ANRV286-MI60-05 ARI 16 August 2006 16:34 Arsenic and Selenium in Microbial Metabolism∗ John F. Stolz,1 Partha Basu,2 Joanne M. Santini,3 and Ronald S. Oremland4 1Department of Biological Sciences, Duquesne University, Pittsburgh, Pennsylvania 15282; email: [email protected] 2Department of Chemistry and Biochemistry, Duquesne University, Pittsburgh, Pennsylvania 15282; email: [email protected] 3Department of Biology, University College London, London WC1E 6BT, United Kingdom; email: [email protected] 4Water Resources Division, U.S. Geological Survey, Menlo Park, California 94025; email: [email protected] Annu. Rev. Microbiol. 2006. 60:107–30 Key Words First published online as a Review in selenate respiration, selenocysteine, arsenate reductase, arsenite Advance on May 8, 2006 oxidase, biogeochemical cycles, organoarsenicals The Annual Review of Microbiology is online at micro.annualreviews.org Abstract This article’s doi: Arsenic and selenium are readily metabolized by prokaryotes, par- 10.1146/annurev.micro.60.080805.142053 ticipating in a full range of metabolic functions including as- by Duquesne University on 09/12/06. For personal use only. Copyright c 2006 by Annual Reviews. similation, methylation, detoxification, and anaerobic respiration. All rights reserved Arsenic speciation and mobility is affected by microbes through 0066-4227/06/1013-0107$20.00 oxidation/reduction reactions as part of resistance and respiratory ∗The U.S. Government has the right to processes. A robust arsenic cycle has been demonstrated in diverse Annu. Rev. Microbiol. 2006.60:107-130. Downloaded from arjournals.annualreviews.org retain a nonexclusive, royalty-free license environments. Respiratory arsenate reductases, arsenic methyltrans- in and to any copyright covering this ferases, and new components in arsenic resistance have been recently paper. described. The requirement for selenium stems primarily from its in- corporation into selenocysteine and its function in selenoenzymes. Selenium oxyanions can serve as an electron acceptor in anaero- bic respiration, forming distinct nanoparticles of elemental selenium that may be enriched in 76Se. The biogenesis of selenoproteins has been elucidated, and selenium methyltransferases and a respiratory selenate reductase have also been described. This review highlights recent advances in ecology, biochemistry, and molecular biology and provides a prelude to the impact of genomics studies. 107 ANRV286-MI60-05 ARI 16 August 2006 16:34 lights some of the most recent advances in Contents ecology, biochemistry, and molecular biology and discusses the impact genomics studies are INTRODUCTION................. 108 beginning to have. Phylogeny and Diversity .......... 108 Ecology.......................... 109 ARSENIC IN CELLULAR Phylogeny and Diversity METABOLISM.................. 112 Concerted efforts have been made over the Methylation ...................... 112 past decade to isolate and characterize organ- Organoarsenicals ................. 114 isms capable of generating energy from oxi- Arsenic Resistance ................ 114 dation/reduction reactions with oxyanions of Respiratory Arsenate Reductase . 115 arsenic and selenium. These efforts have been Arsenite Oxidase ................. 117 aided by the identification of environments SELENIUM IN CELLULAR where these elements play an important role METABOLISM.................. 118 in ecology (see below), the development of Selenocysteine ................... 119 selective media, and the inclusion of arsenate Methylation ...................... 120 and selenate as electron acceptors tested in Respiratory Selenate Reductase . 121 the characterization of new isolates. As a re- CONCLUSIONS AND FUTURE sult, the list of species capable of carrying out DIRECTIONS .................. 121 oxidization/reduction reactions with oxyan- ions of selenium and arsenic continues to grow. Arsenite-oxidizing bacteria have been INTRODUCTION known since 1918 (34); however, the first Selenium (Se) has been called an “essential chemolithoautotrophic species were de- toxin,” as it is required for certain cell pro- scribed only recently (92, 121). More Selenate cesses and enzymes, but it becomes delete- than 30 strains representing at least nine respiration: the generation of energy rious at greater doses. The requirement for genera of arsenite-oxidizing prokaryotes through the selenium stems primarily from its incorpora- have been reported and include α-, β-, dissimilatory tion into selenocysteine and its function in and γ-Proteobacteria, and Thermus (97). reduction of selenate selenoenzymes. Arsenic (As) is also consid- Physiologically diverse, they include het- Chemolitho- ered an essential toxin, but its beneficial qual- erotrophic and chemolithoautotrophic by Duquesne University on 09/12/06. For personal use only. autotrophic ities are more subtle. In humans, acute and arsenite-oxidizing prokaryotes (32, 117, 121, arsenite-oxidizing chronic exposures result in defined patholo- 122). It is also apparent that green sulfur (e.g., prokaryotes: microbes that gies (e.g., arsenicosis, arseniasis, and death), Chlorobium limicola and Chlorobium phaeobac- generate energy and yet arsenic can promote angiogenesis and teroides) and filamentous green nonsulfur Annu. Rev. Microbiol. 