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Effect of Heavy Metals on the Growth of Bacteria Isolated from Sewage Sludge Compost Tea

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DOI: 10.4236/aim.2014.410070    4,531 Downloads   5,911 Views   Citations


The amount of urban sewage sludge is increasing daily. For this reason, it is necessary to have an environmentally friendly use for this residue. Land applications in olive grove soil, poor quality soil, as a compost or a compost tea could be considered as one of the best options, because it has a high content of organic matter. However, the presence of heavy metals in some sewage sludge could be an environmental problem. In this sense, the aim of this work is to check the tolerance of the culturable microbiota present in sewage sludge compost tea to four heavy metals, Cu, Cd, Pb and Zn. Among microbiota isolated, eight strains showed high resistance to Pb, Zn, Cu and Cd, and one microbe (Rhodococcus sp.) showed a special tolerance to every heavy metal. The strains were divided into six genrera: Rhodococcus, Virgibacillus, Leifsoni, Achromobacter, Cupriavidus and Oceanobacillus sp. Finally, Rhodococcus sp. strain 3 was able to remove different amounts of heavy metals from the culture media with intracellular and surface accumulation of Cu, Zn, Pb and Cd. The application of this bacterial strain in bioremediation processes is discussed.

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Vela-Cano, M. , Castellano-Hinojosa, A. , Vivas, A. and Toledo, M. (2014) Effect of Heavy Metals on the Growth of Bacteria Isolated from Sewage Sludge Compost Tea. Advances in Microbiology, 4, 644-655. doi: 10.4236/aim.2014.410070.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] BOJA (Boletín Oficial de la Junta de Andalucía) (2011) Ley 5/2011, de 6 de octubre, del olivar de Andalucía, 205, 6-13.
[2] Duarte, F., Jones, N. and Fleskens, L. (2007) Traditional Olive Orchards on Sloping Land: Sustainability or Abandonment? Journal of Environmental Management, 89, 86-98.
[3] de Graaff, J., Duran, V.H., Jones, N. and Fleskens, L. (2008) Olive Production Systems on Loping Land: Prospects and Scenarios. Journal of Environmental Management, 89, 129-139.
[4] Areal, F.J. and Riesgo, L. (2013) Farmers’ Views on the Future of Olive Farming in Andalusia, Spain. Land Use Policy, 36, 543-553.
[5] Milgroom, J., Soriano, M.A., Garrido, J.M., Gómez, J.A. and Fereres, E. (2005) The Influence of a Shift from Conventional to Organic Olive Farming on Soil Management and Erosion Risk in Southern Spain. Renewable Agriculture and Food Systems, 22, 1-10.
[6] Serramiá, N., Sánchez-Monedero, M.A., Roig, A., Contin, M. and de Nobili, M. (2013) Changes in Soil Humic Pools after Soil Application of Two-Phase Olive Mill Waste Compost. Geoderma, 192, 21-30.
[7] Fernández, J.M., Senesi, N., Plaza, C., Brunetti, G. and Polo, A. (2009) Effects of Composted and Thermally Dried Sewage Sludges on Soil and Soil Humic Acid Properties. Pedosphere, 193, 281-291.
[8] Ingelmo, F., Molina, M.J., Soriano, M.D., Gallardo, A. and Lapena, L. (2012) Influence of Organic Matter Transformations on the Bioavailability of Heavy Metals in a Sludge Based Compost. Journal of Environmental Management, 95, 104-109.
[9] He, M., Tian, G. and Liang, X. (2009) Phytotoxicity and Speciation of Copper, Zinc and Lead during the Aerobic Composting of Sewage Sludge. Journal of Hazardous Materials, 163, 671-677.
[10] Theodoratos, P., Moirou, A., Xenidis, A. and Paspaliaris, I. (2000) The Use of Municipal Sewage Sludge for the Stabilization of Soil Contaminated by Mining Activities. Journal of Hazardous Materials, B77, 177-191.
[11] Epstein, E., Chaney, R.L., Henry, C. and Logan, T.J. (1992) Trace Elements in Municipal Solid Waste Compost. Biomass and Bioenergy, 3, 227-238.
