ARTÍCULO ORIGINAL
BIOSORPTION OF CD, CR, MN, AND PB FROM AQUEOUS SOLUTIONS BY Bacillus SP STRAINS ISOLATED FROM INDUSTRIAL WASTE ACTIVATE SLUDGE
Biosorción de Cd, Cr, Mn y Pb de soluciones acuosas industriales por cepas de Bacillus sp aisladas de lodos activados
Rocío Garcíaa,
, Juan Camposb, Julio Alfonso Cruzb, Ma. Elena Calderónc, Ma. Elena Raynald, Germán Buitróne
Corresponding author
a Grupo de Aerosoles Atmosféricos Centro de Ciencias de la Atmósfera. Universidad Nacional Autónoma de México, Ciudad Universitaria, Deleg. Coyoacán, C.P. 04510, México, D.F., México
b Grupo de Genotoxicología Ambiental, Centro de Ciencias de la Atmósfera. Universidad Nacional Autónoma de México, Ciudad Universitaria, Deleg. Coyoacán, C.P. 04510, México, D.F., México
c Unidad de Microbiología Básica y Aplicada, Campus Aeropuerto, Facultad de Química,Universidad Autónoma de Querétaro, Cerro de las Campanas s/n, Querétaro, Qro., C.P. 76010, México
d Depto. de Ingeniería Civil y Ambiental, Universidad de las Américas Puebla, Apartado postal 100, Sta. Catarina Mártir, C.P. 72820, Cholula, Puebla, México
e Lab. de Investigación en Procesos Avanzados de Tratamiento de Aguas (LIPATA), Instituto de Ingeniería, Universidad Nacional Autónoma de México, Campus Juriquilla s/n, C.P. 76230, Querétaro, Qro., México
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UvrY contiene un dominio receptor con un residuo D conservado, seguido de un dominio efector con un motivo de unión al ADN. En presencia de acetato y/o formato, BarA se autofosforila de manera dependiente de ATP en el residuo H, y posteriormente transfosforila a UvrY (UvrY-P) en el residuo D vía un fosforelevo que involucra el dominio receptor y de fosfotranferencia de BarA. UvrY-P activa directamente la transcripción de los RNAs pequeños no-codificantes (sRNAs) CsrB y CsrC, los cuales poseen 18 y 9 sitios de unión a la proteína CsrA, regulando negativamente su actividad. Hasta el momento en <span class="elsevierStyleItalic">E. coli</span> se han identificado más de 700 posibles mensajeros blanco de CsrA. La estabilidad de los sRNAs depende de la proteína integral de membrana CsrD, cuya traducción es reprimida por CsrA, que los convierte en blancos de degradación a través de un mecanismo que involucra a la RNasa E. Además, CsrA activa indirectamente la expresión de UvrY y afecta positivamente la actividad cinasa de BarA a través de los factores X y Y, respectivamente, los cuales aún no han sido identificados. Finalmente, la proteína Crp activa la expresión del sRNA McaS, el cual secuestra a CsrA en la fase estacionaria tardía. Modificado de la ref. 8.</p>" ] ] ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "Martha I. Camacho, Dimitris Georgellis, Adrián F. Álvarez" "autores" => array:3 [ 0 => array:2 [ "nombre" => "Martha I." "apellidos" => "Camacho" ] 1 => array:2 [ "nombre" => "Dimitris" "apellidos" => "Georgellis" ] 2 => array:2 [ "nombre" => "Adrián F." "apellidos" => "Álvarez" ] ] ] ] ] "idiomaDefecto" => "es" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S1405888X16000036?idApp=UINPBA00004N" "url" => "/1405888X/0000001900000001/v1_201602260016/S1405888X16000036/v1_201602260016/es/main.assets" ] "en" => array:20 [ "idiomaDefecto" => true "cabecera" => "<span class="elsevierStyleTextfn">ARTÍCULO ORIGINAL</span>" "titulo" => "BIOSORPTION OF CD, CR, MN, AND PB FROM AQUEOUS SOLUTIONS BY <span class="elsevierStyleItalic">Bacillus</span> SP STRAINS ISOLATED FROM INDUSTRIAL WASTE ACTIVATE SLUDGE" "tieneTextoCompleto" => true "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "5" "paginaFinal" => "14" ] ] "autores" => array:1 [ 0 => array:4 [ "autoresLista" => "Rocío García, Juan Campos, Julio Alfonso Cruz, Ma. Elena Calderón, Ma. Elena Raynal, Germán Buitrón" "autores" => array:6 [ 0 => array:4 [ "nombre" => "Rocío" "apellidos" => "García" "email" => array:1 [ 0 => "gmrocio@atmosfera.unam.mx" ] "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">*</span>" "identificador" => "cor0005" ] ] ] 1 => array:3 [ "nombre" => "Juan" "apellidos" => "Campos" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] ] ] 2 => array:3 [ "nombre" => "Julio Alfonso" "apellidos" => "Cruz" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] ] ] 3 => array:3 [ "nombre" => "Ma. Elena" "apellidos" => "Calderón" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">c</span>" "identificador" => "aff0015" ] ] ] 4 => array:3 [ "nombre" => "Ma. Elena" "apellidos" => "Raynal" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">d</span>" "identificador" => "aff0020" ] ] ] 5 => array:3 [ "nombre" => "Germán" "apellidos" => "Buitrón" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">e</span>" "identificador" => "aff0025" ] ] ] ] "afiliaciones" => array:5 [ 0 => array:3 [ "entidad" => "Grupo de Aerosoles Atmosféricos Centro de Ciencias de la Atmósfera. Universidad Nacional Autónoma de México, Ciudad Universitaria, Deleg. Coyoacán, C.P. 04510, México, D.F., México" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Grupo de Genotoxicología Ambiental, Centro de Ciencias de la Atmósfera. Universidad Nacional Autónoma de México, Ciudad Universitaria, Deleg. Coyoacán, C.P. 04510, México, D.F., México" "etiqueta" => "b" "identificador" => "aff0010" ] 2 => array:3 [ "entidad" => "Unidad de Microbiología Básica y Aplicada, Campus Aeropuerto, Facultad de Química,Universidad Autónoma de Querétaro, Cerro de las Campanas s/n, Querétaro, Qro., C.P. 76010, México" "etiqueta" => "c" "identificador" => "aff0015" ] 3 => array:3 [ "entidad" => "Depto. de Ingeniería Civil y Ambiental, Universidad de las Américas Puebla, Apartado postal 100, Sta. Catarina Mártir, C.P. 72820, Cholula, Puebla, México" "etiqueta" => "d" "identificador" => "aff0020" ] 4 => array:3 [ "entidad" => "Lab. de Investigación en Procesos Avanzados de Tratamiento de Aguas (LIPATA), Instituto de Ingeniería, Universidad Nacional Autónoma de México, Campus Juriquilla s/n, C.P. 76230, Querétaro, Qro., México" "etiqueta" => "e" "identificador" => "aff0025" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Biosorción de Cd, Cr, Mn y Pb de soluciones acuosas industriales por cepas de <span class="elsevierStyleItalic">Bacillus</span> sp aisladas de lodos activados" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 4185 "Ancho" => 1706 "Tamanyo" => 345421 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">(a b,c and d). Effects of metals on cell growth to C13 and metal biosorption for Cd, Cr, Mn and Pb conditions: 50<span class="elsevierStyleHsp" style=""></span>mg L<span class="elsevierStyleSup">-1</span> of metal concentration.