Adsorción de metales pesados utilizando sustancias poliméricas extracelulares inmovilizadas en un polisacárido aniónico

Josselyn Andreina Arteaga Mesías; Lady Laura Delgado Macías; Ernesto Alonso Rosero Delgado; Naga Raju Maddela

Enviado enero 18, 2022

Publicado 2022-01-14

Artículos

Vol. 9 Núm. 1 (2022): Revista Colón Ciencias, Tecnología y Negocios

Adsorción de metales pesados utilizando sustancias poliméricas extracelulares inmovilizadas en un polisacárido aniónico

Josselyn Andreina Arteaga Mesías⁺⁻
Lady Laura Delgado Macías⁺⁻
Ernesto Alonso Rosero Delgado⁺⁻
Naga Raju Maddela⁺⁻

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DOI: ND

Publicado: 2022-01-14

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Arteaga Mesías, J. A., Delgado Macías, L. L., Rosero Delgado, E. A., & Maddela, N. R. (2022). Adsorción de metales pesados utilizando sustancias poliméricas extracelulares inmovilizadas en un polisacárido aniónico. Revista Colón Ciencias, Tecnología Y Negocios, 9(1), 114–133. Recuperado a partir de https://revistas.up.ac.pa/index.php/revista_colon_ctn/article/view/2627

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En este estudio se evaluó el efecto de las sustancias poliméricas extracelulares (EPS), inmovilizadas en un soporte de alginato de sodio, sobre la concentración de plomo (Pb²⁺), cromo (Cr⁴⁺) y cobre (Cu²⁺) presentes en una matriz acuosa sintética. La concentración de carbohidratos totales más alta en EPS fue de 42.72 ± 0.17 ug/L de la cepa E6. Las perlas inmovilizadas con EPS tuvieron valores de humedad crecientes en dependencia del aumento de la concentración. La mayor remoción de los contaminantes se consiguió con el EPS obtenido de la cepa M2-3, de concentración 15% (remoción= 98.97% Pb²⁺, 98.05% Cr⁴⁺ y 97.25% Cu²⁺) y una capacidad de adsorción del metal pesado de 0.240 mg/g (PS) para Pb²⁺, 0.237 mg/g (PS) Cr⁴⁺ y 0.471 mg/g (PS) Cu²⁺. Estos hallazgos demuestran el gran potencial de las perlas con EPS inmovilizados, para su utilización como biosorbente en el tratamiento de aguas contaminadas con metales pesados.