[12] Council Directive 91/271/EEC (1991) Concerning Urban Waste-Water Treatment.
[13] Xu, C., Chen, W. and Hong, J. (2013) Life-Cycle Environmental and Economic Assessment of Sewage Sludge Treatment in China. Journal of Cleaner Production, 67, 79-87.
[14] Cai, Q., Mo, C., Wu, Q., Zeng, Q. and Katsoyiannis, A. (2007) Concentration and Speciation of Heavy Metals in Six Different Sewage Sludge-Composts. Journal of Hazardous Materials, 147, 1063-1072.
[15] Paradelo, M., Devesa, R., Moldes, A.B. and Barral, M.T. (2007) Physiologically Based Extraction of Heavy Metals in Compost: Preliminary Results. Journal of Trace Elements in Medicine and Biology, 21, 83-85.
[16] Nyamangara, J. (1998) Use of Sequential Extraction to Evaluate Zinc and Copper in a Soil Amended with Sewage Sludge and Inorganic Metal Salts. Agriculture, Ecosystems and Environment, 69, 135-141.
[17] Rodríguez, L., Ruiz, E., Alonso-Azcárate, J. and Rincón, J. (2009) Heavy Metal Distribution and Chemical Speciation in Tailings and Soils around a Pb-Zn Mine in Spain. Journal of Environmental Management, 90, 1106-1116.
[18] Ahluwalia, S. and Goyal, D. (2007) Microbial and Plant Derived Biomass for Removal of Heavy Metals from Wastewater. Bioresource Technology, 98, 2243-2257.
[19] Vullo, D.L., Ceretti, H.M., Daniel, M.A., Ramírez, S.A.M. and Zalts, A. (2008) Cadmium, Zinc and Copper Biosorption Mediated by Pseudomonas veronii 2E. Bioresource Technology, 99, 5574-5581.
[20] Munoz, A.J., Ruiz, E., Abriouel, H., Gálvez, A., Ezzouhri, L., Larini, K. and Espínola, F. (2012) Heavy Metal Tolerance of Microorganisms Isolated from Wastewaters: Identification and Evaluation of Its Potential for Biosorption. Chemical Engineering Journal, 210, 325-332.
[21] Vijayaraghavan, K. and Yun, Y. (2008) Bacterial Biosorbents and Biosorption. Biotechnology Advances, 26, 266-291.
[22] Wang, J. and Chen, C. (2009) Biosorbents for Heavy Metals Removal and Their Future. Biotechnology Advances, 27, 195-226.
[23] Munoz, A.J., Ruiz, E., Abriouel, H., Gálvez, A., Ezzouhri, L., Larini, K. and Espínola, F. (2012) Heavy Metal Tolerance of Microorganisms Isolated from Wastewaters: Identification and Evaluation of Its Potential for Biosorption. Chemical Engineering Journal, 210, 325-332.
[24] Fomina, M. and Gadd, G.M. (2014) Biosorption: Current Perspectives on Concept, Definition and Application. Bioresource Technology, 160, 3-14.
[25] Avidano, L., Gamalero, E., Cossa, G.P. and Carraro, E. (2005) Characterization of Soil Health in an Italian Polluted Site by Using Microorganisms as Bioindicators. Applied Soil Ecology, 30, 21-33.
[26] Weisburg, W.G., Barns, S.M., Pelletier, D.A. and Lane, D.J. (1991) 16S Ribosomal DNA Amplification for Phylogenetic Study. Journal of Bacteriology, 173, 697-703.
[27] Vinuesa, P., Rademaker, J.L.W., de Bruijn, F.J. and Werner, D. (1998) Genotypic Characterization of Bradyrhizobium Strains Nodulating Endemic Woody Legumes of the Canary Islands by PCR-Restriction Fragment Length Polymorphism Analysis of Genes Encoding 16S rRNA (16S rDNA) and 16S-23S rDNA Intergenic Spacers, Repetitive Extragenic Palindromic PCR Genomic Fingerprinting, and Partial 16S rDNA Sequencing. Applied and Environmental Microbiology, 64, 2096-2104.