</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">INTRODUCTION</span><p id="par0005" class="elsevierStylePara elsevierViewall">Analysis of heavy metals in wastewater is important because of their significant role in various complex processes, such as surface soil and water loading, bioaccumulation in living organisms, cloud stability, atmospheric catalysis, and increases in the frequency of air and water-borne diseases<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">[1,2]</span></a>. The concentrations of trace metals in the atmosphere are continuously increasing due to both natural and anthropogenic emission sources, such as winds, storms, volcanic eruptions, biomass burning, evaporation, fossil fuels combustion, ore smelting, thermal power plant fly ash, and unsustainable use of natural resources. Trace metals are subject to biogeochemical cycles that determine their presence and concentrations in different compartments of the environment: soil, groundwater, surface water, air, and living organisms. Human intervention can alter the metal concentrations in these compartments and change the distribution of metals in the environment. The toxicological importance of metals is enormous because of their ubiquity, their extensive industrial and domestic use, and their environmental persistence. This persistence depends upon the characteristics of the chemical compound that the metal comprises, which determine the metal's environmental mobility and its bioavailability<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">[3]</span></a>. The metals in the hydrosphere are of environmental importance because of their interactions with solid geological materials, their influence on biological processes, and their interactions with the atmosphere by evaporation processes<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">[4]</span></a>. Biosorption is a technology that represents an alternative to conventional water treatments for heavy metal recovery. This technology allows the reuse of agricultural and industrial residues. Biosorption is a term that describes the removal of polluting agents from aqueous solutions by using biomass. The mechanism of removal by biosorption is not controlled by metabolism, but mainly by surface adsorption. In contrast, the term bioaccumulation describes an active process of metal removal that requires the metabolic activity of a live organism<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">[5]</span></a>. Heavy metal removal by biomaterials such as biosorbents offers an alternative for toxic metal removal from industrial effluents<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">[6]</span></a>. It is known that biomaterial residues such as agents seaweed, bacteria, fungi and certain aquatic flora have the ability to concentrate and accumulate metals from dilute aqueous solutions<a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">[7]</span></a>. When selecting the metals of interest to examine their removal or recovery options by the application of appropriate technologies, the following considerations are mainly taken into consideration: environmental pollution problems and deterioration of several ecosystems with the accumulation of many toxic metals<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">[8]</span></a>.</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">MATERIALS AND METHODS</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Isolation of bacteria</span><p id="par0010" class="elsevierStylePara elsevierViewall">For the growth and isolation of bacteria, a 1<span class="elsevierStyleHsp" style=""></span>mL sample of activated sludge was deposited in a tube containing 9<span class="elsevierStyleHsp" style=""></span>mL of a sterile saline solution (NaCl to 0.5%). The tube was warmed to a temperature of 80<span class="elsevierStyleHsp" style=""></span>°C over the course of 20<span class="elsevierStyleHsp" style=""></span>minutes, resulting in thermal selection of bacteria that are capable of forming spores The tube was then incubated at 36<span class="elsevierStyleHsp" style=""></span>°C for 24<span class="elsevierStyleHsp" style=""></span>hours. After treatment 100<span class="elsevierStyleHsp" style=""></span>μL from this sample was spread in duplicate onto plates with medium Luria Bertani (LB) agar and nutritious agar). Plates were then incubated at 36<span class="elsevierStyleHsp" style=""></span>°C for 24<span class="elsevierStyleHsp" style=""></span>hours. Strains were characterized by growing in LB agar and nutritious agar prepared with CdCl<span class="elsevierStyleInf">2</span>, MnCl<span class="elsevierStyleInf">2</span>, CrCl<span class="elsevierStyleInf">2</span> and PbCl<span class="elsevierStyleInf">2</span> at 50 and 100<span class="elsevierStyleHsp" style=""></span>mg L<span class="elsevierStyleSup">-1</span>. A total of 37 strains were isolated, 16 of which grew in LB agar and 31 of which grew in nutritious agar.</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Effects of metals on bacterial growth</span><p id="par0015" class="elsevierStylePara elsevierViewall">The solutions with heavy metals were sterilized by using 0.45<span class="elsevierStyleHsp" style=""></span>μm pore-size sterile filters. The strains that could tolerante the highest heavy metal concentration were selected and identified. Two strains (C-13 and C-16) displayed growth at concentrations of 50<span class="elsevierStyleHsp" style=""></span>mg L<span class="elsevierStyleSup">-1</span> for all the metals. Growth was recorded after 1–3 days of incubation at 36<span class="elsevierStyleHsp" style=""></span>°C. The lowest concentration of metal that completely prevented growth was termed the minimal inhibitory concentration (MIC).