Iodate Reduction by Shewanella oneidensis Requires Genes Encoding an Extracellular Dimethylsulfoxide Reductase

Microbial iodate (IO(3)(–)) reduction is a major component of the iodine biogeochemical reaction network in anaerobic marine basins and radioactive iodine-contaminated subsurface environments. Alternative iodine remediation technologies include microbial reduction of IO(3)(–) to iodide (I(–)) and microbial methylation of I(–) to volatile gases. The metal reduction pathway is required for anaerobic IO(3)(–) respiration by the gammaproteobacterium Shewanella oneidensis. However, the terminal IO(3)(–) reductase and additional enzymes involved in the S. oneidensis IO(3)(–) electron transport chain have not yet been identified. In this study, gene deletion mutants deficient in four extracellular electron conduits (EECs; ΔmtrA, ΔmtrA-ΔmtrDEF, ΔmtrA-ΔdmsEF, ΔmtrA-ΔSO4360) and DMSO reductase (ΔdmsB) of S. oneidensis were constructed and examined for anaerobic IO(3)(–) reduction activity with either 20 mM lactate or formate as an electron donor. IO(3)(–) reduction rate experiments were conducted under anaerobic conditions in defined minimal medium amended with 250 μM IO(3)(–) as anaerobic electron acceptor. Only the ΔmtrA mutant displayed a severe deficiency in IO(3)(–) reduction activity with lactate as the electron donor, which suggested that the EEC-associated decaheme cytochrome was required for lactate-dependent IO(3)(–) reduction. The ΔmtrA-ΔdmsEF triple mutant displayed a severe deficiency in IO(3)(–) reduction activity with formate as the electron donor, whereas ΔmtrA-ΔmtrDEF and ΔmtrA-ΔSO4360 retained moderate IO(3)(–) reduction activity, which suggested that the EEC-associated dimethylsulfoxide (DMSO) reductase membrane-spanning protein DmsE, but not MtrA, was required for formate-dependent IO(3)(–) reduction. Furthermore, gene deletion mutant ΔdmsB (deficient in the extracellular terminal DMSO reductase protein DmsB) and wild-type cells grown with tungsten replacing molybdenum (a required co-factor for DmsA catalytic activity) in defined growth medium were unable to reduce IO(3)(–) with either lactate or formate as the electron donor, which indicated that the DmsAB complex functions as an extracellular IO(3)(–) terminal reductase for both electron donors. Results of this study provide complementary genetic and phenotypic evidence that the extracellular DMSO reductase complex DmsAB of S. oneidensis displays broad substrate specificity and reduces IO(3)(–) as an alternate terminal electron acceptor.