[28] Altschul, S.F., Madden, T.L., Schaffer1, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: A New Generation of Protein Database Search Programs. Nucleic Acids Research, 25, 3389-3402.
[29] Jeanmougin, F., Thompson, J.D., Gouy, M., Higgins, D.G. and Gibson, T.J. (1998) Multiple Sequence Alignment with Clustal X. Trends in Biochemical Sciences, 23, 403-405.
[30] Kumar, S., Tamura, K., Jakobsen, I.B. and Nei, M. (2001) MEGA2: Molecular Evolutionary Genetics Analysis Software. Bioinformatics, 17, 1244-1245.
[31] Lin, Y., Du, D., Si, C., Zhao, Q., Li, Z. and Li, P. (2014) Potential Biocontrol Bacillus sp. Strains Isolated by an Improved Method from Vinegar Waste Compost Exhibit Antibiosis against Fungal Pathogens and Promote Growth of Cucumbers. Biological Control, 71, 7-15.
[32] Colak, F., Atarb, N., Yazicioglu, D. and Olgunb, A. (2011) Biosorption of Lead from Aqueous Solutions by Bacillus Strains Possessing Heavy-Metal Resistance. Chemical Engineering Journal, 173, 422-428.
[33] Van der Geize, R. and Dijkhuizen, L. (2004) Harnessing the Catabolic Diversity of Rhodococci for Environmental and Biotechnological Applications. Current Opinion in Microbiology, 7, 255-261.
[34] Fleck, L.C., Correa, F. and Zachia, M.A. (2000) Physiological Aspects of Hydrocarbon Emulsification, Metal Resistance and DNA Profile of Biodegrading Bacteria Isolated from Oil Polluted Sites. Biotechnology Letters, 22, 285-289.
[35] Belimov, A.A., Hontzeas, N., Safronova, V.I., Demchinskaya, S.V., Piluzza, G., Bullitta, S. and Glick, B.R. (2005) Cadmium-Tolerant Plant Growth-Promoting Bacteria Associated with the Roots of Indian Mustard (Brassica juncea L. Czern.). Soil Biology & Biochemistry, 37, 241-250.
[36] Esposito, A., Pagnanelli, F., Lodi, A., Solisio, C. and Vegliò, F. (2001) Biosorption of Heavy Metals by Sphaerotilus natans: An Equilibrium Study at Different pH and Biomass Concentrations. Hydrometallurgy, 60, 129-141.
[37] Karakagh, R.M., Chorom, S., Motamedi, H., Kalkhajeh, Y.K. and Oustan, S. (2012) Biosorption of Cd and Ni by Inactivated Bacteria Isolated from Agricultural Soil Treated with Sewage Sludge. Ecohydrology & Hydrobiology, 12, 191-198.
[38] Malik, A. and Jaiswal, R. (2000) Metal Resistance in Pseudomonas Strains Isolated from Soil Treated with Industrial Wastewater. World Journal of Microbiology & Biotechnology, 16, 177-182.
[39] Gisset, T., Botero, A.E., de Mesquita, L.M. and Torem, M.L. (2007) Biosorptive Removal of Cd and Zn from Liquid Streams with a Rhodococcus opacus Strain. Minerals Engineering, 20, 939-944.
[40] Bueno, B.Y.M., Torem, M.L., de Carvalho, R.J., Pino, G.A.H. and de Mesquita, L.M.S. (2011) Fundamental Aspects of Biosorption of Lead (II) Ions onto a Rhodococcus opacus Strain for Environmental Applications. Minerals Engineering, 24, 1619-1624.
[41] Areco, M.M., Hanela, S., Duran, J. and Afonso, M.S. (2012) Biosorption of Cu(II), Zn(II), Cd(II) and Pb(II) by Dead Biomasses of Green Alga Ulva lactuca and the Development of a Sustainable Matrix for Adsorption Implementation. Journal of Hazardous Materials, 213-214, 123-132.
[42] Jing, H., Mezgebe, B., Hassan, A.A., Sahle-Demessie, E., Sorial, G.A. and Bennett-Stamper, C. (2014) Experimental and Modeling Studies of Sorption of Ceria Nanoparticle on Microbial Biofilms. Bioresource Technology, 161, 109-117.

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