Abstract
Hexavalent chromium Cr(VI) is a widespread environmental contaminant. Many microorganisms have been reported to detoxify hexavalent chromium. The present work is the first report of a strain of Enterococcus having the ability of resistance to and reduction of Cr(VI). This strain was isolated from tannery waste-contaminated soil and identified as Enterococcus gallinarum, by biochemical methods and 16S rDNA analysis. The strain also exhibited multiple heavy metals (Cu2+, Ni 2+, Pb2+, Co2+ and Zn2+) tolerance. It was found to reduce chromate to 100% at a concentration of 200 mg l-1, in aerobic conditions. The cells reduced Cr(VI) under a wide range of temperatures (25-45°C) and pH (7–11) with optimum at 37°C and initial pH 10. The presence of other metals, such as Cu2+, stimulated Cr(VI) reduction, while Pb2+ and Ni 2+ had no significant effect on reduction ability by the strain. Assay with resting and permeabilized cells (treated with toluene and Triton X-100) demonstrated that the reduction of Cr(VI) is mediated by cell membrane bound or soluble proteins of the cell. The results obtained in this study have significance for the bioremediation of chromate pollution.







Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Ackerley DF, Gonzalez CF, Keyhan M, Blake R, Matin A (2004) Mechanism of chromate reduction by the Escherichia coli protein, NfsA, and the role of different chromate reductases in minimizing oxidative stress during chromate reduction. Environ Microbiol 6:851–860
Badar U, Ahmed N, Beswick AJ, Pattanapipitpaisal P, Macaskie LE (2000) Reduction of chromate by microorganisms isolated from metal contaminated sites of Karachi, Pakistan. Biotechnol Lett 22:829–836
Bai RS, Abraham TE (2003) Studies on chromium (VI) adsorption–desorption using immobilized fungal biomass. Bioresour Technol 87:17–26
Branco R, Alpoim MC, Morais PV (2004) Ochrobactrum tritici strain 5bvl1 characterization of aCr(VI)-resistant and Cr(VI)-reducing strain. Can J Microbiol 50:697–703
Camargo FAO, Okeke BC, Bento FM, Frankenberger WT (2003) Chromate reduction by chromium resistant bacteria isolated from soils contaminated with dichromate. J Environ Qual 32:1228–1233
Chen JM, Hao OJ (1998) Microbial chromium(VI) reduction. Crit Rev Environ Sci Technol 28:219–251
Chen DK, Pearce L, McGeer A, Low DE, Willey BM (2000) Evaluation of D-Xylose and 1% Methyl-α-D-Glucopyranoside fermentation tests for distinguishing Enterococcus gallinarum from Enterococcus faecium. J Clin Microbiol 38:3652–3655
DeLeo PC, Ehrlich HL (1994) Reduction of hexavalent chromium by Pseudomonas flourescens LB300 in batch and continuous cultures. Appl Microbiol Biotechnol 40:756–759
Devriese LA, Pot B, Collins MD (1993) Phenotypic identification of the genus Enterococcus and differentiation of phylogenetically distinct enterococcal species and species groups. J Appl Microbiol 75:399–408
Elangovan R, Abhipsa S, Rohit B, Ligy P, Chandraraj K (2006) Reduction of Cr(VI) by a Bacillus sp. Biotechnol Lett 28:247–252
U.S. EPA (1978) Reviews of the environmental effects of pollutants III. Chromium. EPA 600/1-78-023. U.S. Environmental Protection Agency, Washington, D.C.
Federal Register (2004) Occupational safety and health administration. Occupational exposure to hexavalent chromium. Federal Register 69:59404
Ganguli A, Tripathi AK (2001) Inducible periplasmic chromate reducing activity in Pseudomonas aeruginosa isolated from a leather tannery effluent. J Microbiol Biotechnol 11:355–361
Garbisu C, Alkorta I, Llama MJ, Serra JL (1998) Aerobic chromate reduction by Bacillus subtilis. Biodegradation 9:133–141
Guha H, Jayachandran K, Maurrasse F (2001) Kinetics of chromium (VI) reduction by a type strain Shewanella alga under different growth conditions. Environ Pollut 115:209–218
Konovalova VV, Dmytrenko GM, Nigmatullin RR, Bryk MT, Gvozdyak PI (2003) Chromium(VI) reduction in a membrane bioreactor with immobilized Pseudomonas cells. Enzyme Microb Technol 33:899–907
Krishna KR, Philip L (2005) Bioremediation of Cr(VI) in contaminated soils. J Hazard Mater 121:109–117
Liu C, Gorby YA, Zachara JM, Fredrickson JK, Brown CF (2002) Reduction kinetics of Fe(III), Co(III), U(VI), Cr(VI) and Tc(VII) in cultures of dissimilatory metal-reducing bacteria. Biotechnol Bioeng 80:637–648
Liu YG, Xu WH, Zeng GM, Tang CF, Li CF (2004) Experimental study on reduction by Pseudomonas aeruginosa. J Environ Sci 16:797–801
Lotfi M, Adhoum N (2002) Modified activated carbon for the removal of copper, zinc, chromium and cyanide from wastewater. Sep Purif Technol 26:137–146
McLean J, Beveridge TJ (2001) Chromate reduction by a pseudomonad isolated from a site contaminated with chromated copper arsenate. Appl Environ Microbiol 67:1076–1084
Megharaj M, Avudainayagam S, Naidu R (2003) Toxicity of hexavalent chromium and its reduction by bacteria isolated from soil contaminated with tannery waste. Curr Microbiol 47:51–54
Michel C, Brugna M, Aubert C, Bernadac A, Bruschi M (2001) Enzymatic reduction of chromate: comparative studies using sulfate-reducing bacteria. Key role of polyheme cytochrome c and hydro-genases. Appl Microbiol Biotechnol 55:95–100