</p><p id="par0020" class="elsevierStylePara elsevierViewall">The metal susceptibility of each strain was determined using CdCl<span class="elsevierStyleInf">2</span>, MnCl<span class="elsevierStyleInf">2</span>, CrCl<span class="elsevierStyleInf">2</span> and PbCl<span class="elsevierStyleInf">2</span>. Liquid cultures in LB medium were incubated in a shaker at 37<span class="elsevierStyleHsp" style=""></span>°C until the suspension reached an OD600 between 0.4 and 0.5. A volume of 100<span class="elsevierStyleHsp" style=""></span>μL of each strain was spread in LB medium diluted to 50% of normal strength. A volume of 5<span class="elsevierStyleHsp" style=""></span>μL of each metal with concentrations of 50<span class="elsevierStyleHsp" style=""></span>μg/mL to 300<span class="elsevierStyleHsp" style=""></span>μg/mL was spotted on the agar plates in triplicate and plates were incubated overnight at 37<span class="elsevierStyleHsp" style=""></span>°C. After overnight incubation, inhibitory or clear zones were recorded and MIC (the lowest concentration of metal ion which completely inhibited growth) determined.</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Determination of Cd, Cr, Mn and Pb content in solutions</span><p id="par0025" class="elsevierStylePara elsevierViewall">To determine the biosorption capacity of the <span class="elsevierStyleItalic">Bacillus</span> sp. (C13 and C16), each of the subject treatment samples were analyzed using a GBC double beam 932AA Atomic Absorption Spectrophotometer coupled with a System 3000 graphite furnace accessory, a GF3000 graphite power supply and a PAL3000 furnace auto-sampler controlled by an Intel personal computer. For background correction, a deuterium lamp was used. Pyrolytically coated graphite tubes and boosted discharge hollow cathode lamps (Photron Super Lamp) were used for Cd and Pb analysis at 228.8 and 217.0<span class="elsevierStyleHsp" style=""></span>nm, respectively. Hollow cathode lamps (Photron) for Cr and Mn, at 357.9 and 279.5, respectively, were used before and after sorption equilibrium established.</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Isolation and molecular characterization</span><p id="par0030" class="elsevierStylePara elsevierViewall">Microscopic characterization was carried out by means of the Wirtz's tension using 7.6% malachite green and 0.25% saffron, observing the presence of bacterial endospores<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">[9]</span></a>. Amplification of a 16s rDNA gene sequence was performed by PCR with the conserved eubacterial primers fD1 and rD1<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">[8]</span></a>. The reactions were performed in 30<span class="elsevierStyleHsp" style=""></span>μL volumes using the Platinum PCR Supermix High Fidelity system (Invitrogen). Amplification conditions using a Bio-Rad C1000 Thermal Cycler were: 94<span class="elsevierStyleHsp" style=""></span>°C (2<span class="elsevierStyleHsp" style=""></span>min), 30 cycles of 94<span class="elsevierStyleHsp" style=""></span>°C (30 s), 45<span class="elsevierStyleHsp" style=""></span>°C (40 s), and 72<span class="elsevierStyleHsp" style=""></span>°C (2<span class="elsevierStyleHsp" style=""></span>min), with a final 5<span class="elsevierStyleHsp" style=""></span>min chain elongation at 72<span class="elsevierStyleHsp" style=""></span>°C. The amplification products were purified using the DNA clean concentrator-5 kit (Zymo Research) according to the specifications of the manufacturer. The sequencing reactions were performed by LANGEBIO, Mexico. The obtained 16s rDNA sequences were aligned against nucleotide sequences from the GenBank<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">[9]</span></a> and the Ribosomal Database Project (RDP)<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">[10]</span></a> using the ClustalX2 method<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">[11]</span></a>. Sequencing reactions were performed by the Macrogen Korea Institute (Seoul, Republic of Korea) using the Sanger technique<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">[12]</span></a>. The 16s rDNA sequences were aligned and compared by BLAST<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">[13]</span></a> against nucleotide sequences from GenBank<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">[14]</span></a>, the best results were recovered and the alignment of the sequences was performed with the ClustalW program<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">[15]</span></a>. Phylogenetic reconstruction was done with the MEGA6 program<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">[16]</span></a> using the following parameters: maximum likelihood<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">[17]</span></a> with 1000 bootstrap replicates, which shown a tree > 50% support.</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Metal Biosorption in dead biomass</span><p id="par0035" class="elsevierStylePara elsevierViewall">Two strains of <span class="elsevierStyleItalic">Bacillus</span> sp. (C13 and C16) were inoculated into 250<span class="elsevierStyleHsp" style=""></span>mL of LB medium in 250<span class="elsevierStyleHsp" style=""></span>mL Erlenmeyer flasks and incubated on a shaker at 150<span class="elsevierStyleHsp" style=""></span>rpm for 24<span class="elsevierStyleHsp" style=""></span>h at 36<span class="elsevierStyleHsp" style=""></span>°C. The cells were grown to exponential phase, harvested by centrifugation at 14000<span class="elsevierStyleHsp" style=""></span>rpm for 30<span class="elsevierStyleHsp" style=""></span>minutes at room temperature and washed three times with deionized water. Cells were dried in an oven at 80<span class="elsevierStyleHsp" style=""></span>°C for 12<span class="elsevierStyleHsp" style=""></span>hrs. Tests biosorption in batch system were performed with each strain in 250<span class="elsevierStyleHsp" style=""></span>mL Erlenmeyer flasks with 90<span class="elsevierStyleHsp" style=""></span>mL of a solution of Cd, Cr, Mn and Pb of 50<span class="elsevierStyleHsp" style=""></span>mg L<span class="elsevierStyleSup">-1</span> and adding 10<span class="elsevierStyleHsp" style=""></span>mL of 24 hour culture with a dead biomass concentration of 1<span class="elsevierStyleHsp" style=""></span>g L<span class="elsevierStyleSup">-1</span><a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">[18]</span></a>.