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Watt, G., Britton, A., Gilmour, H., Moore , M., Murray, G., & Robertson, S. (2000). Public health implications of new guidelines for lead in drinking water: a case study in an area with historically high water lead levels. Food and Chemical Toxicology, 38(1), S73-S79.
Wingender, J., Neu, T., & Flemming, H. (1999). Microbial Extracellular Polymeric Substances: Characterization, Structure, and Function.
Ahmaruzzaman, M. (2011). Industrial wastes as low-cost potential adsorbents for the treatment of wastewater laden with heavy metals. Advances in Colloid and Interface Science, 166(1-2), 36–59.
Anurag, P., Debabrata , B., Anupam, S., & Lalitagauri , R. (2007). Studies on Cr(VI), Pb(II) and Cu(II) adsorption–desorption using calcium alginate as biopolymer. Chemical Speciation & Bioavailability, 19(1), 17-24.
APHA. (2005). Standard Methods for the Examination of Water and Wastewater, 21st ed. Washington, DC.
Arıca, M., Arpa, Ç., Ergene, A., Bayramog˘lu, G., & Genç, Ö. (2003). Ca-alginate as a support for Pb (II) and Zn (II) biosorption with immobilized Phanerochaete chrysosporium . Carbohydr. Polym. , 52, 167–174.
Bala, S. S., Yan, S., Tyagi, R., & Surampalli, R. (2010). Extracellular polymeric substances (EPS) producing bacterial strains of municipal wastewater sludge: isolation, molecular identification, EPS characterization and performance for sludge settling and dewatering. Water Resources, 44, 2253–2266.
Biswas, J. K., Banerjee, A., Sarkar, B., Sarkar, D., Sarkar, S. K., Rai, M., & Vithanage, M. (2020). Exploration of an Extracellular Polymeric Substance from Earthworm Gut Bacterium (Bacillus licheniformis) for Bioflocculation and Heavy Metal Removal Potential. Applied. Sciences, 10, 349.
Bohli, T., Ouederni, A., Fiol, N., & Villaescusa, I. (2015). Evaluation of an activated carbon from olive stones used as an adsorbent for heavy metal removal from aqueous phases. Comptes Rendus Chimie, 18(1), 88–99 .
Bradl, H. (2005). Heavy Metals in the Environment: Origin, Interaction and Remediation. London: Elsevier/Academic Press.
Cain, D., Hanks, H., Weis, M., Bottoms, C., & Lawson, J. (2009). Microbiology laboratory manual. McKinney, TX: Collin County Community College District.
Chuah, T. G., Jumasiah, A., Azni, I., Katayon, S., & Choong, S. Y. (2005). Rice husk as a potentially low-cost biosorbent for heavy metal and dye removal: an overview. Desalination, 175(3), 305–316.
Concórdio, P., & Freitas, F. (2019). Environmental Applications: Biopolymer Sorbents for Heavy Metal Removal. FL, USA: CRC Press: Boca Raton.
Concórdio, R. P., Reis, M. A., & Freitas, F. (2020). Biosorption of Heavy Metals by the Bacterial Exopolysaccharide FucoPol. Applied Sciences, 10, 6708.
Czaczyk, K., & Myszka, K. (2007). Biosynthesis of extracellular polymeric substances (EPS) and its role in microbial biofilm formation. Polish Journal of Environmental Studies, 16, 799-806.
Delgado, V. A., & Mieles, L. E. (2011). Identificación de metales pesados para establecer el nivel de contaminación en el río Portoviejo entre los puentes Velasco Ibarra y El Salto en la ciudad de Portoviejo durante el período 2009 - 2010. La Técnica, 64-69.
Dubois, M., Gilles, K., Hamilton, J., Rebers, P., & Smith, F. (1956). Colorimetric method for determination of sugars and related substances. Analytical Chemistry, 28, 350–356.
Freitas, F., Alves, V. D., & Reis, M. A. (2011). Advances in bacterial exopolysaccharides: from production to biotechnological applications. Trends in Biotechnology, 29, 388-398.
Freitas, F., Alves, V. D., Torres, C. A., Cruz, M., Sousa, I., Melo, M. J., Ramos, A.M. & Reis, M. A. (2011). (Fucose-containing exopolysaccharide produced by the newly isolated Enterobacter strain A47 DSM 23139. Carbohydrate Polymers, 83, 159-165.
Freitas, F., Alves, V., Pais, J., Costa, N., Oliveira, C., Mafra, L., Hilliou, L., Oliveira, R. & Reis, M. (2009). Characterization of an extracellular polysaccharide produced by a Pseudomonas strain grown on glycerol. Bioresource technology, 100, 859-865.
