The ars detoxification system is advantageous but not required for As(V) respiration by the genetically tractable Shewanella species strain ANA-3.
Arsenate [As(V); HAsO(4)(2-)] 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); HAsO(2)]. The generation time and lactate molar growth yield (Y(lactate)) 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 Y(lactate) 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.
Department Geological and Planetary Sciences, California Institute of Technology, Pasadena, CA 91125, USA.
Chad W
CW
Saltikov
Ana
A
Cifuentes
Kasthuri
K
Venkateswaran
Dianne K
DK
Newman
D001149:Arsenates / Q000493:pharmacokinetics*; D053501:Arsenite Transporting ATPases; D001483:Base Sequence; D019069:Cell Respiration; D004269:DNA, Bacterial / Q000235:genetics; D004275:DNA, Ribosomal / Q000235:genetics; D008658:Inactivation, Metabolic; D016623:Ion Pumps / Q000235:genetics* / Q000378:metabolism*; D009097:Multienzyme Complexes / Q000235:genetics* / Q000378:metabolism*; D016296:Mutagenesis; D009876:Operon; D010802:Phylogeny; D020592:Shewanella / Q000145:classification / Q000235:genetics* / Q000302:isolation & purification / Q000378:metabolism*; D014871:Water Microbiology; D014874:Water Pollutants, Chemical / Q000493:pharmacokinetics*
D001149:Arsenates; D004269:DNA, Bacterial; D004275:DNA, Ribosomal; D016623:Ion Pumps; D009097:Multienzyme Complexes; D014874:Water Pollutants, Chemical; D053501:Arsenite Transporting ATPases; C025657:arsenic acid