</p><p id="par0040" class="elsevierStylePara elsevierViewall">For biosorbent activate the two treatment conditions for metal were provided for the two strains:</p><p id="par0045" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">Alkaline treatment</span>: Before contact with the metal solution, 800<span class="elsevierStyleHsp" style=""></span>μL of 0.5<span class="elsevierStyleHsp" style=""></span>M NaOH was added to 50<span class="elsevierStyleHsp" style=""></span>mg of dead biomass for 5<span class="elsevierStyleHsp" style=""></span>minutes to remove possible ions and to activate functional groups of the microorganisms according to the description by<a class="elsevierStyleCrossRefs" href="#bib0095"><span class="elsevierStyleSup">[19–22]</span></a>.</p><p id="par0050" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">Acid treatment</span>: In this treatment, 800<span class="elsevierStyleHsp" style=""></span>μL of 0.1 MHClO<span class="elsevierStyleInf">4</span> was added to 50<span class="elsevierStyleHsp" style=""></span>mg of dead bacterial biomass for a contact time of 5<span class="elsevierStyleHsp" style=""></span>minutes in each experimental flask. The experiments were performed in 125<span class="elsevierStyleHsp" style=""></span>mL. For both treatments, samples were taken every 5<span class="elsevierStyleHsp" style=""></span>minutes to measure the concentration of metals adsorbed in a 1-hour period. This was continued for 3 days by taking samples every 12<span class="elsevierStyleHsp" style=""></span>hours.</p><p id="par0055" class="elsevierStylePara elsevierViewall">Batch tests were carried out in 250<span class="elsevierStyleHsp" style=""></span>mL Erlenmeyer flasks to check the influence of starting metal concentration (50<span class="elsevierStyleHsp" style=""></span>mg L<span class="elsevierStyleSup">-1</span>), in order to check the possible maximum removal of metal ions. A control assay accompanied each experiment.</p><p id="par0060" class="elsevierStylePara elsevierViewall">At the end of each experiment, flasks were removed from the shaker and solutions were separated from the biomass by filtration through filter of 0.45<span class="elsevierStyleHsp" style=""></span>μm pore-size. 0.5<span class="elsevierStyleHsp" style=""></span>M solutions of NaOH and HCl were used to adjust pH of the medium to 10.</p><p id="par0065" class="elsevierStylePara elsevierViewall">The results obtained in this study showed that the alkaline treatment is more effective in removing metal ions from an aqueous system. Therefore, alkaline pH of 10 was selected to be the optimum pH for all further studies.</p></span></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">RESULTS AND DISCUSSION</span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Effects of metals on bacterial growth</span><p id="par0070" class="elsevierStylePara elsevierViewall">Activated sludge is a dynamic, multi-component system, whose properties are continually modified by microbial and chemical processes. Some metals are essential to microorganisms and therefore required by them, whereas others are toxic, even in small quantities. The measurement from the culture incubates for 15<span class="elsevierStyleHsp" style=""></span>hours were in agreement according to the growth resistance in solid media. However, when the strain C13 in media containing 50<span class="elsevierStyleHsp" style=""></span>mg L<span class="elsevierStyleSup">-1</span> Cd and Mn (panel a and d, <a class="elsevierStyleCrossRef" href="#fig0005">Figure 1</a>), showed a slightly longer lag phase that in absence of metals. The growth curve of the strain C13 in the media containing Cr and Pb follow the same grow pattern as the control, we did not observe inhibition for Cr and Pb at 50<span class="elsevierStyleHsp" style=""></span>mg L<span class="elsevierStyleSup">-1</span>. On the other hand, when the strain C16 was grown in media containing 50<span class="elsevierStyleHsp" style=""></span>mg L<span class="elsevierStyleSup">-1</span> Cd (panel a, <a class="elsevierStyleCrossRef" href="#fig0010">Figure 2</a>), it followed the same growth pattern as the control. However, the growth in presence of media containing 50<span class="elsevierStyleHsp" style=""></span>mg L<span class="elsevierStyleSup">-1</span> Cr, Mn and Pb (panel b, c and d, <a class="elsevierStyleCrossRef" href="#fig0010">Figure 2</a>), the growth showed a slightly longer logarithmic phase that in absence of metals. In comparison to previous studies, the <span class="elsevierStyleItalic">Bacillus</span> sp. (C13 and C16) were able to grow at high concentrations of Cd, Cr, Mn and Pb in liquid media, which might be important to survival in presence of metals under natural conditions<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">[23]</span></a>.</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><elsevierMultimedia ident="fig0010"></elsevierMultimedia></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Identification and properties of isolates</span><p id="par0075" class="elsevierStylePara elsevierViewall">To examine carbon source preferences, the isolates were grown on M9 minimal medium agar and supplemented with 0.2% of different sugars at 35<span class="elsevierStyleHsp" style=""></span>°C. As shown in <a class="elsevierStyleCrossRef" href="#tbl0005">Table I</a>, two strains were able to use all the carbon sources. The bacterial strains that were utilized in the experiments described above were identified by DNA sequence analysis of 808 to 943 by fragments of 16s rDNA prepared by PCR as described in the Materials and Methods section. Comparison of those sequences using the BLAST program indicated 99% identity of the PCR products with the rDNA sequences of <span class="elsevierStyleItalic">Bacillus</span> sp. (<a class="elsevierStyleCrossRef" href="#fig0015">Figure 3</a>).