2006.60:107-130. Downloaded from arjournals.annualreviews.org through arsenite increased respiratory capacity. In prokaryotes, bacteria (e.g., Chloroflexus aurantiacus) may oxidation while using these two elements are readily metabolized be capable of arsenite oxidation, as homologs carbon dioxide for and participate in a full range of metabolic of arsenite oxidase have been identified in cell carbon functions including assimilation, methylation, their genomes. Arsenite oxidation by Archaea Heterotrophic detoxification, and anaerobic respiration. Re- has yet to be definitively demonstrated; arsenite-oxidizing prokaryotes: cent reviews have provided overviews of the however, arsenic oxidation and reduction in microbes that oxidize microbial ecology of selenium (133) and ar- Sulfolobus acidocaldarius have been reported arsenite but require senic (97, 98); the resistance mechanisms for (130) and homologs of arsenite oxidase have an alternative source arsenic (82, 112); and the biochemistry and been identified in the genomes of Sulfolobus of energy and molecular biology involved in selenoproteins tokodaii and Aeropyrum pernix (64). In addi- organic matter for growth (24), selenate respiration (123), and arsenic tion, archaeal 16S rDNA sequences, those metabolism (15, 123, 131). This review high- of both Crenarchaeota and Euryarchaeota, 108 Stolz et al. ANRV286-MI60-05 ARI 16 August 2006 16:34 were found to coincide with the zone of ing other terminal electron acceptors such arsenite oxidation in a Yellowstone hot spring as oxygen, nitrate, nitrite, Fe(III), fumarate, (50). Most species are aerobic, using oxygen sulfate, thiosulfate, sulfur, dimethyl sulfoxide, Arsenate as the electron acceptor. However, the and trimethyl amine oxide (97). respiration: the γ-Proteobacterium Alcalilimnicola ehrlichei Prokaryotes capable of gaining energy generation of energy (strain MLHE-1) oxidizes arsenite under from oxidation/reduction reactions with through the anoxic conditions while respiring nitrate (92), oxyanions of selenium are also phylogenet- dissimilatory and two recently described chemolithoau- ically diverse and metabolically versatile. At reduction of arsenate totrophs, α-Proteobacterium strain DAO10 present, 20 species are known and include and β-Proteobacterium strain DAO1, couple members of the Crenarchaeota, low and high arsenite oxidation to denitrification (110). G+C gram-positive bacteria, Halanaerobac- Thus, arsenite can serve as an electron donor ter, and β-, γ-, and ε-Proteobacteria. Many of in anaerobic respiration. The discovery of the organisms also use arsenate as a terminal arsenite oxidase in anaerobic photosynthetic electron acceptor; however, only the haloalka- bacteria poses the intriguing possibility that liphilic Bacillus selenitireducens (137) and three arsenite might be a source of electrons in strains of an Aquificales species (HGMK-1, 2, photosynthesis. and 3) (138) use selenite. Dissimilatory arsenate-reducing bacteria are a more recent discovery (3, 63, 70, 71, 87). Nevertheless, at last count at least 24 Ecology prokaryotes use arsenate as a terminal electron Biogeochemical cycle of arsenic. Arsenic acceptor (97, 98). They include members of primarily occurs in four oxidation states, arse- the Crenarchaeota, Aquificae, Chrysiogenes, nate As(V), arsenite As(III), elemental As(0), Deferribacteres, low G+C gram-positive bac- and arsenide As(-III). Inorganic As(V) and − teria, Halanaerobacter, and γ-, δ-, and ε- As(III) are readily soluble with H2AsO4 and = Proteobacteria (98). A full range of elec- HAsO4 occurring primarily in aerobic envi- o − tron donors are also employed including ronments, and H3AsO3 and H2AsO3 more organics, such as acetate, lactate, and aro- common in anoxic environments. Elemental matics (e.g., syringic acid, ferulic acid, phe- arsenic occurs rarely, and arsines have been nol, benzoate, toluene) (3, 51, 66, 86, 89, identified from fungal cultures and strongly 134, 139), and inorganics (e.g., hydrogen, sul- reducing environments (6). The importance fide). The recently described chemolithoau- of arsenic in microbial ecology and its bio- by Duquesne University on 09/12/06. For personal use only. totrophic arsenate respirer, strain MLMS-1 geochemical cycle have also been realized (a δ-Proteobacterium),