Indigeneous Streptomyces spp. isolated from Cyperus rotundus rhizosphere indicate high mercuric reductase activity as a pontential bioremediation agent
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Abstract. Rahayu HM, Putri WA, Khasanah AU, Sembiring L, Purwestri YA. 2021. Indigenous Streptomyces spp. isolated from Cyperus rotundus rhizosphere indicate high mercuric reductase activity as a potential bioremediation agent. Biodiversitas 22: 1519-1526. The purification and characterization of mercuric reductase of four indigenous Streptomyces spp. from Cyperus rotundus L. rhizosphere in mercury-contaminated area have been investigated. Cell-free extract was obtained by disrupting cells using sea sand at 4 °C followed by centrifugation. Mercuric reductase was purified by ammonium sulfate precipitation, dialysis, and chromatography column (DEAE Sepharose anion column chromatography). The determination of optimum pH and temperature of mercuric reductase activity was measured based on the number of NADPH2 oxidized to NADP per mg protein per minute using a spectrophotometer. The molecular weight of mercuric reductase was determined using SDS-PAGE. Result showed that the highest specific activity of mercuric reductase was recorded from Streptomyces spp. BR28. The optimum pH and temperature of cell-free extract enzyme mercuric reductase were 7.5 and 80 °C, respectively. The enzyme was purified to 431.87-fold with specific activity 21918.95 U/mg protein. SDS PAGE showed that the molecular weight of mercuric reductase in Streptomyces spp. BR 28 ranged from 50 kDa to 75 kDa. It can be concluded that Streptomyces isolates contain mercuric reductase and have potential as mercury bioremediation agent to overcome mercury contamination in the environment.
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References
Amroso, M.J., G.R. Castro., F.J. Carlino., N.C. Romero., R.T. Hill., G. Oliver. 1998. Screening of Heavy Metal-Tolerant Actinomycetes Isolated from The Sali River. J. Gen. Appl. Microbiol 44: 129-132.
Bafana, A., Khan, F., Suguna, K. 2017. Structural and Functional Characterization of Mercuric Reductase from Lysinibacillus sphaericus strain G1. Biometals.
Bogdanova, E.S., Mindlin, S.Z., Kalyaeva, E.S., Nikiforov, V.G. 1988. The Diversity of Mercury Reductase Among Mercury-resistant Bacteria. Elsevier. 234: 280-282.
Bradford, M.M. 1976. A Rapid and Sensitive Method for Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding. Analytical Biochemistry. 72: 248-254
Byrne, K. 2013. Factor Affecting Enzyme Activity. Bio Factsheet. Birmingham.
Copeland, R.A. 2000. Enzymes, A Practical Introduction to Structure, Mechanism, and Data Analysis. Wiley-VCH Inc.
Dash, H.R., Das, S., 2012. Bioremediation of mercury and the importance of bacterial mer genes. Int. Biodeterior. Biodegrad. 75: 207–213
Deepika, L. & Kannabiran. K.2010. Biosurfactan and Heavy Metal Resistance Activity of Streptomyces spp. Isolated from Saltpan Soil. British Journal of Pharmacology and Toxicologgy 1(1): 33-39.
Fatimawali., Kepel, B.J., Gani, M.A., Tallei, T.E. 2020. Comparison of Bacterial Community Structure and Diversity in Traditional Gold Mining Waste Disposal Site and Rice Field by Using a Metabarcoding Approach. International Journal of Microbiology
Fox, B. & Walsh, C.T. 1982. Mercuric Reductase, Purification, and Characterization of A Transposon-Encoded Flavoprotein Containing an Oxidation-Reduction Active Disulfide. The Journal of Biological Chemistry. 257: 2498-2503.
Freedman, Z., Zhu, C., Barkay, T. 2012. Mercury Resistance and Mercuric Reductase Activities and Expression Among Chemotrophic Thermophilic Aquaificae. Applied and Environmental Microbiology. 78 (18): 6568-6575.
Furukawa, K. & Tonomura, K. 1971. Metallic Mercury-releasing Enzyme in Mercuri-resistant Pseudomonas. Agr. Biol. Chem. 36: 217-226
Gadd, G.M. 1990. Metal Tolerance in Microbiology of Extreme Environments. Clive Edward (ED) Open University Press. Millon Keynes. pp. 178-192.
