To investigate their roles in extracellular reduction of iodate (IO3−) with lactate as an electron donor, the gene clusters of dmsEFAB, mtrCAB, mtrDEF and so4360‐4357 in Shewanella oneidensis MR‐1 were systematically deleted. Deletions of dmsEFAB and/or mtrCAB gene clusters diminished the bacterial ability to reduce IO3−. Furthermore, DmsEFAB and MtrCAB worked collaboratively to reduce IO3− of which DmsEFAB played a more dominant role than MtrCAB. MtrCAB was involved in detoxifying the reaction intermediate hydrogen peroxide (H2O2). The reaction intermediate hypoiodous acid (HIO) was also found to inhibit microbial IO3− reduction. SO4360‐4357 and MtrDEF, however, were not involved in IO3− reduction. Collectively, these results suggest a novel mechanism of extracellular reduction of IO3− at molecular level, in which DmsEFAB reduces IO3− to HIO and H2O2. The latter is further reduced to H2O by MtrCAB to facilitate the DmsEFAB‐mediated IO3− reduction. The extracellular electron transfer pathway of S. oneidensis MR‐1 is believed to mediate electron transfer from bacterial cytoplasmic membrane, across the cell envelope to the DmsEFAB and MtrCAB on the bacterial outer membrane.

The γ-proteobacterium Shewanella oneidensis MR-1 reduces iodate to iodide extracellularly. Both dmsEFAB and mtrCAB gene clusters are involved in extracellular reduction of iodate by S. oneidensis MR-1. DmsEFAB reduces iodate to hypoiodous acid and hydrogen peroxide (H2O2). Subsequently, H2O2 is reduced by MtrCAB to facilitate DmsEFAB-mediated extracellular reduction of iodate. To investigate the distribution of bacteria with the capability for extracellular reduction of iodate, bacterial genomes were systematically searched for both dmsEFAB and mtrCAB gene clusters. The dmsEFAB and mtrCAB gene clusters were found in three Ferrimonas and 26 Shewanella species. Coexistence of both dmsEFAB and mtrCAB gene clusters in these bacteria suggests their potentials for extracellular reduction of iodate. Further analyses demonstrated that these bacteria were isolated from a variety of ecosystems, including the lakes, rivers, and subsurface rocks in East and Southeast Asia, North Africa, and North America. Importantly, most of the bacteria with both dmsEFAB and mtrCAB gene clusters were found in different marine environments, which ranged from the Arctic Ocean to Antarctic coastal marine environments as well as from the Atlantic Ocean to the Indian and Pacific Oceans. Widespread distribution of the bacteria with capability for extracellular reduction of iodate around the world suggests their significant importance in global biogeochemical cycling of iodine. The genetic organization of dmsEFAB and mtrCAB gene clusters also varied substantially. The identified mtrCAB gene clusters often contained additional genes for multiheme c-type cytochromes. The numbers of dmsEFAB gene cluster detected in a given bacterial genome ranged from one to six. In latter, duplications of dmsEFAB gene clusters occurred. These results suggest different paths for these bacteria to acquire their capability for extracellular reduction of iodate.