</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><elsevierMultimedia ident="fig0015"></elsevierMultimedia></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Effect of pH</span><p id="par0080" class="elsevierStylePara elsevierViewall">The effect of the pH of a solution is a major factor that determines the biosorption property of removing metals ions from an aqueous system. The pH of solution has a significant impact on metal uptake since it determines the surface charge of adsorbent, solubility of the metals ions and the degree of ionization and speciation of adsorbate<a class="elsevierStyleCrossRefs" href="#bib0120"><span class="elsevierStyleSup">[24,25]</span></a>. Cd, Cr, Mn and Pb adsorption increases linearly with in solution pH in the range of 7 to 10 as shown in <a class="elsevierStyleCrossRef" href="#fig0020">Figure 4</a> for the isolated strain <span class="elsevierStyleItalic">Bacillus</span> sp. (C13 and C16). In contrast, decreases the Cd, Cr, Mn and Pb adsorption at low pH values is due to an increase in competition for adsorption sites by H<span class="elsevierStyleSup">+</span><a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">[26]</span></a>. The results obtained in this study showed that the alkaline treatment is more effective in removing metals, as after 5<span class="elsevierStyleHsp" style=""></span>minutes the biosorption process removed 90% of the metals<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">[27]</span></a>. The possible reasons for this is that at pH less than 3, polymers are protonated and restrict entry of metallic ions, and at higher pH, the groups responsible for the retention of metals are negatively charged facilitating the binding of the metals ions<a class="elsevierStyleCrossRefs" href="#bib0120"><span class="elsevierStyleSup">[24,28–31]</span></a>. This resulted in a more favorable electrostatic attraction capacity of Cd, Cr, Mn and Pb: a concentration of 50<span class="elsevierStyleHsp" style=""></span>mg L<span class="elsevierStyleSup">-1</span> of metal forces, and so enhances, cationic metal ion adsorption at a temperature of 27 ± 1<span class="elsevierStyleHsp" style=""></span>°C.</p><elsevierMultimedia ident="fig0020"></elsevierMultimedia></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Effect of contact time</span><p id="par0085" class="elsevierStylePara elsevierViewall">The contact time was evaluated as one of the important parameters affecting the biosorption efficiency. <a class="elsevierStyleCrossRefs" href="#fig0025">Figures 5 and 6</a> show the biosorption efficiency of <span class="elsevierStyleItalic">Bacillus</span> sp. (C13 and C16) at concentrations of 50<span class="elsevierStyleHsp" style=""></span>mg L<span class="elsevierStyleSup">-1</span> and at temperature of 27±1<span class="elsevierStyleHsp" style=""></span>°C for all the metals (Cd, Cr, Mn and Pb) as a function of contact time. The Cd>Mn>Cr>Pb uptake increases with a rise in contact time up to 80<span class="elsevierStyleHsp" style=""></span>minutes, and after that it is almost constant. The fast initial metal biosorption rate was attributed to the surface binding and the following slower sorption was attributed to the interior penetration. Different kinds of functional groups, with different affinities to metal ions, are usually present on the biomass surface. According to these results, a contact time of 120<span class="elsevierStyleHsp" style=""></span>minutes was set in order to ensure that equilibrium conditions are attained. Beyond 180<span class="elsevierStyleHsp" style=""></span>minutes equilibrium no longer exists and amount of metal adsorbed decreases with time up to 2,140<span class="elsevierStyleHsp" style=""></span>minutes and aging increases.</p><elsevierMultimedia ident="fig0025"></elsevierMultimedia><elsevierMultimedia ident="fig0030"></elsevierMultimedia></span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Isotherm and Kinetics Study</span><p id="par0090" class="elsevierStylePara elsevierViewall">Several kinetic models are available to understand the behavior of biosorbents and also to examine the rate of the controlling mechanism of the adsorption process. The Langmuir constants b and qmax and the correlation coefficient R<span class="elsevierStyleSup">2</span> are given in <a class="elsevierStyleCrossRef" href="#tbl0010">Table II</a>. The calculated value of Langmuir constant b showed that adsorption is favorable, and the linearized equation presented a good correlation of the removal capacity for Cd, Cr, Mn and Pb. <a class="elsevierStyleCrossRef" href="#fig0035">Figure 7</a> shows the Langmuir adsorption isotherm. The plots of C/q versus Cf (mg L<span class="elsevierStyleSup">-1</span>) of <span class="elsevierStyleItalic">Bacillus</span> sp. (C13 and C16) for Cd, Cr, Mn and Pb resulted in straight lines.</p><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><elsevierMultimedia ident="fig0035"></elsevierMultimedia><p id="par0095" class="elsevierStylePara elsevierViewall">Langmuir Model: The Langmuir treatment is based on the assumptions that maximum adsorption corresponds to a saturated monolayer of solute molecules on the adsorbent surface, that the energy of adsorption is constant, and that there is no transmigration of adsorbate in the plane of the surface. The linear form of the Langmuir isotherm model is given by the following equation:<elsevierMultimedia ident="eq0005"></elsevierMultimedia></p><p id="par0100" class="elsevierStylePara elsevierViewall">Where b and C<span class="elsevierStyleInf">f</span> are adjustable parameters:<elsevierMultimedia ident="eq0010"></elsevierMultimedia></p></span></span><span id="sec0070" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">CONCLUSIONS</span><p id="par0105" class="elsevierStylePara elsevierViewall">The strains showed a high capacity for the uptake of heavy metals (Cd > Cr >Pb>Mn) both in single and in mixed heavy metal solution. The biosorption process depends significantly the pH of the solution and is favored at around value of 7 to 10 and 24<span class="elsevierStyleHsp" style=""></span>hours pre-culture times. Thus, the presence of metal in the growth medium allowed the maintenance of tolerance at a level comparable with that observed in isolation. The study indicated that the dead biomass of <span class="elsevierStyleItalic">Bacillus</span> sp. could be used as an efficient biosorbent material for the removal of heavy metals in aqueous solutions. The Langmuir adsorption model used for the mathematical description of the biosorption equilibrium of the adsorption isotherm metallic ions onto alkaline treatment showed the best correlation (<a class="elsevierStyleCrossRef" href="#tbl0005">Table I</a>) for the adsorption. Greater than 90% of adsorbed heavy metals were distributed both in cell wall and in cell membrane fractions. Therefore, this study reports a method that could be useful for bioremediation. Biosorption has received great attention during the last years, due to the potential use of microorganisms for cleaning metal-polluted water or wastewater streams. Biosorption, utilizing the ability of non-living biomass to accumulate heavy metals from wastewater, is considered as a more competitive, effective and economically attractive treatment method than bioaccumulation, because maintaining a viable biomass during the metal removal process can be rather difficult. The future prospect lies in the application of this microorganism for purposes like heavy metal remediation and potential use in extracting rare metals from dilute solution or removing toxic metals from industrial effluents. However, the application of these treatment processes is sometimes restricted, due to technological and economical constrains.