March | 37 | 12 | 49 |
| 2024 February | 51 | 15 | 66 |
| 2024 January | 49 | 3 | 52 |
| 2023 December | 32 | 3 | 35 |
| 2023 November | 39 | 4 | 43 |
| 2023 October | 82 | 14 | 96 |
| 2023 September | 20 | 0 | 20 |
| 2023 August | 24 | 6 | 30 |
| 2023 July | 31 | 4 | 35 |
| 2023 June | 27 | 1 | 28 |
| 2023 May | 54 | 2 | 56 |
| 2023 April | 71 | 1 | 72 |
| 2023 March | 41 | 1 | 42 |
| 2023 February | 36 | 4 | 40 |
| 2023 January | 38 | 14 | 52 |
| 2022 December | 47 | 10 | 57 |
| 2022 November | 53 | 12 | 65 |
| 2022 October | 26 | 17 | 43 |
| 2022 September | 75 | 22 | 97 |
| 2022 August | 73 | 22 | 95 |
| 2022 July | 62 | 11 | 73 |
| 2022 June | 34 | 10 | 44 |
| 2022 May | 31 | 19 | 50 |
| 2022 April | 25 | 15 | 40 |
| 2022 March | 32 | 10 | 42 |
| 2022 February | 44 | 11 | 55 |
| 2022 January | 27 | 22 | 49 |
| 2021 December | 33 | 11 | 44 |
| 2021 November | 29 | 11 | 40 |
| 2021 October | 32 | 18 | 50 |
| 2021 September | 15 | 15 | 30 |
| 2021 August | 28 | 26 | 54 |
| 2021 July | 30 | 13 | 43 |
| 2021 June | 30 | 8 | 38 |
| 2021 May | 23 | 13 | 36 |
| 2021 April | 69 | 42 | 111 |
| 2021 March | 59 | 4 | 63 |
| 2021 February | 34 | 9 | 43 |
| 2021 January | 52 | 8 | 60 |
| 2020 December | 30 | 22 | 52 |
| 2020 November | 34 | 14 | 48 |
| 2020 October | 27 | 31 | 58 |
| 2020 September | 23 | 10 | 33 |
| 2020 August | 24 | 13 | 37 |
| 2020 July | 22 | 6 | 28 |
| 2020 June | 18 | 14 | 32 |
| 2020 May | 26 | 14 | 40 |
| 2020 April | 12 | 8 | 20 |
| 2020 March | 33 | 6 | 39 |
| 2020 February | 28 | 9 | 37 |
| 2020 January | 18 | 4 | 22 |
| 2019 December | 17 | 15 | 32 |
| 2019 November | 14 | 6 | 20 |
| 2019 October | 30 | 19 | 49 |
| 2019 September | 32 | 12 | 44 |
| 2019 August | 15 | 12 | 27 |
| 2019 July | 33 | 14 | 47 |
| 2019 June | 30 | 18 | 48 |
| 2019 May | 85 | 48 | 133 |
| 2019 April | 33 | 13 | 46 |
| 2019 March | 8 | 6 | 14 |
| 2019 February | 8 | 13 | 21 |
| 2019 January | 9 | 4 | 13 |
| 2018 December | 3 | 7 | 10 |
| 2018 November | 6 | 6 | 12 |
| 2018 October | 9 | 20 | 29 |
| 2018 September | 8 | 3 | 11 |
| 2018 August | 7 | 5 | 12 |
| 2018 July | 2 | 5 | 7 |
| 2018 June | 2 | 3 | 5 |
| 2018 May | 5 | 5 | 10 |
| 2018 April | 0 | 1 | 1 |
| 2018 March | 2 | 1 | 3 |
| 2018 February | 6 | 2 | 8 |
| 2018 January | 7 | 2 | 9 |
| 2017 December | 8 | 2 | 10 |
| 2017 November | 3 | 2 | 5 |
| 2017 October | 4 | 7 | 11 |
| 2017 September | 10 | 5 | 15 |
| 2017 August | 4 | 3 | 7 |
| 2017 July | 14 | 6 | 20 |
| 2017 June | 13 | 3 | 16 |
| 2017 May | 18 | 6 | 24 |
| 2017 April | 9 | 2 | 11 |
| 2017 March | 14 | 31 | 45 |
| 2017 February | 16 | 1 | 17 |
| 2017 January | 20 | 5 | 25 |
| 2016 December | 22 | 2 | 24 |
| 2016 November | 18 | 3 | 21 |
| 2016 October | 24 | 3 | 27 |
| 2016 September | 27 | 9 | 36 |
| 2016 August | 20 | 4 | 24 |
| 2016 July | 7 | 2 | 9 |
| 2016 June | 12 | 3 | 15 |
| 2016 May | 5 | 4 | 9 |
| 2016 April | 7 | 1 | 8 |
| 2016 March | 11 | 5 | 16 |
| 2016 February | 13 | 7 | 20 |
| 2016 January | 16 | 5 | 21 |
| 2015 April | 0 | 2 | 2 |
| 2015 March | 0 | 2 | 2 |
| 2015 February | 1 | 0 | 1 |
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