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Applied and Environmental Microbiology, May 2003, p. 2800-2809, Vol. 69, No. 5
0099-2240/03/$08.00+0     DOI: 10.1128/AEM.69.5.2800-2809.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

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

Chad W. Saltikov,1 Ana Cifuentes,1 Kasthuri Venkateswaran,2 and Dianne K. Newman1*

Department Geological and Planetary Sciences, California Institute of Technology, Pasadena, California 91125,1 Jet Propulsion Laboratory, Planetary Protection Technologies, Pasadena, California 911092

Received 14 October 2002/ Accepted 26 February 2003

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.

* Corresponding author. Mailing address: Department Geological and Planetary Sciences, California Institute of Technology, Mailstop 100-23, Pasadena, CA 91125. Phone: (626) 395-6790. Fax: (626) 683-0621. E-mail: dkn{at}gps.caltech.edu.

Applied and Environmental Microbiology, May 2003, p. 2800-2809, Vol. 69, No. 5
0099-2240/03/$08.00+0     DOI: 10.1128/AEM.69.5.2800-2809.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.



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