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Microbial respiration on selenium and arsenic oxyanions

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Text Box:Selenium and arsenic are intriguing elements: Se is an essential trace element, but toxic in excess, while As is one of the most toxic elements even in trace amounts. Although generally present in the environment at low levels, Se and As are actively metabolized by microorganisms, a process that has a strong impact on their mobility and bioavailability. Changes in the redox environment are expected to impact the microbially mediated oxidation-reduction reactions of Se and As. These transformations may modulate the toxicity of these elements and change their mobility and bioavailability, which in turn affect their translocation and accumulation in the environment.
Despite the low availability of As and Se, the reduction of their oxyanions for energy conservation is well established and now shown to be widespread in bacteria and archaea. Given the scarcity of Se and As on the Earth’s crust, it is puzzling that pathways dedicated to the respiration of their oxyanions have arisen and have been maintained throughout evolution, in the most diverse environments and taxonomic groups. Over the past decade, several microbes have been cultivated that can respire selenium and arsenic oxyanions and new species continue to be discovered. Microorganisms that can utilize Se and As oxyanions as terminal electron acceptors in dissimilatory reduction are ubiquitous and phylogenetically diverse. Their physiological and metabolic characteristics vary greatly and the ability to respire these oxyanions is usually one of the distinguishing factors separating them from their close relatives.

Text Box: One of the most recently described species, Desulfurispirillum indicum strain S5, is an obligate anaerobic bacterium able to grow by respiring a range of different electron acceptors, including arsenate, selenate and nitrate. Consistent with thermodynamic predictions, the reduction of nitrate to ammonium yields higher cell densities than the reduction arsenate to arsenite. However, D. indicum grows considerably faster by respiration on arsenate compared to nitrate. D. indicum thus represents the physiology of an As-respiring “specialist”. An intriguing question is how this strong response to arsenate evolved in D. indicum and whether it is found in other As-respiring microorganisms. While nitrate is a common electron acceptor for many different microorganisms, the ability to respire arsenate is comparatively rare. Interesting,, another isolate, Seleniivibrio woodruffii in the Defferribacteraceae, can respire arsenate and selenate, but not nitrate.
The occurrence, physiology and ecology of these organisms in As- and Se-rich soils and sediments merit further investigation. We seek to elucidate the role of Se and As-respiring microorganisms in the biogeochemical cycling of these elements and determine how their activity is impacted by the redox environment. Our overall hypothesis is that the interaction of water level-driven variation in redox conditions and microbial community composition controls how As- and Se-respiring bacteria affect the geochemistry which affects the bioavailability, mobility and/or toxicity of these two elements.

Collaborators: Nathan Yee, Elisabetta Bini, John Reinfelder, Yong-Guan Zhu

Rauschenbach I, Narasingarao P, Häggblom MM (2011) Desulfurispirillum indicum sp. nov., a selenate and selenite respiring bacterium isolated from an estuarine canal in Southern India. Int. J. System. Evol. Microbiol. 61: 654 - 658. (doi:10.1099/ijs.0.022392-0)

Rauschenbach I, Yee N, Häggblom MM, Bini E (2011) Energy metabolism and multiple respiratory pathways revealed by genome sequencing of Desulfurispirillum indicum strain S5. Environmental Microbiology 13:1611-1621. (doi:10.1111/j.1462-2920.2011.02473.x)

Rauschenbach I, Bini E, Häggblom MM, Yee N (2012) Physiological response of Desulfurispirillum indicum strain S5 to arsenate and nitrate as terminal electron acceptors. FEMS Microbiology Ecology 81:156-162. (DOI: 10.1111/j.1574-6941.2012.01351.x)

Rauschenbach I, Posternak V, Cantarella P, McConnell J, Starovoytov V, Häggblom MM (2013) Seleniivibrio woodruffii gen. nov., sp. nov., a selenate and arsenate respiring bacterium in the Deferribacteraceae. Int. J. System. Evol. Microbiol. 63:3659-3665. (DOI 10.1099/ijs.0.043547-0)