Giovanella., p., Cabral, l., Bento, f., Gianello, C., Camargo, F, A, O. 2015. Mercury (II) Removal by Resistant Bacterial Isolate and Mercuric (II) Reductase activity in A New Strain of Pseudomonas sp B50A. New Biotechnology. 00: 1-8
Glumoff, T. 2004. Physiology and Maintenance, on the Determination of Enzyme Structure, Function, and Mechanism. Encyclopedia of life support systems.
Gopinath, E., Kaaret, T.W., Bruice, T.C. 1989. Mechanism of Mercury (II) Reductase and influence of Ligation on the Reduction of Mercury (II) by Water Soluble 1,5-dihydroflavin. Proc. National Academy of Sciences. 86: 3041-3044.
Gosh, S., Sadhukhan, P.C., Chaudhuri, J., Gosh, D.K., Mandal, A. 1998. Purification and Properties of Mercuric Reductase from Azotobacter chroococcum. Journal of Applied Microbiology 86: 7-12.
Hobman, J.L. & Brown, N.L. 2007. Bacterial Mercury-Resistance Genes in Metal ions in Biological System, Mercury, and its effects on Environment and Biology. 34. Marcel Dekker Inc, USA.
Huang, C.C., Chien, M.F., Lin, K.H. 2010. Bacterial Mercury Resistance of TnMERI1 and Its’ Application in Bioremediation. Interdisciplinary Studies on Environmental pp. 23-29.
Hughes, M.M & Poole, R.K. 1989. Metal and Microorganism. Chapman and Hall. London
Imron, M.F., Kurniawan, S.B., Soegianto, A. 2019. Characterization of mercury-reducing potential bacteria isolated from Keputih non-active sanitary landfill leachate, Surabaya, Indonesia under different saline conditions. Journal of Environmental Management. 241: 113-122
Irawati, W., Patricia, Soraya, Y., Baskoro, A.H. 2012. A Study on Mercury-Resistant Bacteria Isolated from a Gold Mine in Pongkor Village, Bogor, Indonesia. HAYATI Journal of Biosciences Vol. 19 No. 4: 197-200
Kumar, A. & Garg, N. 2006. Enzymology, Enzyme Purification. School of Biotechnology Devi Ahiliya University.
Kumari, S., Amit., Jamwal, R., Mishra, N., Singh, D.K. 2020. Recent Development in Environmental Mercury Bioremediation and Its Toxicity: A Review. Environmental Nanotechnology, Monitoring & Management. 13: 100283
Krisnayanti, B.D., Anderson, C.W.N., Utomo, W.H., ad Xinbin Feng, X., Handayanto, E., Mudarisna, N., Ikram, H., Khususiah. 2012. Assessment of environmental mercury discharge at a four-year-old artisanal gold mining area on Lombok Island, Indonesia. Journal of Environmental. 14: 2598
Madigan, M., Martinko, J., Stahl, D., Clark, D. 2012. Brock Biology of Microorganism, 13th edition. Pearson Education. New Jersey.
Maged, M., Hosseiny, A.E., Saadeldin, M.K., Aziz, R.K., Ramadan, E. 2019. Thermal Stability of a Mercuric Reductase from The Red Sea Atlantis II Hot Brine Environment as Analyzed by Site-Directed Mutagenesis. Applied and Environmental Microbiology. 85 (3): e02387-18.
Mahbub, K.R., Bahar, M.M., Labbate, M., Krishnan, K., Andrews, S., Naidu, R., Megharaj, M., 2017. Bioremediation of mercury: not properly exploited in contaminated soils. Appl. Microbiol. Biotechnol. 101 (3): 963–976.
Male, Y.T., Reichelt-Brushett, A.J., Matt Pocock, M., Nanlohy, A. 2013. Recent mercury contamination from artisanal gold mining on Buru Island, Indonesia – Potential future risks to environmental health and food safety. Marine Pollution Bulletin.77: 428-433
Maziyah, S. 2011. Keanekaragaman dan Potensi Streptomycetes Rizosper Rumput Teki (Cyperus rotundus L.) Daerah Tercemar Merkuri sebagai Agen Bioremediasi Cemaran Logam. Tesis. Fakultas Biologi. UGM. Yogyakarta.
Morel, F.M.M., Kraepiel, A.M.L., Amyot, M.1998. The Chemical Cycle and Bioaccumulation of Mercury. Annual Review of Ecology and Systematics. 29: 543-66.
