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The ars Detoxification System Is Advantageous but Not Required for As(V) Respiration by the Genetically Tractable Shewanella Species Strain ANA-3

Saltikov, Chad W. and Cifuentes, Ana and Venkateswaran, Kasthuri and Newman, Dianne K. (2003) The ars Detoxification System Is Advantageous but Not Required for As(V) Respiration by the Genetically Tractable Shewanella Species Strain ANA-3. Applied and Environmental Microbiology, 69 (5). pp. 2800-2809. ISSN 0099-2240. PMCID PMC154534.

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Arsenate [As(V); HAsO42-] respiration by bacteria is poorly understood at the molecular level largely due to a paucity of genetically tractable organisms with this metabolic capability. We report here the isolation of a new As(V)-respiring strain (ANA-3) that is phylogenetically related to members of the genus Shewanella and that also provides a useful model system with which to explore the molecular basis of As(V) respiration. This gram-negative strain stoichiometrically couples the oxidation of lactate to acetate with the reduction of As(V) to arsenite [As(III); HAsO2]. The generation time and lactate molar growth yield (Ylactate) are 2.8 h and 10.0 g of cells mol of lactate-1, respectively, when it is grown anaerobically on lactate and As(V). ANA-3 uses a wide variety of terminal electron acceptors, including oxygen, soluble ferric iron, oxides of iron and manganese, nitrate, fumarate, the humic acid functional analog 2,6-anthraquinone disulfonate, and thiosulfate. ANA-3 also reduces As(V) to As(III) in the presence of oxygen and resists high concentrations of As(III) (up to 10 mM) when grown under either aerobic or anaerobic conditions. ANA-3 possesses an ars operon (arsDABC) that allows it to resist high levels of As(III); this operon also confers resistance to the As-sensitive strains Shewanella oneidensis MR-1 and Escherichia coli AW3110. When the gene encoding the As(III) efflux pump, arsB, is inactivated in ANA-3 by a polar mutation that also eliminates the expression of arsC, which encodes an As(V) reductase, the resulting As(III)-sensitive strain still respires As(V); however, the generation time and the Ylactate value are two- and threefold lower, respectively, than those of the wild type. These results suggest that ArsB and ArsC may be useful for As(V)-respiring bacteria in environments where As concentrations are high, but that neither is required for respiration.

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Newman, Dianne K.0000-0003-1647-1918
Additional Information:© 2003, American Society for Microbiology. Received 14 October 2002/ Accepted 26 February 2003 We thank Joanna Levitt and Anabel Anton for help with the isolation of ANA-3 during the 1998 MBL Microbial Diversity Course, Doug Lies and members of the Newman lab for valuable discussions, Angela Snow for laboratory assistance, and B. P. Rosen for providing E. coli strain AW3110. Funding was provided by grants from the Luce Foundation and the Packard Foundation to D.K.N. and by a National Science Foundation Postdoctoral Fellowship in Microbial Biology to C.W.S.
Funding AgencyGrant Number
Henry Luce FoundationUNSPECIFIED
David and Lucile Packard FoundationUNSPECIFIED
NSF Postdoctoral FellowshipUNSPECIFIED
Issue or Number:5
PubMed Central ID:PMC154534
Record Number:CaltechAUTHORS:SALaem03
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Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:1978
Deposited By: Archive Administrator
Deposited On:28 Feb 2006
Last Modified:02 Oct 2019 22:48

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