Gorman, R., & Adley, C. C. (2004). An evaluation of five preservation techniques and conventional freezing temperatures of− 20° C and− 85° C for long‐term preservation of Campylobacter jejuni. Letters in applied microbiology, 38(4), 306-310.
Gupta, P., & Diwan, B. (2017). Bacterial Exopolysaccharide mediated heavy metal removal: A Review on biosynthesis,mechanism and remediation strategies. Biotechnology Reports, 13, 58–71.
Hu, Z., Jin, J., Abruna, H., Houston, P., Hay, A., & Ghiorse, W. (2007). Spatial distributions of copper in microbial biofilms by scanning electrochemical microscopy. Environmental Sciences Technology, 41, 936-41.
Kumari, S., Mahapatra, S., & Das , S. (2017). Ca-alginate as a support matrix for Pb(II) biosorption with immobilized biofilm associated extracellular polymeric substances of Pseudomonas aeruginosa N6P6. Chemical Engineering Journal, 328, 556-566.
Lombardi, P., Peri, S., & Guerrero, N. (2010). ALA-D and ALA-D reactivated as biomarkers of lead contamination in the fish Prochilodus lineatus. Ecotoxicology and Environmental Safety, 73 (7), 1704–1711.
Maddela, N., Zhou, Z., Yu, Z., Zhao, S., & Meng, F. (2018). Functional determinants of extracellular polymeric substances to membrane biofouling: Experimental evidence from pure-cultured sludge bacteria. Applied and Environmental Microbiology Biotechnol., 84(15). doi:10.1128/AEM.00756-18
Mehta, S. K., & Gaur, J. P. (2005). Use of Algae for Removing Heavy Metal Ions from Wastewater: Progress and Prospects. Critical Review in Biotechnology, 25 (3), 113–152. doi: 10.1080/07388550500248571
Mohammed, S. (2012.). Removal of cadmium from simulated wastewater using biosorption. [Master Thesis, University of Baghdad].
Morillo, J. A., García, R., Quesada, T., Aguilera, M., Ramos, A., & Monteoliva, M. (2008). Biosorption of heavy metals by the exopolysaccharide produced by Paenibacillus jamilae. World Journal of Microbiology and Biotechnology, 24(11), 2699–2704. doi: 10.1007/s11274-008-9800-9
Nielsen , P., & Jahn, A. (1999). Microbial extracellular polymeric substances: characterization, structure and function. In Extraction of EPS (pp. 49-72). Berlin Heidelberg: Springer-Verlag.
Öner, E. T. (2013). Microbial production of extracellular polysaccharides from biomass. In Pretreatment Techniques for Biofuels and Biorefineries. 35-56. Springer.
Ozdemir, G., Ceyhan, N., & Manav, E. (2005). Utilization in alginate beads for Cu (II) and Ni (II) adsorption of an exopolysaccharide produced by Chryseomonas luteola TEM05 . World Journal of Microbiology and Biotechnology., 21 (2), 163–167. doi: 10.1007/s11274-004-1563-3
Percival, E. (1979). The polysaccharides of green, red and brown seaweeds: their basic structure, biosynthesis and function. British Phycological Journal, 14(2), 103-117.
Salehizadeh, H., & Shojaosadati, S. A. (2003). Removal of metal ions from aqueous solution by polysaccharide produced from Bacillus firmus. Water Resources, 37, 4231–4235.
Sheng, G.-P., Yu , H.-Q., & Li, X.-Y. (2010). Extracellular polymeric substances (EPS) of microbial aggregates in biological wastewater treatment systems: a review. Biotechnology Advances. Biotechnology Advances, 28, 882-894.
Tchounwou, P. B., Yedjou, C. G., Patlolla, A. K., & Sutton, D. J. ( 2012). Heavy Metal Toxicity and the Environment. Molecular, Clinical and Environmental Toxicology, 101, 133–164. doi: 10.1007/978-3-7643-8340-4_6.
Tortora, G. J., Funke, B. R., & Case, C. L. (2007). Introducción a la microbiología. Buenos Aires: Editorial Medica Panamericana.
Wei, W., Wang, Q., Li, A., Yang, J., Ma, F., Pi, S., & Wu, D. (2016). Biosorption of Pb (II) from aqueous solution by extracellular polymeric substances extracted from Klebsiella sp. J1: Adsorption behavior and mechanism assessment. Scientific Reports, 6(31575). https://doi.org/10.1038/srep31575