Moore, M., Distefano, M.D., Walsh, C.T., Schiering, N., Pai, E.F. 1989. Purification, Crystallization, and Preliminary X-ray Diffraction Studies of Flavoenzyme Mercuric Ion Reductase from Bacillus sp. Strain RC607. The Journal of Biological Chemistry 264: 14386-14388.
Meissner, P. S & Falkinham III, J.O. 1983. Plasmid-Encoded Mercuric Reductase in Mycobacterium scrofulaceum. Journal of Bacteriology 157(2): 669-672.
Nakahara, H., Schottel, J.L., Yamada, T., Miyakawa, Y., Asakawa, M., Harville, J., Silver, S. 1985. Mercuric Reductase Enzymes from Streptomyces Species and Group B Streptococcus. Journal of General and Applied Microbiology. 131: 1053-1059.
Nies, D.H.1999. Microbial Heavy-Metal Resistance. Appl Microbiol Biotechnol 51: 730-750.
Ogunseitan, O.A. 1998. Protein Method for Investigating Mercuric Reductase Gene Expression in Aquatic Environment. Applied and Environmental Microbiology. 64(2): 695-202.
Olson, G.J., Porter, F.D., Rubinstein, J., Silver, S. 1982. Mercuric Reductase Enzyme from a Mercury-Volatilizing Strain of Thiobacillus ferroxidans. Journal of Bacteriology. 151:1230-1236.
Petrus, A.K., Rutner, C., Liu, S., Wang, Y., Wiatrowski, H.A. 2015. Mercury Reduction and Methyl Mercury Degradation by the Soil Bacterium Xanthobacter autotrophicus Py2. Applied And Environmental Microbiology. 81 (22): 7833-7838
Popa, C & Bahrim, G. 2011. Streptomyces Tyrosinase: Production and Practical Application. Innovative Romanian Food Biotechnology 8: 1-7.
Purkan, P., Nuzulla, Y.F., Hadi, S., Prasetyawati, E.T. Biochemical Properties of Mercuric Reductase from Local Isolate of Bacillus sp for Bioremediation Agent. Molekul. 12(2): 182-188.
Rintala, H. 2003. Streptomycetes in Indoor Environments PCR based Detection and Diversity. Academic Dissertation. Department of Environmental Health National Public Health Institute and Department of Environmental Science, Kuopio University, Finland. Copyright National Public Health Institute, Helsinki.
Robinson, J.B. & Tuovinen, O.H. 1984. Mechanism of Microbial Resistance and Detoxification of Mercury and Organomercury Compounds: Physiological, Biochemical, and Genetic Analyses. Microbiological Reviews. 48(2): 95-124.
Sayed, A., Ghazy, M.A., Ferreira, A.J.S., Setubal, J.C., Chambergo, F.S., Ouf, A., Adel, M., Dawe, A.S., Archer, J.A.C., Bajic, V.B., Siam, R., El-Dorry, H. 2014. A Novel Mercuric Reductase from The Unique Deep Brine Environmet of Atlantis II in The Red Sea. 289(3): 1675-1687
Schottel, Janet L. 1977. The Mercuric and Organomercurial Detoxifying Enzymes from a Plasmid-bearing Strain of Escherichia coli. The Journal of Biological Chemistry. 253: 12.
Silver, S. & Hobman, J.L.2007. Mercury Microbiology: Resistance Systems, Environmental Aspects, Methylation, and Human Health. Microbiol Monogr. 6: 357-370.
Silver, S. & Phung, L.T. 2005. A Bacterial View of the Periodic Table: Genes and Proteins for Toxic Inorganic Ions. J Ind. Microbiol Biotechnol. 32: 587-605.
Summers, A.O. 1986. Organization, Expression, and Evolution of Genes for Mercury Resistance. Annual Review of Microbiology. 40: 607-34.
Tomiyasu, T., Kodamatani, H., Hamada, Y.K., Matsuyama, A., Imura, R., Taniguchi, Y., Hidayati, N., Rahajoe, J.S. 2016. Distribution of total mercury and methyl mercury around the small-scale gold mining area along the Cikaniki River, Bogor, Indonesia. Environ Sci Pollut Res.
