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

Submitted January 18, 2022

Published 2022-01-14

Artículos

Vol. 9 No. 1 (2022): Revista Colón Ciencias, Tecnología y Negocios

Adsorption of heavy metals using extracellular polymeric substances immobilized in an anionic polysaccharide

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

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DOI: ND

Published: 2022-01-14

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Arteaga Mesías, J. A., Delgado Macías, L. L., Rosero Delgado, E. A., & Maddela, N. R. (2022). Adsorption of heavy metals using extracellular polymeric substances immobilized in an anionic polysaccharide. Revista Colón Ciencias, Tecnología Y Negocios, 9(1), 114–133. Retrieved from https://revistas.up.ac.pa/index.php/revista_colon_ctn/article/view/2627

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Abstract

In this study, the effect of extracellular polymeric substances (EPS), immobilized on a sodium alginate support, on the concentration of lead (Pb²⁺), chromium (Cr⁴⁺) and copper (Cu²⁺) present in a synthetic aqueous matrix was evaluated. The highest total carbohydrate concentration in EPS was 42.72 ± 0.17 ug/L of the E6 strain. The EPS immobilized beads had increasing moisture values as a function of increasing concentration. The highest removal of contaminants was achieved with the EPS obtained from the strain M2-3, with a concentration of 15% (removal = 98.97% Pb²⁺, 98.05% Cr⁴⁺ and 97.25% Cu²⁺) and an adsorption capacity of the heavy metal of 0.240 mg / g (PS) for Pb²⁺, 0.237 mg/g (PS) Cr⁴⁺ and 0.471 mg/g (PS) Cu²⁺. These findings demonstrate the great potential of the beads with immobilized EPS, for their use as a biosorbent in the treatment of water contaminated with heavy metals.

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References

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

[33] Percival, E. (1979). The polysaccharides of green, red and brown seaweeds: their basic structure, biosynthesis and function. British Phycological Journal, 14(2), 103-117.

[34] Salehizadeh, H., & Shojaosadati, S. A. (2003). Removal of metal ions from aqueous solution by polysaccharide produced from Bacillus firmus. Water Resources, 37, 4231–4235.

[35] 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.

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