Watt, G., Britton, A., Gilmour, H., Moore , M., Murray, G., & Robertson, S. (2000). Public health implications of new guidelines for lead in drinking water: a case study in an area with historically high water lead levels. Food and Chemical Toxicology, 38(1), S73-S79.
Wingender, J., Neu, T., & Flemming, H. (1999). Microbial Extracellular Polymeric Substances: Characterization, Structure, and Function.
Ahmaruzzaman, M. (2011). Industrial wastes as low-cost potential adsorbents for the treatment of wastewater laden with heavy metals. Advances in Colloid and Interface Science, 166(1-2), 36–59.
Anurag, P., Debabrata , B., Anupam, S., & Lalitagauri , R. (2007). Studies on Cr(VI), Pb(II) and Cu(II) adsorption–desorption using calcium alginate as biopolymer. Chemical Speciation & Bioavailability, 19(1), 17-24.
APHA. (2005). Standard Methods for the Examination of Water and Wastewater, 21st ed. Washington, DC.
Arıca, M., Arpa, Ç., Ergene, A., Bayramog˘lu, G., & Genç, Ö. (2003). Ca-alginate as a support for Pb (II) and Zn (II) biosorption with immobilized Phanerochaete chrysosporium . Carbohydr. Polym. , 52, 167–174.
Bala, S. S., Yan, S., Tyagi, R., & Surampalli, R. (2010). Extracellular polymeric substances (EPS) producing bacterial strains of municipal wastewater sludge: isolation, molecular identification, EPS characterization and performance for sludge settling and dewatering. Water Resources, 44, 2253–2266.
Biswas, J. K., Banerjee, A., Sarkar, B., Sarkar, D., Sarkar, S. K., Rai, M., & Vithanage, M. (2020). Exploration of an Extracellular Polymeric Substance from Earthworm Gut Bacterium (Bacillus licheniformis) for Bioflocculation and Heavy Metal Removal Potential. Applied. Sciences, 10, 349.
Bohli, T., Ouederni, A., Fiol, N., & Villaescusa, I. (2015). Evaluation of an activated carbon from olive stones used as an adsorbent for heavy metal removal from aqueous phases. Comptes Rendus Chimie, 18(1), 88–99 .
Bradl, H. (2005). Heavy Metals in the Environment: Origin, Interaction and Remediation. London: Elsevier/Academic Press.
Cain, D., Hanks, H., Weis, M., Bottoms, C., & Lawson, J. (2009). Microbiology laboratory manual. McKinney, TX: Collin County Community College District.
Chuah, T. G., Jumasiah, A., Azni, I., Katayon, S., & Choong, S. Y. (2005). Rice husk as a potentially low-cost biosorbent for heavy metal and dye removal: an overview. Desalination, 175(3), 305–316.
Concórdio, P., & Freitas, F. (2019). Environmental Applications: Biopolymer Sorbents for Heavy Metal Removal. FL, USA: CRC Press: Boca Raton.
Concórdio, R. P., Reis, M. A., & Freitas, F. (2020). Biosorption of Heavy Metals by the Bacterial Exopolysaccharide FucoPol. Applied Sciences, 10, 6708.
Czaczyk, K., & Myszka, K. (2007). Biosynthesis of extracellular polymeric substances (EPS) and its role in microbial biofilm formation. Polish Journal of Environmental Studies, 16, 799-806.
Delgado, V. A., & Mieles, L. E. (2011). Identificación de metales pesados para establecer el nivel de contaminación en el río Portoviejo entre los puentes Velasco Ibarra y El Salto en la ciudad de Portoviejo durante el período 2009 - 2010. La Técnica, 64-69.
Dubois, M., Gilles, K., Hamilton, J., Rebers, P., & Smith, F. (1956). Colorimetric method for determination of sugars and related substances. Analytical Chemistry, 28, 350–356.
Freitas, F., Alves, V. D., & Reis, M. A. (2011). Advances in bacterial exopolysaccharides: from production to biotechnological applications. Trends in Biotechnology, 29, 388-398.
Freitas, F., Alves, V. D., Torres, C. A., Cruz, M., Sousa, I., Melo, M. J., Ramos, A.M. & Reis, M. A. (2011). (Fucose-containing exopolysaccharide produced by the newly isolated Enterobacter strain A47 DSM 23139. Carbohydrate Polymers, 83, 159-165.
Freitas, F., Alves, V., Pais, J., Costa, N., Oliveira, C., Mafra, L., Hilliou, L., Oliveira, R. & Reis, M. (2009). Characterization of an extracellular polysaccharide produced by a Pseudomonas strain grown on glycerol. Bioresource technology, 100, 859-865.
