Microbial Redox Cycling of Arsenic Oxyanions in Anoxic Environments

By Ronald S. Oremland
U.S. Geological Survey 345 Middlefield Road, Bldg. 15, Menlo Park, California 94025

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Abstract

While we normally associate the element arsenic with poisoning and death, paradoxically it can also serve as the fundamental basis for life-giving bioenergetic reactions in certain types of microorganisms. This is not to say that microbes differ from metazoans with regard to As toxicity; indeed it is also quite toxic to them as well. However, many microorganisms have evolved a variety of plasmid encoded strategies that protect them from the deleterious effects of heavy metals, including arsenic. Most of these resistance mechanisms involve redox reactions whereby either the internal pools of cytoplasmic arsenate [As(V)] are rapidly reduced to arsenite [As(III)] for extrusion from the cell, or external As(III) is oxidized at the cell surface and denied entry into the cell. But in the case of arsenic, and to a great extent selenium as well, other anaerobic Bacteria and Archaea can actually conserve the energy gained via the oxidation of organic compounds (or H₂) with the reduction of As(V) to As(III). This process is termed dissimilatory arsenate reduction, and is a means of anaerobic respiration that supports the growth of a number of recently discovered, phylogenetically diverse microorganisms (Figure 1). For example, growth of the bacterium Sulfurospirillum barnesii on lactate and As(V) at pH 7.0 conforms to the following stoichiometry:

Lactate^- + 2HAsO₄⁼ + 3 H⁺   →   Acetate^-  + 2 H₃AsO₃  + HCO₃^-       ΔG_o^/   =  - 174 kJ/mole lactate

Because As(III) is hydrologically more mobile and biochemically more toxic than As(V), the dissimilatory reduction of As(V) represents an important means by which arsenic can be mobilized and transported from the adsorbed solid phase into the liquid phase (Zobrist and others, 2000). This process can therefore be of importance in anoxic sediments, soils, and subsurface aquifers. Several recent reviews on this phenomenon have appeared in the literature (Newman and others, 1998; Stolz and Oremland, 1999; Oremland and Stolz, 2000; Oremland and others, 2001). In certain anoxic, arsenic-rich environments, As(V) reduction represents an ecologically significant  terminal electron acceptor for the mineralization of organic carbon. For example, in Mono Lake, California where the dissolved inorganic arsenic concentration is 0.2 mM, dissimilatory As(V) reduction can mineralize 8 - 14 % of annual primary production by phytoplankton (Oremland et al., 2000).

It was in alkaline (pH = 9.8), hypersaline Mono Lake that another aspect of microbial redox cycling of arsenic was recently discovered, namely the anaerobic oxidation of As(III) with nitrate or Fe(III) as oxidants (Hoeft and others, 2002). A Gram negative bacterium, strain MLHE-1, was isolated from lake water that demonstrated chemoautotrophic growth with As(III) as its electron donor according to the equation:

H₂AsO₃^- + NO₃^-  →   H₂AsO₄^- + NO₂^-          ΔG_o^/ = - 87.16 kJ/mole   (Oremland and others, 2002).

Microbiologically-linked oxidation of As(III) with nitrate has also been inferred to occur in Upper Mystic Lake, MA, an As-contaminated freshwater lake (D. Senn and H. Hemond, personal communication). Therefore, this process is not confined to just soda lakes, but is likely to be widespread in nature. When taken together with the aerobic chemoautotrophic oxidation of As(III) by strain NT-26 (Santini and others, 2000), it is clear that some microorganisms can also conserve energy for growth by oxidizing As(III) with stronger oxidants, like Fe(III), nitrate, or oxygen. This process is likely to be of importance in retarding the mobility of arsenic in subsurface aquifers that are poor in organics, but have abundant oxygen or nitrate to serve as oxidants. In addition, it is possible that oxygen- or nitrate-linked oxidation of As(III) by these microbes can be a mechanism by which arsenopyrite minerals in rocks ultimately undergo dissolution.    

Figure 1: Dissimilatory reduction of arsenate and selenate amongst the taxonomic domains of Bacteria and Archaea. Prokaryotes that respire arsenate are shown as black dots, selenium oxyanions as white dots, and microbes that can achieve respiratory growth with oxyanions of both elements as gray dots. This property occurs in both Gram + and diverse Gram - species, as well as in the Crenoachaeota. Since this tree was constructed in June, 2001, several new species have been described in literature that are not included in the figure.

References

Hoeft, S.E. and others. 2002. Characterization of microbial arsenate reduction in the anoxic bottom waters of  Mono Lake, California. Geomicrobiol. J. 19: 1 - 18.

Newman, D.K., and others. 1998. A brief review of microbial arsenate respiration. Geomicrobiol. J. 15: 255 - 268.

Oremland, R.S., and others. 2002. Anaerobic oxidation of arsenite by a chemoautotrophic bacterium isolated from Mono Lake, California. Nature (in review).

Oremland, R.S. and others. 2001. Bacterial respiration of arsenate and its significance in the environment. In Environmental Chemistry of Arsenic (W.T. Frankenberger, Jr., ed.), p. 273 - 295, Marcel Dekker, N.Y.

Oremland, R.S., and J.F. Stolz. 2000. Dissimilatory reduction of selenate and arsenate in nature. In Environmental Mtela-Microbe Interactions (D.R. Lovley, ed.), p. 199 - 224, ASM Press, Washington, D.C.

Oremland, R.S., and others.2000. Bacterial dissimilatory reduction of arsenate and sulfate in meromictic Mono Lake, California. Geochim. Cosmochim. Acta 64: 3073 - 3084.

Santini, J.M., and others. 2000. A new chemoautotrophic arsenite-oxidizng bacterium isolated from a gold mine: phylogenetic, physiological, and preliminary biochemical studies. Appl. Environ. Microbiol. 66: 92 - 97.

Stolz, J.F., and R.S. Oremland. 1999. Bacterial respiration of arsenic and selenium. FEMS Microbiol. Rev. 23: 615 - 627.

Zobrist, J. and others. 2000.  Mobilization of arsenite by dissimilatory reduction of adsorbed arsenate. Environ. Sci. Technol. 34: 4747 - 4753.

In George R. Aiken and Eve L. Kuniansky, editors, 2002, U.S. Geological Survey Artificial Recharge Workshop Proceedings, Sacramento, California, April 2-4, 2002: USGS Open-File Report 02-89

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