Myers CR, Carstens BP, Antholine WE, Myers JM (2000) Chromium(VI) reductase activity is associated with the cytoplasmic membrane of anaerobically grown Shewanella putrefaciens MR-1. J Appl Microbiol 88:98–106
Naidu R, Kookana RS, Cox J, Mowat D, Smith LH (2000) Fate of chromium at tannery waste contaminated sites at Mount barker, South Australia. In: Naidu R, Willet IR, Mahimairaja S, Kookana RS, Ramasamy K (eds) Towards Better Management of Soils Contaminated with Tannery Waste. Proc. No. 88. Australian Centre for International Agricultural Research, Canberra, Australia, pp 57–70
Ohtake H, Fujii E, Toda K (1990) Reduction of toxic chromate in an industrial effluent by use of a chromate reducing strain of Enterobacter cloacae. Environ Sci Technol 11:663–668
Padilla AP, Tavani E (1999) Treatment of an industrial effluent by reverse osmosis. Desalination 129:219–226
Pal A, Paul AK (2004) Aerobic chromate reduction by chromium resistant bacteria isolated from serpentine soil. Microbiol Res 159:347–354
Papp JF (2001) Mineral Commodity Summaries. Chromium. US Department of the Interior, US Geological Survey, Washington, DC
Park CH, Keyhan M, Wielinga B, Fendorf S, Martin A (2000) Purification to homogeneity and characterization of a novel Pseudomonas putida chromate reductase. Appl Environ Microbiol 66:1788–1795
Pattanapipitpaisal P, Brown NL, Macaskie LE (2001) Chromate reduction and 16S rRNA identification of bacteria isolated from Cr(VI) contaminated site. Appl Microbiol Biotechnol 57:257–261
Raja ChE, Anbazhagan K, Selvam GS (2006) Isolation and characterization of a metal-resistant Pseudomonas aeruginosa strain. World J Microbiol Biotechnol 22:577–585
Rengaraj S, Joo CK, Kim Y, Yi J (2003) Kinetics of removal of chromium from water and electronic process wastewater by ion exchange resins: 1200H, 1500H and IRN97H. J Hazard Mater 102:257–275
Sarangi A, Krishnan C (2007) Comparison of in vitro Cr(VI) reduction by CFEs of chromate resistant bacteria isolated from chromate contaminated soil. Bioresour Technol 99(10):4130–4137
Shakoori AR, Makhdoom M, Haq RU (2000) Hexavalent chromium reduction by a dichromate-resistant Gram-positive bacterium isolated from effluents of tanneries. Appl Microbiol Biotechnol 53:348–351
Shen H, Wang YT (1994) Biological reduction of chromium by E. coli. J Environ Eng 120(3):560–572
Srinath T, Khare S, Ramteke PW (2001) Isolation of hexavalent chromium reducing Cr-tolerant facultative anaerobies from tannery effluent. J Gen Appl Microbiol 47:307–312
Sultan S, Hasnain S (2005) Chromate reduction capability of a Gram positive bacterium isolated from effluent of dying industry. Bull Environ Contam Toxicol 75:699–706
Sultan S, Hasnain S (2007) Reduction of toxic hexavalent chromium by Ochrobactrum intermedium strain SDCr-5 stimulated by heavy metals. Bioresour Technol 98:340–344
Thacker U, Madamwar D (2005) Reduction of toxic chromium and partial localization of chromium reductase activity in bacterial isolate DM1. World J Microbiol Biotechnol 21:891–899
Thacker U, Parikh R, Shouche Y, Madamwar D (2006) Hexavalent chromium reduction by Providencia sp. Process Biochem 41:1332–1337
Thacker U, Parikh R, Shouche Y, Madamwar D (2007) Reduction of chromate by cell-free extract of Brucella sp. isolated from Cr(VI) contaminated sites. Bioresour Technol 98:1541–1547
Viamajala S, Peyton BM, Petersen JN (2003) Modeling chromate reduction in Shewanella oneidensis MR-1: development of a novel dual-enzyme kinetic model. Biotechnol Bioeng 83:790–797
Viti C, Pace A, Giovannetti L (2003) Characterization of Cr(VI) resistant bacteria isolated from chromium contaminated soil by tannery activity. Curr Microbiol 46:1–5
Wang PC, Mori T, Komori K, Sasatsu M, Toda K, Ohtake H (1989) Isolation and characterization of an Enterobacter cloacae strain that reduces hexavalent chromium under anaerobic conditions. Appl Environ Microbiol 55:1665–1669
Wang PC, Mori T, Toda K, Ohtake H (1990) Membrane-associated chromate reductase activity from Enterobacter cloacae. J Bacteriol 172:1670–1672
Zahoor A, Rehman A (2009) Isolation of CrVI reducing bacteria from industrial effluents and their potentiel use in bioremediation of chromium containing wastewater. J Environ Sci 21:814–820
Zhiguo H, Fengling G, Tao S, Yuehua H, Chao H (2009) Isolation and characterization of a Cr(VI)-reduction Ochrobactrum sp. strain CSCr-3 from chromium landfill. J Hazard Mater 163:869–873
Acknowledgement
The authors gratefully acknowledge the financial and scientific support of the Microbial Biotechnology, Faculty of Sciences and Technology Laboratory and Regional Center of interface, SMBA University, Fez, Morocco.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Sayel, H., Bahafid, W., Tahri Joutey, N. et al. Cr(VI) reduction by Enterococcus gallinarum isolated from tannery waste-contaminated soil. Ann Microbiol 62, 1269–1277 (2012). https://doi.org/10.1007/s13213-011-0372-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13213-011-0372-9


