Metal Reduction and Protein Secretion Genes Required for Iodate Reduction by Shewanella oneidensis

The metal-reducing gammaproteobacterium Shewanella oneidensis reduces iodate (IO₃^-) as an anaerobic terminal electron acceptor. Microbial IO₃^- electron transport pathways are postulated to terminate with nitrate (NO₃^-) reductase, which reduces IO₃^- as an alternative electron acceptor. Recent studies with S. oneidensis, however, have demonstrated that NO₃^- reductase is not involved in IO₃^- reduction. The main objective of the present study was to determine the metal reduction and protein secretion genes required for IO₃^- reduction by Shewanella oneidensis with lactate, formate, or H₂ as the electron donor. With all electron donors, the type I and type V protein secretion mutants retained wild-type IO₃^- reduction activity, while the type II protein secretion mutant lacking the outer membrane secretin GspD was impaired in IO₃^- reduction. Deletion mutants lacking the cyclic AMP receptor protein (CRP), cytochrome maturation permease CcmB, and inner membrane-tethered c-type cytochrome CymA were impaired in IO₃^- reduction with all electron donors, while deletion mutants lacking c-type cytochrome MtrA and outer membrane β-barrel protein MtrB of the outer membrane MtrAB module were impaired in IO₃^- reduction with only lactate as an electron donor. With all electron donors, mutants lacking the c-type cytochromes OmcA and MtrC of the metal-reducing extracellular electron conduit MtrCAB retained wild-type IO₃^- reduction activity. These findings indicate that IO₃^- reduction by S. oneidensis involves electron donor-dependent metal reduction and protein secretion pathway components, including the outer membrane MtrAB module and type II protein secretion of an unidentified IO₃^- reductase to the S. oneidensis outer membrane.IMPORTANCE Microbial iodate (IO₃^-) reduction is a major component in the biogeochemical cycling of iodine and the bioremediation of iodine-contaminated environments; however, the molecular mechanism of microbial IO₃^- reduction is poorly understood. Results of the present study indicate that outer membrane (type II) protein secretion and metal reduction genes encoding the outer membrane MtrAB module of the extracellular electron conduit MtrCAB are required for IO₃^- reduction by S. oneidensis On the other hand, the metal-reducing c-type cytochrome MtrC of the extracellular electron conduit is not required for IO₃^- reduction by S. oneidensis These findings indicate that the IO₃^- electron transport pathway terminates with an as yet unidentified IO₃^- reductase that associates with the outer membrane MtrAB module to deliver electrons extracellularly to IO₃^.