Gorman, R., & Adley, C. C. (2004). An evaluation of five preservation techniques and conventional freezing temperatures of− 20° C and− 85° C for long‐term preservation of Campylobacter jejuni. Letters in applied microbiology, 38(4), 306-310.
Gupta, P., & Diwan, B. (2017). Bacterial Exopolysaccharide mediated heavy metal removal: A Review on biosynthesis,mechanism and remediation strategies. Biotechnology Reports, 13, 58–71.
Hu, Z., Jin, J., Abruna, H., Houston, P., Hay, A., & Ghiorse, W. (2007). Spatial distributions of copper in microbial biofilms by scanning electrochemical microscopy. Environmental Sciences Technology, 41, 936-41.
Kumari, S., Mahapatra, S., & Das , S. (2017). Ca-alginate as a support matrix for Pb(II) biosorption with immobilized biofilm associated extracellular polymeric substances of Pseudomonas aeruginosa N6P6. Chemical Engineering Journal, 328, 556-566.
Lombardi, P., Peri, S., & Guerrero, N. (2010). ALA-D and ALA-D reactivated as biomarkers of lead contamination in the fish Prochilodus lineatus. Ecotoxicology and Environmental Safety, 73 (7), 1704–1711.
Maddela, N., Zhou, Z., Yu, Z., Zhao, S., & Meng, F. (2018). Functional determinants of extracellular polymeric substances to membrane biofouling: Experimental evidence from pure-cultured sludge bacteria. Applied and Environmental Microbiology Biotechnol., 84(15). doi:10.1128/AEM.00756-18
Mehta, S. K., & Gaur, J. P. (2005). Use of Algae for Removing Heavy Metal Ions from Wastewater: Progress and Prospects. Critical Review in Biotechnology, 25 (3), 113–152. doi: 10.1080/07388550500248571
Mohammed, S. (2012.). Removal of cadmium from simulated wastewater using biosorption. [Master Thesis, University of Baghdad].
Morillo, J. A., García, R., Quesada, T., Aguilera, M., Ramos, A., & Monteoliva, M. (2008). Biosorption of heavy metals by the exopolysaccharide produced by Paenibacillus jamilae. World Journal of Microbiology and Biotechnology, 24(11), 2699–2704. doi: 10.1007/s11274-008-9800-9
Nielsen , P., & Jahn, A. (1999). Microbial extracellular polymeric substances: characterization, structure and function. In Extraction of EPS (pp. 49-72). Berlin Heidelberg: Springer-Verlag.
Öner, E. T. (2013). Microbial production of extracellular polysaccharides from biomass. In Pretreatment Techniques for Biofuels and Biorefineries. 35-56. Springer.
Ozdemir, G., Ceyhan, N., & Manav, E. (2005). Utilization in alginate beads for Cu (II) and Ni (II) adsorption of an exopolysaccharide produced by Chryseomonas luteola TEM05 . World Journal of Microbiology and Biotechnology., 21 (2), 163–167. doi: 10.1007/s11274-004-1563-3
Percival, E. (1979). The polysaccharides of green, red and brown seaweeds: their basic structure, biosynthesis and function. British Phycological Journal, 14(2), 103-117.
Salehizadeh, H., & Shojaosadati, S. A. (2003). Removal of metal ions from aqueous solution by polysaccharide produced from Bacillus firmus. Water Resources, 37, 4231–4235.
Sheng, G.-P., Yu , H.-Q., & Li, X.-Y. (2010). Extracellular polymeric substances (EPS) of microbial aggregates in biological wastewater treatment systems: a review. Biotechnology Advances. Biotechnology Advances, 28, 882-894.
Tchounwou, P. B., Yedjou, C. G., Patlolla, A. K., & Sutton, D. J. ( 2012). Heavy Metal Toxicity and the Environment. Molecular, Clinical and Environmental Toxicology, 101, 133–164. doi: 10.1007/978-3-7643-8340-4_6.
Tortora, G. J., Funke, B. R., & Case, C. L. (2007). Introducción a la microbiología. Buenos Aires: Editorial Medica Panamericana.
Wei, W., Wang, Q., Li, A., Yang, J., Ma, F., Pi, S., & Wu, D. (2016). Biosorption of Pb (II) from aqueous solution by extracellular polymeric substances extracted from Klebsiella sp. J1: Adsorption behavior and mechanism assessment. Scientific Reports, 6(31575). https://doi.org/10.1038/srep31575
Yan, G., & Viraraghavan, T. (2001). Heavy metal removal in a biosorption column by immobilized M. rouxii biomass. Bioresource Technology, 78 (3), 243–249. https://doi.org/10.1016/S0960-8524(01)00020-7