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:9 [ 0 => array:3 [ "identificador" => "xres609035" "titulo" => "ABSTRACT" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec622563" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres609034" "titulo" => "RESUMEN" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0010" ] ] ] 3 => array:2 [ "identificador" => "sec0005" "titulo" => "INTRODUCTION" ] 4 => array:3 [ "identificador" => "sec0010" "titulo" => "MATERIALS AND METHODS" "secciones" => array:5 [ 0 => array:2 [ "identificador" => "sec0015" "titulo" => "Isolation of bacteria" ] 1 => array:2 [ "identificador" => "sec0020" "titulo" => "Effects of metals on bacterial growth" ] 2 => array:2 [ "identificador" => "sec0025" "titulo" => "Determination of Cd, Cr, Mn and Pb content in solutions" ] 3 => array:2 [ "identificador" => "sec0030" "titulo" => "Isolation and molecular characterization" ] 4 => array:2 [ "identificador" => "sec0035" "titulo" => "Metal Biosorption in dead biomass" ] ] ] 5 => array:3 [ "identificador" => "sec0040" "titulo" => "RESULTS AND DISCUSSION" "secciones" => array:5 [ 0 => array:2 [ "identificador" => "sec0045" "titulo" => "Effects of metals on bacterial growth" ] 1 => array:2 [ "identificador" => "sec0050" "titulo" => "Identification and properties of isolates" ] 2 => array:2 [ "identificador" => "sec0055" "titulo" => "Effect of pH" ] 3 => array:2 [ "identificador" => "sec0060" "titulo" => "Effect of contact time" ] 4 => array:2 [ "identificador" => "sec0065" "titulo" => "Isotherm and Kinetics Study" ] ] ] 6 => array:2 [ "identificador" => "sec0070" "titulo" => "CONCLUSIONS" ] 7 => array:2 [ "identificador" => "xack205283" "titulo" => "ACKNOWLEDGEMENTS" ] 8 => array:1 [ "titulo" => "REFERENCES" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2015-05-04" "fechaAceptado" => "2016-01-30" "PalabrasClave" => array:1 [ "en" => array:2 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec622563" "palabras" => array:5 [ 0 => "biomass" 1 => "biosorption" 2 => "dead biomass" 3 => "heavy metal" 4 => "microbial removal" ] ] 1 => array:3 [ "clase" => "keyword" "identificador" => "xpalclavsec622564" "palabras" => array:5 [ 0 => "biomasa" 1 => "biosorción" 2 => "biomasa muerta" 3 => "metales pesados" 4 => "remoción microbiana" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:2 [ "titulo" => "ABSTRACT" "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">The microorganisms are capable of accumulating heavy metal ions from water as biosorbent agents, offering a potential alternative for the detoxification and recovery of toxic/precious metals in industrial wastewater. In the present work, metal-resistant bacterial strains were isolated and identified from activated sludge of a waste treatment plant in the Municipality of Santa Rosa Jauregui, Querétaro. To obtain bacteria tolerant to metals, 37 bacterial strains and two isolates were selected based on their ability to show high tolerance (strains C-13 and C-16), maximum adsorption capacity for the studied metals. In this article, the term biosorption is used to encompass uptake by whole (dead) biomass via physicochemical mechanisms such as adsorption or ion exchange. The adsorption capacity was measured with alkaline and acid treatments to determine the conditions for maximum adsorption. The adsorption capacity with acid treatment was lower than biosorbent with alkaline treatment. A second part of the study was the biosorption of heavy metals (Cd, Cr, Mn, and Pb) from aqueous dead biomass of <span class="elsevierStyleItalic">Bacillus</span> sp (strain C13 and C16) isolated from the activated sludge in the first stage.</p></span>" ] "es" => array:2 [ "titulo" => "RESUMEN" "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Los microorganismos tienen capacidad de acumular metales pesados como agentes bioadsorbentes ofreciendo una alternativa para la remoción de metales tóxicos en aguas de efluentes industriales. El objetivo del presente trabajo fue aislar e identificar bacterias tolerantes a los metales pesados (Cd, Cr, Mn y Pb) de lodos activados provenientes de la planta de tratamiento de agua del Municipio de Santa Rosa Jáuregui, Querétaro. Para seleccionar las bacterias que son tolerantes a los metales se aislaron 37 cepas bacterianas de las cuales se seleccionaron la Cepa-13 y Cepa-16 (C-13 y C-16), que presentaron una máxima capacidad de adsorción para los metales estudiados. En este artículo, el término biosorción describe la remoción de contaminantes y la utilización de biomasas (muerta) mediante mecanismos fisicoquímicos como el proceso de adsorción o de intercambio iónico. Para obtener las condiciones de máxima adsorción se aplicó un tratamiento alcalino y uno ácido. La capacidad de adsorción fue menor en medio ácido que el bioadsorbente con tratamiento alcalino. Una segunda etapa del estudio fue la biosorción de metales pesados (Cd, Cr, Mn, y Pb) utilizando las biomasas muertas de <span class="elsevierStyleItalic">Bacillus</span> sp (cepa C13 y C16) aisladas de los lodos activados de la primera etapa.</p></span>" ] ] "multimedia" => array:11 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 4185 "Ancho" => 1706 "Tamanyo" => 345421 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">(a b,c and d). Effects of metals on cell growth to C13 and metal biosorption for Cd, Cr, Mn and Pb conditions: 50<span class="elsevierStyleHsp" style=""></span>mg L<span class="elsevierStyleSup">-1</span> of metal concentration.</p>" ] ] 1 => array:7 [ "identificador" => "fig0010" "etiqueta" => "Figure 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 4185 "Ancho" => 1707 "Tamanyo" => 340278 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">(a,b,c and d). Effects of metals on cell growth to C16 and metal biosorption for Cd, Cr, Mn and Pb conditions: 50<span class="elsevierStyleHsp" style=""></span>mg L<span class="elsevierStyleSup">-1</span> of metal concentration.