Arsenate respiration

Macy JM, K Nuna, KD Hagen, DR Dixon, PJ Harbour, M Cahill, LI Sly (1996) Chrysiogenes arsenatis gen. nov., sp. nov., a new arsenate-respiring bacterium isolated from gold mine wastewater. Int J Syst Bacteriol 46 1153-1157. 

Saltikov CW, RA Wildman, DK Newman (2005) Expression dynamics of arsenic respiration and detoxification in Shewanella sp. strain ANA-3. J Bacteriol 187 7390-7396. 

Macy, J.M. and Santini, J.M. (2002) Unique modes of arsenate respiration by Chrysiogenes arsenatis and Desulfomi-crobium sp. str. Ben-RB, in Environmental Chemistry of Arsenic (ed. W.T. Frankenberger Jr.), Marcel Dekker, New York, pp. 297-312. 

Microbial arsenate respiration contributes to the mobilization of arsenic from the solid to the soluble phase in various locales worldwide. In particular, microbial respiratory reduction of arsenate, As(V), to arsenite, As(III), is thought... 

FIGURE 72.2. Arsenic detoxification mechanisms (reduction, oxidation, methylation, and resistance) in prokaryotes. (A) Respiratory arsenate reductase (Arr) is involved in the reduction of As(V) by the dissimilatory arsenate respiring organisms. (B) Arsenite oxidase (Aox/Aso) is responsible for oxidation of As(III) by chemoautotrophic or heterotrophic arsenite oxidizers. 

TABLE 72.1. Dissimilatory arsenate-respiring prokaryotes characterized at molecular level... 

Gihring, T.M., Banfield, J.F. (2001). Arsenite oxidation and arsenate respiration by a new Thermus isolate. FEMS Microbiol. Lett. 204 335-40. 

L.L., Lisak, J., Stolz, J.F., Oremland, R.S. (2002). Dissimila-tory arsenate reductase activity and arsenate-respiring bacteria in bovine rumen fluid, hamster feces, and the termite hindgut. FEMS Microbiol. Ecol. 41 59-67. 

Santini, J.M., Streimann, I.C., Vanden Hoven, R.N. (2004). Bacillus macyae sp. nov., an arsenate-respiring bacterium isolated from an Australian gold mine. Int. J. Syst. Evol. Microbiol. 54 2241-4. 

High arsenic concentrations can also occur in alkaline, closed-basin lakes. Mono Lake, California, USA has dissolved arsenic concentrations of (10-20) X lO pg with pH values in the range 9.5-10 as a result of the combined influences of geothermal activity, weathering of mineralized volcanic rocks, evaporation of water at the lake surface, and a thriving population of arsenate-respiring bacteria (Maest et al., 1992 Oremland et al., 2000). 

Newman et al. (56), and Rochette et al. (68) suggest that the reduction of arsenate by dissolved sulfide is very slow at circumneutral pH values. However, at pH values less than 5, the reduction rates of arsenate due to sulfide may be significant in natural systems, where half-lives as short as 21 hr have been reported (68) for this abiotic pathway (Table 3). Rochette et al. (68) also revealed the potential importance of intermediate As-O-S species in electron transfer reactions between sulfide and arsenate, such as H2 As OsS H2As 02S , and H2 As OS2. It is not known whether these chemical species may also serve as important redox active species for microbial metabolism. These authors have also compared the rates of As(V) reduction in the presence of sulfide versus those rates expected via dissimilatory reduction by an arsenate-respiring organism (strain SES-3) (54) and for those measured in lake sediments (69) at pH values less than 5, reduction rates due to dissolved sulfide can become more significant than reduction rates due to anaerobic respiration where As(V) is used as the terminal electron acceptor (Fig. 8). 

Figure 8 Predicted contributions, based on comparison of rates, for biological and sulfide reduction of arsenate in (a) pure cultures of arsenate respiring bacteria and (b) for natural settings. (Rate data for biological reduction by strain SES3 are from Ref. 54, and for sediments from Ref. 69 data from Refs. 56 and 68 used to calculate sulfide reduction rates.)...