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[1] Watt, G., Britton, A., Gilmour, H., Moore , M., Murray, G., & Robertson, S. (2000). Public health implications of new guidelines for lead in drinking water: a case study in an area with historically high water lead levels. Food and Chemical Toxicology, 38(1), S73-S79.

[2] Wingender, J., Neu, T., & Flemming, H. (1999). Microbial Extracellular Polymeric Substances: Characterization, Structure, and Function.

[3] Ahmaruzzaman, M. (2011). Industrial wastes as low-cost potential adsorbents for the treatment of wastewater laden with heavy metals. Advances in Colloid and Interface Science, 166(1-2), 36–59.

[4] Anurag, P., Debabrata , B., Anupam, S., & Lalitagauri , R. (2007). Studies on Cr(VI), Pb(II) and Cu(II) adsorption–desorption using calcium alginate as biopolymer. Chemical Speciation & Bioavailability, 19(1), 17-24.

[5] APHA. (2005). Standard Methods for the Examination of Water and Wastewater, 21st ed. Washington, DC.

[6] Arıca, M., Arpa, Ç., Ergene, A., Bayramog˘lu, G., & Genç, Ö. (2003). Ca-alginate as a support for Pb (II) and Zn (II) biosorption with immobilized Phanerochaete chrysosporium . Carbohydr. Polym. , 52, 167–174.

[7] Bala, S. S., Yan, S., Tyagi, R., & Surampalli, R. (2010). Extracellular polymeric substances (EPS) producing bacterial strains of municipal wastewater sludge: isolation, molecular identification, EPS characterization and performance for sludge settling and dewatering. Water Resources, 44, 2253–2266.

[8] Biswas, J. K., Banerjee, A., Sarkar, B., Sarkar, D., Sarkar, S. K., Rai, M., & Vithanage, M. (2020). Exploration of an Extracellular Polymeric Substance from Earthworm Gut Bacterium (Bacillus licheniformis) for Bioflocculation and Heavy Metal Removal Potential. Applied. Sciences, 10, 349.

[9] Bohli, T., Ouederni, A., Fiol, N., & Villaescusa, I. (2015). Evaluation of an activated carbon from olive stones used as an adsorbent for heavy metal removal from aqueous phases. Comptes Rendus Chimie, 18(1), 88–99 .

[10] Bradl, H. (2005). Heavy Metals in the Environment: Origin, Interaction and Remediation. London: Elsevier/Academic Press.

[11] Cain, D., Hanks, H., Weis, M., Bottoms, C., & Lawson, J. (2009). Microbiology laboratory manual. McKinney, TX: Collin County Community College District.

[12] Chuah, T. G., Jumasiah, A., Azni, I., Katayon, S., & Choong, S. Y. (2005). Rice husk as a potentially low-cost biosorbent for heavy metal and dye removal: an overview. Desalination, 175(3), 305–316.

[13] Concórdio, P., & Freitas, F. (2019). Environmental Applications: Biopolymer Sorbents for Heavy Metal Removal. FL, USA: CRC Press: Boca Raton.

[14] Concórdio, R. P., Reis, M. A., & Freitas, F. (2020). Biosorption of Heavy Metals by the Bacterial Exopolysaccharide FucoPol. Applied Sciences, 10, 6708.

[15] Czaczyk, K., & Myszka, K. (2007). Biosynthesis of extracellular polymeric substances (EPS) and its role in microbial biofilm formation. Polish Journal of Environmental Studies, 16, 799-806.

[16] Delgado, V. A., & Mieles, L. E. (2011). Identificación de metales pesados para establecer el nivel de contaminación en el río Portoviejo entre los puentes Velasco Ibarra y El Salto en la ciudad de Portoviejo durante el período 2009 - 2010. La Técnica, 64-69.