</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" => 2720 "Ancho" => 3582 "Tamanyo" => 828621 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Phylogenetic tree derived from 16s rDNA sequence data of strain C13 and C16 and other related species (blue line) and external group (black line).</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" => 4184 "Ancho" => 2653 "Tamanyo" => 452420 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Effect of initial pH on equilibrium biosorption capacity for Cd, Cr, Mn and Pb conditions: 50<span class="elsevierStyleHsp" style=""></span>mg L<span class="elsevierStyleSup">-1</span> of metal concentration.</p>" ] ] 4 => array:7 [ "identificador" => "fig0025" "etiqueta" => "Figure 5" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr5.jpeg" "Alto" => 2057 "Ancho" => 3580 "Tamanyo" => 343740 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">(a,b,c and d) Effect of contact time to C13 on Cd, Cr, Mn and Pb at temperature of 27±1<span class="elsevierStyleHsp" style=""></span>°C.</p>" ] ] 5 => array:7 [ "identificador" => "fig0030" "etiqueta" => "Figure 6" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr6.jpeg" "Alto" => 2057 "Ancho" => 3580 "Tamanyo" => 344313 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">(a,b,c and d) Effect of contact time to C16 on Cd, Cr, Mn and Pb at temperature of 27±1<span class="elsevierStyleHsp" style=""></span>°C.</p>" ] ] 6 => array:7 [ "identificador" => "fig0035" "etiqueta" => "Figure 7" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr7.jpeg" "Alto" => 4381 "Ancho" => 3580 "Tamanyo" => 615805 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">Langmuir adsorption isotherm for C13 and C16 for Cd, Cr, Mn and Pb a 27 ± 1<span class="elsevierStyleHsp" style=""></span>°C.</p>" ] ] 7 => array:7 [ "identificador" => "tbl0005" "etiqueta" => "Table I" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "tabla" => array:2 [ "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="table-head " align="" valign="top" scope="col" style="border-bottom: 2px solid black"> \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " colspan="5" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Utilization of carbon source<a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">1</span></a></th><th class="td" title="table-head " colspan="4" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Metal resistance (mg L<span class="elsevierStyleSup">-1</span>)</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Strains \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Gl \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Fr \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Ga \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Xyl \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Su \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Cd \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Cr \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Mn \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Pb \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Bacillus</span> sp (C13) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">50 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">50 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">50 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">50 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Bacillus</span> sp (C16) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">50 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">50 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">50 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">50 \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab997010.png" ] ] ] "notaPie" => array:1 [ 0 => array:3 [ "identificador" => "tblfn0005" "etiqueta" => "1" "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Carbon source used in this work were Glucose (Gl); Fructose (Fr); Galactose (Ga);Xylose (Xyl) and Sucrose (Su).</p>" ] ] ] "descripcion" => array:1 [ "en" => "<p id="spar0050" class="elsevierStyleSimplePara elsevierViewall">Characterization of bacterial strains isolated from an activated sludge at a wastewater.</p>" ] ] 8 => array:7 [ "identificador" => "tbl0010" "etiqueta" => "Table II" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "tabla" => array:1 [ "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="table-head " rowspan="3" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Adsorption isotherm</th><th class="td" title="table-head " colspan="3" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">C13</th><th class="td" title="table-head " colspan="3" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">C16</th></tr><tr title="table-row"><th class="td-with-role" title="table-head ; entry_with_role_rowhead " align="left" valign="top" scope="col">Parameters \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col">Value \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " rowspan="2" align="left" valign="top" scope="col" style="border-bottom: 2px solid black">R<span class="elsevierStyleSup">2</span></th><th class="td" title="table-head " align="left" valign="top" scope="col">Parameters \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col">Value \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " rowspan="2" align="left" valign="top" scope="col" style="border-bottom: 2px solid black">R<span class="elsevierStyleSup">2</span></th></tr><tr title="table-row"><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">q<span class="elsevierStyleInf">max</span> (mg/g) \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">b (mg/L) \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">q<span class="elsevierStyleInf">max</span> (mg/g) \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">b (mg/L) \t\t\t\t\t\t\n \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Cd \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.489 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.114 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.998 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.463 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.119 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.995 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Cr \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.528 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.120 