Most of the above examples followed the dissolution of arsenic in complex sediment systems amended with scorodite and cultures of iron- or arsenate-respiring bacteria. More work was needed with simpler, defined systems to unravel the biological mechanisms from the adsorptive chemical phenomena. Zobrist et al. (43) studied the reductive dissolution of ferrihydrite that was coprecipitated with arsenate. Sulfurospirillum barnesii was the organism of choice because it respires both Fe(III) and As(V). Washed cell suspensions of S. barnesii simultaneously reduced Fe(III) as well as As(V) (Fig. 9). However, As(III) still had a... 

These experiments pointed out that respiratory reduction of As(V) sorbed to solid phases can indeed occur in nature, but its extent and the degree of mobilization of the As(III) product is constrained by the type of minerals present in a given system. What remains unclear is whether micro-organisms can actually reduce As(V) while it is attached to the mineral surface, or if they attack a mono-layer of aqueous As(V) that is in equilibrium with the As(V) adsorbed onto the surface layer. If, as is the case for dissimilatory metal-reducing bacteria such as Geobacter sulfurreducens and Shewanella oneidensis (44,45), components of the electron transport chain are localized to the outer-membrane of some arsenate-respiring bacteria, direct reductive dissolution of insoluble arsenate minerals may be possible by attached bacteria. Too little is known at present about the topology... 

Anoxic water samples, because they contain little in the way of particles, are far easier than aquifer materials to develop radioassays for the measurement of arsenate reduction. Arsenic speciation quantitatively changes from arsenate to arsenite with vertical transition from the surface oxic waters to the anoxic bottom depths of stratified lakes and fjords (55,56). This also occurs in Mono Lake, California (57), a transiently meromictic, alkaline (pH = 9.8), and hypersaline (salinity = 70-90 g/L) soda lake located in eastern California (Fig. 11). The combined effects of hydrothermal sources coupled with evaporative concentration have resulted in exceptionally high ( 200 fiM) dissolved arsenate concentrations in its surface waters. Haloalkaliphilic arsenate-respiring bacteria have been isolated from the lake sediments (26), and sulfate reduction, achieved with... 

DK Newman, D Ahmann, FMM Morel. A brief review of microbial arsenate respiration. Geomicrobiol J 15 255-268, 1998. 

Unique Modes of Arsenate Respiration by Chrysiogenes arsenatis and Desulfomicrobium sp. str. Ben-RB... 

The reduction of arsenate [As(V)] to arsenite [As(III)] is known to occur in anoxic environments (1,2). Until recently, however, the organisms responsible for this reduction were not known. A number of different bacteria have been isolated that are able to respire with arsenate, reducing it to arsenite. With one exception, these organisms use the nonrespiratory substrate lactate as the electron donor (3-6) and are listed in Table 1. Two of them, Desulfotomaculum auripig-mentum str. OREX-4 (7,8) md Desulfomicrobium sp. str. Ben-RB (9), also respire with sulfate as the terminal electron acceptor. None are able to use the respiratory substrate acetate as the electron donor for arsenate respiration. The only organism known able to do so is Chrysiogenes arsenatis (10). 

Phylogenetically, C. arsenatis differs from the other arsenate-respiring bacteria and from other phyla of the Bacteria and so is the first representative of a new phylum (11) (see Table 1). The other arsenate-respiring bacteria fall within three different divisions of the Bacteria (see Table 1). The two Bacillus species are, however, unrelated to D. auripigmentum even though they are all members of the low G + C gram-positive bacteria. 

This chapter concentrates on arsenate respiration by Chrysiogenes arsenatis and Desulfomicrobium sp. str. Ben-RB. The evidence indicates that they have specific respiratory arsenate reductases involved in energy generation. The isolation, phytogeny, physiology, and biochemistry of arsenate reduction are described separately for each organism. 

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