AUTHOR=Shin Hyun-Dong , Toporek Yael , Mok Jung Kee , Maekawa Ruri , Lee Brady D. , Howard M. Hope , DiChristina Thomas J. 

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

JOURNAL=Frontiers in Microbiology

VOLUME=Volume 13 - 2022

YEAR=2022

URL=https://www.frontiersin.org/journals/microbiology/articles/10.3389/fmicb.2022.852942

DOI=10.3389/fmicb.2022.852942

ISSN=1664-302X

ABSTRACT=Microbial iodate (IO3-) 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 IO3- to iodide (I-) and microbial methylation of I- to volatile gases. The metal reduction pathway is required for anaerobic IO3- respiration by the gamma-proteobacterium Shewanella oneidensis. However, the terminal IO3- reductase and additional enzymes involved in the S. oneidensis IO3- electron transport chain have not yet been identified. In the present study, gene deletion mutants deficient in four extracellular electron conduits (EECs; mtrA, mtrA-mtrDEF, mtrA-dmsEF, mtrA-SO4360) and DMSO reductase (dmsB) of S. oneidensis were constructed and examined for anaerobic IO3- reduction activity with either 20 mM lactate or formate as electron donor. IO3- reduction rate experiments were conducted under anaerobic conditions in defined minimal medium amended with 250 μM IO3- as anaerobic electron acceptor. Only the mtrA mutant displayed a severe deficiency in IO3- reduction activity with lactate as electron donor, which suggested that the EEC-associated decaheme cytochrome was required for lactate-dependent IO3- reduction. The mtrA-dmsEF triple mutant displayed a severe deficiency in IO3- reduction activity with formate as electron donor, while mtrA-mtrDEF and mtrA-SO4360 retained moderate IO3- reduction activity, which suggested that the EEC-associated dimethylsulfoxide (DMSO) reductase membrane-spanning protein DmsE, but not MtrA, was required for formate-dependent IO3- reduction. Furthermore, gene deletion mutant dmsB (deficient in the extracellular terminal DMSO reductase protein DmsB) and wild-type cells grown with tungsten replacing molybdenum (a required cofactor for DmsA catalytic activity) in defined growth medium were unable to reduce IO3- with either lactate or formate as electron donor, which indicated that the DmsAB complex functions as an extracellular IO3- terminal reductase for both electron donors.  Results of the present study provide complementary genetic and phenotypic evidence that the extracellular DMSO reductase complex DmsAB of S. oneidensis displays broad substrate specificity and reduces IO3- as an alternate terminal electron acceptor.