Undabarrena, A., Ugalde, J.A., Seeger, M., Camara, B. 2017. Genomic data mining of the marine actinobacteria Streptomyces sp. H-KF8 unveils insights into multi-stress related genes and metabolic pathways involved in antimicrobial synthesis. PeerJ. 2-35
Weiss, A.A., Murphy, S.D., Silver, S.1977. Mercury and Organomercurial Resistance Determined by Plasmids in Staphylococcus aureus. Journal of Bacteriology. 132:197-208.
Winardi, Sudrajat, Haryono, E., Soetarto, E.S. 2019. Potential of Soil Bacteria as Mercury Bioremediation Agent in Traditional Gold Mining. Biosaintifika Journal of Biology & Biology Education. 11 (1): 108-116
Zeroual, Y., A. Moutaouakkil., F.Z. Dzairi., M. Talbi., P.U. Chung., K. Lee., M. Blaghen. 2003. Purification and characterization of cytosolic mercuric reductase from Klebsiella pneumoniae. Annals of Microbiology
Bafana, A., Khan, F., Suguna, K. 2017. Structural and Functional Characterization of Mercuric Reductase from Lysinibacillus sphaericus strain G1. Biometals.
Bogdanova, E.S., Mindlin, S.Z., Kalyaeva, E.S., Nikiforov, V.G. 1988. The Diversity of Mercury Reductase Among Mercury-resistant Bacteria. Elsevier. 234: 280-282.
Bradford, M.M. 1976. A Rapid and Sensitive Method for Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding. Analytical Biochemistry. 72: 248-254
Byrne, K. 2013. Factor Affecting Enzyme Activity. Bio Factsheet. Birmingham.
Copeland, R.A. 2000. Enzymes, A Practical Introduction to Structure, Mechanism, and Data Analysis. Wiley-VCH Inc.
Dash, H.R., Das, S., 2012. Bioremediation of mercury and the importance of bacterial mer genes. Int. Biodeterior. Biodegrad. 75: 207–213
Deepika, L. & Kannabiran. K.2010. Biosurfactan and Heavy Metal Resistance Activity of Streptomyces spp. Isolated from Saltpan Soil. British Journal of Pharmacology and Toxicologgy 1(1): 33-39.
Fatimawali., Kepel, B.J., Gani, M.A., Tallei, T.E. 2020. Comparison of Bacterial Community Structure and Diversity in Traditional Gold Mining Waste Disposal Site and Rice Field by Using a Metabarcoding Approach. International Journal of Microbiology
Fox, B. & Walsh, C.T. 1982. Mercuric Reductase, Purification, and Characterization of A Transposon-Encoded Flavoprotein Containing an Oxidation-Reduction Active Disulfide. The Journal of Biological Chemistry. 257: 2498-2503.
Freedman, Z., Zhu, C., Barkay, T. 2012. Mercury Resistance and Mercuric Reductase Activities and Expression Among Chemotrophic Thermophilic Aquaificae. Applied and Environmental Microbiology. 78 (18): 6568-6575.
Furukawa, K. & Tonomura, K. 1971. Metallic Mercury-releasing Enzyme in Mercuri-resistant Pseudomonas. Agr. Biol. Chem. 36: 217-226
Gadd, G.M. 1990. Metal Tolerance in Microbiology of Extreme Environments. Clive Edward (ED) Open University Press. Millon Keynes. pp. 178-192.
Giovanella., p., Cabral, l., Bento, f., Gianello, C., Camargo, F, A, O. 2015. Mercury (II) Removal by Resistant Bacterial Isolate and Mercuric (II) Reductase activity in A New Strain of Pseudomonas sp B50A. New Biotechnology. 00: 1-8
Glumoff, T. 2004. Physiology and Maintenance, on the Determination of Enzyme Structure, Function, and Mechanism. Encyclopedia of life support systems.
Gopinath, E., Kaaret, T.W., Bruice, T.C. 1989. Mechanism of Mercury (II) Reductase and influence of Ligation on the Reduction of Mercury (II) by Water Soluble 1,5-dihydroflavin. Proc. National Academy of Sciences. 86: 3041-3044.
Gosh, S., Sadhukhan, P.C., Chaudhuri, J., Gosh, D.K., Mandal, A. 1998. Purification and Properties of Mercuric Reductase from Azotobacter chroococcum. Journal of Applied Microbiology 86: 7-12.