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.997 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.465 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.090 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.996 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Mn \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.459 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.054 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.997 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.528 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.149 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.998 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Pb \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.484 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.120 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.998 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.536 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.180 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0.995 \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab997011.png" ] ] ] ] "descripcion" => array:1 [ "en" => "<p id="spar0055" class="elsevierStyleSimplePara elsevierViewall">Langmuir isotherm for Cd, Cr, Mn and Pb conditions: 50<span class="elsevierStyleHsp" style=""></span>mg L<span class="elsevierStyleSup">-1</span> of metal concentration with alkaline treatment.</p>" ] ] 9 => array:5 [ "identificador" => "eq0005" "tipo" => "MULTIMEDIAFORMULA" "mostrarFloat" => false "mostrarDisplay" => true "Formula" => array:1 [ "imagen" => array:1 [ 0 => array:4 [ "Fichero" => "fx1.jpeg" "Tamanyo" => 21832 "Alto" => 336 "Ancho" => 1131 ] ] ] ] 10 => array:5 [ "identificador" => "eq0010" "tipo" => "MULTIMEDIAFORMULA" "mostrarFloat" => false "mostrarDisplay" => true "Formula" => array:1 [ "imagen" => array:1 [ 0 => array:4 [ "Fichero" => "fx2.jpeg" "Tamanyo" => 30291 "Alto" => 144 "Ancho" => 2797 ] ] ] ] ] "bibliografia" => array:2 [ "titulo" => "REFERENCES" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:31 [ 0 => array:3 [ "identificador" => "bib0005" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Sites of metal deposition in the cell wall of <span class="elsevierStyleItalic">Bacillus subtilis</span>" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:2 [ 0 => "T.J. 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To Claudio Amescua for his valuable comments about writing and document structure.</p>" "vista" => "all" ] ] ] "idiomaDefecto" => "en" "url" => "/1405888X/0000001900000001/v1_201602260016/S1405888X16000024/v1_201602260016/en/main.assets" "Apartado" => array:4 [ "identificador" => "41941" "tipo" => "SECCION" "en" => array:2 [ "titulo" => "Artículos originales" "idiomaDefecto" => true ] "idiomaDefecto" => "en" ] "PDF" => "https://static.elsevier.es/multimedia/1405888X/0000001900000001/v1_201602260016/S1405888X16000024/v1_201602260016/en/main.pdf?idApp=UINPBA00004N&text.app=https://www.elsevier.es/" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S1405888X16000024?idApp=UINPBA00004N" ]
| Year/Month | Html | Total | |
|---|---|---|---|
| 2024 November | 2 | 1 | 3 |
| 2024 October | 18 | 3 | 21 |
| 2024 September | 17 | 6 | 23 |
| 2024 August | 32 | 4 | 36 |
| 2024 July | 26 | 7 | 33 |
| 2024 June | 14 | 5 | 19 |
| 2024 May | 17 | 2 | 19 |
| 2024 April | 10 | 4 | 14 |
| 2024 March | 29 | 14 | 43 |
| 2024 February | 19 | 13 | 32 |
| 2024 January | 53 | 7 | 60 |
| 2023 December | 24 | 11 | 35 |
| 2023 November | 31 | 8 | 39 |
| 2023 October | 37 | 4 | 41 |
| 2023 September | 30 | 5 | 35 |
| 2023 August | 28 | 6 | 34 |
| 2023 July | 32 | 4 | 36 |
| 2023 June | 23 | 2 | 25 |
| 2023 May | 54 | 9 | 63 |
| 2023 April | 48 | 5 | 53 |
| 2023 March | 49 | 5 | 54 |
| 2023 February | 41 | 7 | 48 |
| 2023 January | 46 | 2 | 48 |
| 2022 December | 37 | 9 | 46 |
| 2022 November | 41 | 9 | 50 |
| 2022 October | 12 | 10 | 22 |
| 2022 September | 21 | 14 | 35 |
| 2022 August | 16 | 18 | 34 |
| 2022 July | 26 | 10 | 36 |
| 2022 June | 27 | 16 | 43 |
| 2022 May | 34 | 7 | 41 |
| 2022 April | 64 | 26 | 90 |
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| 2022 February | 113 | 7 | 120 |
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| 2021 December | 61 | 17 | 78 |
| 2021 November | 60 | 11 | 71 |
| 2021 October | 29 | 14 | 43 |
| 2021 September | 45 | 18 | 63 |
| 2021 August | 21 | 12 | 33 |
| 2021 July | 27 | 10 | 37 |
| 2021 June | 28 | 11 | 39 |
| 2021 May | 25 | 16 | 41 |
| 2021 April | 66 | 18 | 84 |
| 2021 March | 17 | 15 | 32 |
| 2021 February | 13 | 8 | 21 |
| 2021 January | 19 | 14 | 33 |
| 2020 December | 24 | 12 | 36 |
| 2020 November | 21 | 12 | 33 |
| 2020 October | 6 | 7 | 13 |
| 2020 September | 16 | 9 | 25 |
| 2020 August | 15 | 9 | 24 |
| 2020 July | 9 | 6 | 15 |
| 2020 June | 17 | 7 | 24 |
| 2020 May | 14 | 12 | 26 |
| 2020 April | 12 | 9 | 21 |
| 2020 March | 12 | 8 | 20 |
| 2020 February | 13 | 11 | 24 |
| 2020 January | 18 | 10 | 28 |
| 2019 December | 17 | 16 | 33 |
| 2019 November | 14 | 5 | 19 |
| 2019 October | 14 | 7 | 21 |
| 2019 September | 17 | 14 | 31 |
| 2019 August | 12 | 3 | 15 |
| 2019 July | 12 | 6 | 18 |
| 2019 June | 67 | 16 | 83 |
| 2019 May | 114 | 25 | 139 |
| 2019 April | 50 | 17 | 67 |
| 2019 March | 11 | 7 | 18 |
| 2019 February | 192 | 19 | 211 |
| 2019 January | 82 | 15 | 97 |
| 2018 December | 14 | 8 | 22 |
| 2018 November | 9 | 0 | 9 |
| 2018 October | 24 | 10 | 34 |
| 2018 September | 23 | 6 | 29 |
| 2018 August | 4 | 0 | 4 |
| 2018 July | 6 | 0 | 6 |
| 2018 June | 4 | 2 | 6 |
| 2018 May | 6 | 4 | 10 |
| 2018 April | 10 | 0 | 10 |
| 2018 March | 13 | 2 | 15 |
| 2018 February | 20 | 0 | 20 |
| 2018 January | 4 | 4 | 8 |
| 2017 December | 9 | 0 | 9 |
| 2017 November | 13 | 3 | 16 |
| 2017 October | 17 | 1 | 18 |
| 2017 September | 19 | 5 | 24 |
| 2017 August | 16 | 3 | 19 |
| 2017 July | 14 | 2 | 16 |
| 2017 June | 50 | 4 | 54 |
| 2017 May | 29 | 1 | 30 |
| 2017 April | 14 | 7 | 21 |
| 2017 March | 18 | 30 | 48 |
| 2017 February | 26 | 2 | 28 |
| 2017 January | 32 | 3 | 35 |
| 2016 December | 40 | 7 | 47 |
| 2016 November | 32 | 11 | 43 |
| 2016 October | 43 | 8 | 51 |
| 2016 September | 50 | 6 | 56 |
| 2016 August | 33 | 9 | 42 |
| 2016 July | 65 | 7 | 72 |
| 2016 June | 61 | 21 | 82 |
| 2016 May | 45 | 38 | 83 |
| 2016 April | 38 | 19 | 57 |
| 2016 March | 39 | 14 | 53 |
| 2016 February | 8 | 6 | 14 |
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