Mechanism of hexavalent chromium detoxification by microorganisms and bioremediation application potential: A review

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Abstract

Chromium has been widely used in various industries. Hexavalent chromium (Cr6+) is a priority toxic, mutagenic and carcinogenic chemical, whereas its reduced trivalent form (Cr3+) is much less toxic and insoluble. Hence, the basic process for chromium detoxification is the transformation of Cr6+ to Cr3+. A number of aerobic and anaerobic microorganisms are capable of reducing Cr6+. In the presence of oxygen, microbial reduction of Cr6+ is commonly catalyzed by soluble enzymes, except in Pseudomonas maltophilia O-2 and Bacillus megaterium TKW3, which utilize membrane-associated reductases. Recently, two soluble Cr6+ reductases, ChrR and YieF, have been purified from Pseudomonas putida MK1 and Escherichia coli, respectively. ChrR catalyzes an initially one-electron shuttle followed by a two-electron transfer to Cr6+, with the formation of intermediate(s) Cr5+ and/or Cr4+ before further reduction to Cr3+. YieF displays a four-electron transfer that reduces Cr6+ directly to Cr3+. The membrane-associated Cr6+ reductase of B. megaterium TKW3 was isolated, but its reduction kinetics is as yet uncharacterized. Under anaerobic conditions, both soluble and membrane-associated enzymes of the electron transfer system were reported to mediate Cr6+ reduction as a fortuitous process coupled to the oxidation of an electron donor substrate. In this process, Cr6+ serves as the terminal electron acceptor of an electron transfer chain that frequently involves cytochromes (e.g., b and c). An expanding array of Cr6+ reductases allows the selection of enzymes with higher reductive activity, which genetic and/or protein engineering may further enhance their efficiencies. With the advancement in technology for enzyme immobilization, it is speculated that the direct application of Cr6+ reductases may be a promising approach for bioremediation of Cr6+ in a wide range of environments.

Introduction

The anthropogenic inputs of chromium have increased rapidly since the industrial revolution (Nriagu and Pacyna, 1988; Ayres, 1992). Chromium is extensively used in electroplating (as chromeplating), resistant alloys (e.g., stainless steel), leather tanneries and dye productions (Bailar, 1997; United States Environmental Protection Agency, 1998; Ryan et al., 2002). Chromium exists in a wide range of valency states from −4 to +6, with the hexavalent species (Cr6+) predominant in natural aquifers and its trivalent counterpart (Cr3+) prevailing in the municipal wastewater rich in organics (Fukai, 1967; Jan and Young, 1978). Apart from its toxicity (discussed in Section 2), Cr6+ is also highly soluble and thus mobile and biologically available in the ecosystems. In contrast, Cr3+ displays a high affinity for organics resulting in the formation of complexes that precipitate as amorphous hydroxide (Palmer and Wittbrodt, 1991; Sawyer et al., 1994). Because of its persistence in the environment, anthropogenic release of Cr6+ is a matter of concern (Barlett, 1991; Katz and Salem, 1994).

Section snippets

Toxicity of hexavalent chromium

Chromium is an essential trace element for living organisms (Bailar, 1997). However, a slight elevation in the level of Cr6+ elicits environmental and health problems because of its high toxicity (Petrilli and Flora, 1977; Sharma et al., 1995), mutagenicity (Nishioka, 1975) and carcinogenicity (Venitt and Levy, 1974). Almost every regulatory agency has listed Cr6+ as a priority toxic chemical for control, with the maximum allowable level in drinking water of 50–100 μg l−1 (Tchobanoglous and

Microbial detoxification of hexavalent chromium

Traditionally, physico-chemical processes are used to reduce Cr6+ concentrations to levels that comply with statutory standards. Most commonly used processes include reduction–precipitation, ion exchange and reverse osmosis. However, the costs to set up the required equipment and to operate these processes are prohibitively high for large-scale treatment (Mahajan, 1985; Bhide et al., 1996; Beleza et al., 2001). The cell membrane is nearly impermeable to Cr3+ and thus Cr3+ has only approx.

Bioremediation limitations and potentials

The application of microorganisms to detoxifying metals has been tested in a number of systems, but the viability and metabolic activity of cells are still the major limiting factors affecting the detoxification efficiency of the cellular biomass and enzymes involved. The immobilization of microorganisms on surfaces in treatment systems may increase the biomass loading and hence the rate of metal transformation. For example, the immobilization of cells in the agarose–alginate gel slightly

Acknowledgments

We thank Miss Catty Chan for the computer graphic production. The preparation of this manuscript was supported by The University of Hong Kong and an 863 Project (no. 2002AA601160).

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