[17] Dubois, M., Gilles, K., Hamilton, J., Rebers, P., & Smith, F. (1956). Colorimetric method for determination of sugars and related substances. Analytical Chemistry, 28, 350–356.

[18] Freitas, F., Alves, V. D., & Reis, M. A. (2011). Advances in bacterial exopolysaccharides: from production to biotechnological applications. Trends in Biotechnology, 29, 388-398.

[19] Freitas, F., Alves, V. D., Torres, C. A., Cruz, M., Sousa, I., Melo, M. J., Ramos, A.M. & Reis, M. A. (2011). (Fucose-containing exopolysaccharide produced by the newly isolated Enterobacter strain A47 DSM 23139. Carbohydrate Polymers, 83, 159-165.

[20] Freitas, F., Alves, V., Pais, J., Costa, N., Oliveira, C., Mafra, L., Hilliou, L., Oliveira, R. & Reis, M. (2009). Characterization of an extracellular polysaccharide produced by a Pseudomonas strain grown on glycerol. Bioresource technology, 100, 859-865.

[21] Gorman, R., & Adley, C. C. (2004). An evaluation of five preservation techniques and conventional freezing temperatures of− 20° C and− 85° C for long‐term preservation of Campylobacter jejuni. Letters in applied microbiology, 38(4), 306-310.

[22] Gupta, P., & Diwan, B. (2017). Bacterial Exopolysaccharide mediated heavy metal removal: A Review on biosynthesis,mechanism and remediation strategies. Biotechnology Reports, 13, 58–71.

[23] Hu, Z., Jin, J., Abruna, H., Houston, P., Hay, A., & Ghiorse, W. (2007). Spatial distributions of copper in microbial biofilms by scanning electrochemical microscopy. Environmental Sciences Technology, 41, 936-41.

[24] Kumari, S., Mahapatra, S., & Das , S. (2017). Ca-alginate as a support matrix for Pb(II) biosorption with immobilized biofilm associated extracellular polymeric substances of Pseudomonas aeruginosa N6P6. Chemical Engineering Journal, 328, 556-566.

[25] Lombardi, P., Peri, S., & Guerrero, N. (2010). ALA-D and ALA-D reactivated as biomarkers of lead contamination in the fish Prochilodus lineatus. Ecotoxicology and Environmental Safety, 73 (7), 1704–1711.

[26] Maddela, N., Zhou, Z., Yu, Z., Zhao, S., & Meng, F. (2018). Functional determinants of extracellular polymeric substances to membrane biofouling: Experimental evidence from pure-cultured sludge bacteria. Applied and Environmental Microbiology Biotechnol., 84(15). doi:10.1128/AEM.00756-18

[27] Mehta, S. K., & Gaur, J. P. (2005). Use of Algae for Removing Heavy Metal Ions from Wastewater: Progress and Prospects. Critical Review in Biotechnology, 25 (3), 113–152. doi: 10.1080/07388550500248571

[28] Mohammed, S. (2012.). Removal of cadmium from simulated wastewater using biosorption. [Master Thesis, University of Baghdad].

[29] Morillo, J. A., García, R., Quesada, T., Aguilera, M., Ramos, A., & Monteoliva, M. (2008). Biosorption of heavy metals by the exopolysaccharide produced by Paenibacillus jamilae. World Journal of Microbiology and Biotechnology, 24(11), 2699–2704. doi: 10.1007/s11274-008-9800-9

[30] Nielsen , P., & Jahn, A. (1999). Microbial extracellular polymeric substances: characterization, structure and function. In Extraction of EPS (pp. 49-72). Berlin Heidelberg: Springer-Verlag.

[31] Öner, E. T. (2013). Microbial production of extracellular polysaccharides from biomass. In Pretreatment Techniques for Biofuels and Biorefineries. 35-56. Springer.

[32] Ozdemir, G., Ceyhan, N., & Manav, E. (2005). Utilization in alginate beads for Cu (II) and Ni (II) adsorption of an exopolysaccharide produced by Chryseomonas luteola TEM05 . World Journal of Microbiology and Biotechnology., 21 (2), 163–167. doi: 10.1007/s11274-004-1563-3

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