Hobman, J.L. & Brown, N.L. 2007. Bacterial Mercury-Resistance Genes in Metal ions in Biological System, Mercury, and its effects on Environment and Biology. 34. Marcel Dekker Inc, USA.
Huang, C.C., Chien, M.F., Lin, K.H. 2010. Bacterial Mercury Resistance of TnMERI1 and Its’ Application in Bioremediation. Interdisciplinary Studies on Environmental pp. 23-29.
Hughes, M.M & Poole, R.K. 1989. Metal and Microorganism. Chapman and Hall. London
Imron, M.F., Kurniawan, S.B., Soegianto, A. 2019. Characterization of mercury-reducing potential bacteria isolated from Keputih non-active sanitary landfill leachate, Surabaya, Indonesia under different saline conditions. Journal of Environmental Management. 241: 113-122
Irawati, W., Patricia, Soraya, Y., Baskoro, A.H. 2012. A Study on Mercury-Resistant Bacteria Isolated from a Gold Mine in Pongkor Village, Bogor, Indonesia. HAYATI Journal of Biosciences Vol. 19 No. 4: 197-200
Kumar, A. & Garg, N. 2006. Enzymology, Enzyme Purification. School of Biotechnology Devi Ahiliya University.
Kumari, S., Amit., Jamwal, R., Mishra, N., Singh, D.K. 2020. Recent Development in Environmental Mercury Bioremediation and Its Toxicity: A Review. Environmental Nanotechnology, Monitoring & Management. 13: 100283
Krisnayanti, B.D., Anderson, C.W.N., Utomo, W.H., ad Xinbin Feng, X., Handayanto, E., Mudarisna, N., Ikram, H., Khususiah. 2012. Assessment of environmental mercury discharge at a four-year-old artisanal gold mining area on Lombok Island, Indonesia. Journal of Environmental. 14: 2598
Madigan, M., Martinko, J., Stahl, D., Clark, D. 2012. Brock Biology of Microorganism, 13th edition. Pearson Education. New Jersey.
Maged, M., Hosseiny, A.E., Saadeldin, M.K., Aziz, R.K., Ramadan, E. 2019. Thermal Stability of a Mercuric Reductase from The Red Sea Atlantis II Hot Brine Environment as Analyzed by Site-Directed Mutagenesis. Applied and Environmental Microbiology. 85 (3): e02387-18.
Mahbub, K.R., Bahar, M.M., Labbate, M., Krishnan, K., Andrews, S., Naidu, R., Megharaj, M., 2017. Bioremediation of mercury: not properly exploited in contaminated soils. Appl. Microbiol. Biotechnol. 101 (3): 963–976.
Male, Y.T., Reichelt-Brushett, A.J., Matt Pocock, M., Nanlohy, A. 2013. Recent mercury contamination from artisanal gold mining on Buru Island, Indonesia – Potential future risks to environmental health and food safety. Marine Pollution Bulletin.77: 428-433
Maziyah, S. 2011. Keanekaragaman dan Potensi Streptomycetes Rizosper Rumput Teki (Cyperus rotundus L.) Daerah Tercemar Merkuri sebagai Agen Bioremediasi Cemaran Logam. Tesis. Fakultas Biologi. UGM. Yogyakarta.
Morel, F.M.M., Kraepiel, A.M.L., Amyot, M.1998. The Chemical Cycle and Bioaccumulation of Mercury. Annual Review of Ecology and Systematics. 29: 543-66.
Moore, M., Distefano, M.D., Walsh, C.T., Schiering, N., Pai, E.F. 1989. Purification, Crystallization, and Preliminary X-ray Diffraction Studies of Flavoenzyme Mercuric Ion Reductase from Bacillus sp. Strain RC607. The Journal of Biological Chemistry 264: 14386-14388.
Meissner, P. S & Falkinham III, J.O. 1983. Plasmid-Encoded Mercuric Reductase in Mycobacterium scrofulaceum. Journal of Bacteriology 157(2): 669-672.
Nakahara, H., Schottel, J.L., Yamada, T., Miyakawa, Y., Asakawa, M., Harville, J., Silver, S. 1985. Mercuric Reductase Enzymes from Streptomyces Species and Group B Streptococcus. Journal of General and Applied Microbiology. 131: 1053-1059.
Nies, D.H.1999. Microbial Heavy-Metal Resistance. Appl Microbiol Biotechnol 51: 730-750.
Ogunseitan, O.A. 1998. Protein Method for Investigating Mercuric Reductase Gene Expression in Aquatic Environment. Applied and Environmental Microbiology. 64(2): 695-202.
Olson, G.J., Porter, F.D., Rubinstein, J., Silver, S. 1982. Mercuric Reductase Enzyme from a Mercury-Volatilizing Strain of Thiobacillus ferroxidans. Journal of Bacteriology. 151:1230-1236.
Petrus, A.K., Rutner, C., Liu, S., Wang, Y., Wiatrowski, H.A. 2015. Mercury Reduction and Methyl Mercury Degradation by the Soil Bacterium Xanthobacter autotrophicus Py2. Applied And Environmental Microbiology. 81 (22): 7833-7838
Popa, C & Bahrim, G. 2011. Streptomyces Tyrosinase: Production and Practical Application. Innovative Romanian Food Biotechnology 8: 1-7.
Purkan, P., Nuzulla, Y.F., Hadi, S., Prasetyawati, E.T. Biochemical Properties of Mercuric Reductase from Local Isolate of Bacillus sp for Bioremediation Agent. Molekul. 12(2): 182-188.
Rintala, H. 2003. Streptomycetes in Indoor Environments PCR based Detection and Diversity. Academic Dissertation. Department of Environmental Health National Public Health Institute and Department of Environmental Science, Kuopio University, Finland. Copyright National Public Health Institute, Helsinki.
Robinson, J.B. & Tuovinen, O.H. 1984. Mechanism of Microbial Resistance and Detoxification of Mercury and Organomercury Compounds: Physiological, Biochemical, and Genetic Analyses. Microbiological Reviews. 48(2): 95-124.
Sayed, A., Ghazy, M.A., Ferreira, A.J.S., Setubal, J.C., Chambergo, F.S., Ouf, A., Adel, M., Dawe, A.S., Archer, J.A.C., Bajic, V.B., Siam, R., El-Dorry, H. 2014. A Novel Mercuric Reductase from The Unique Deep Brine Environmet of Atlantis II in The Red Sea. 289(3): 1675-1687
Schottel, Janet L. 1977. The Mercuric and Organomercurial Detoxifying Enzymes from a Plasmid-bearing Strain of Escherichia coli. The Journal of Biological Chemistry. 253: 12.
Silver, S. & Hobman, J.L.2007. Mercury Microbiology: Resistance Systems, Environmental Aspects, Methylation, and Human Health. Microbiol Monogr. 6: 357-370.
Silver, S. & Phung, L.T. 2005. A Bacterial View of the Periodic Table: Genes and Proteins for Toxic Inorganic Ions. J Ind. Microbiol Biotechnol. 32: 587-605.
Summers, A.O. 1986. Organization, Expression, and Evolution of Genes for Mercury Resistance. Annual Review of Microbiology. 40: 607-34.
Tomiyasu, T., Kodamatani, H., Hamada, Y.K., Matsuyama, A., Imura, R., Taniguchi, Y., Hidayati, N., Rahajoe, J.S. 2016. Distribution of total mercury and methyl mercury around the small-scale gold mining area along the Cikaniki River, Bogor, Indonesia. Environ Sci Pollut Res.
Undabarrena, A., Ugalde, J.A., Seeger, M., Camara, B. 2017. Genomic data mining of the marine actinobacteria Streptomyces sp. H-KF8 unveils insights into multi-stress related genes and metabolic pathways involved in antimicrobial synthesis. PeerJ. 2-35
Weiss, A.A., Murphy, S.D., Silver, S.1977. Mercury and Organomercurial Resistance Determined by Plasmids in Staphylococcus aureus. Journal of Bacteriology. 132:197-208.
Winardi, Sudrajat, Haryono, E., Soetarto, E.S. 2019. Potential of Soil Bacteria as Mercury Bioremediation Agent in Traditional Gold Mining. Biosaintifika Journal of Biology & Biology Education. 11 (1): 108-116
Zeroual, Y., A. Moutaouakkil., F.Z. Dzairi., M. Talbi., P.U. Chung., K. Lee., M. Blaghen. 2003. Purification and characterization of cytosolic mercuric reductase from Klebsiella pneumoniae. Annals of Microbiology
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