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

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 gammaproteobacterium 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 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 IO3– reduction activity with either 20 mM lactate or formate as an 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 ΔmtrA mutant displayed a severe deficiency in IO3– reduction activity with lactate as the electron donor, which suggested that the EEC-associated decaheme cytochrome was required for lactate-dependent IO3– reduction. The ΔmtrA-ΔdmsEF triple mutant displayed a severe deficiency in IO3– reduction activity with formate as the electron donor, whereas ΔmtrA-ΔmtrDEF and ΔmtrA-ΔSO4360 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 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 IO3– with either lactate or formate as the electron donor, which indicated that the DmsAB complex functions as an extracellular IO3– 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 IO3– as an alternate terminal electron acceptor.

The roles of DmsEFAB and MtrCAB in extracellular reduction of iodate by Shewanella oneidensis MR‐1 with lactate as the sole electron donor

“…À by other bacteria (Reyes-Umana et al, 2022;Yamazaki et al, 2020), but differ substantially from the mechanism of extracellular reduction of IO 3 À that was recently proposed for S. oneidensis MR-1 (Shin et al, 2022).…”

“…After original submission of this manuscript, new results suggested that when lactate or formate used as the sole electron donor, S. oneidensis MR-1 reduced IO 3 À to I À extracellularly via MtrABDm-sAB or DmsEFAB, respectively. However, whether H 2 O 2 was generated during the reduction was unclear (Shin et al, 2022).…”

Bromate reduction by Shewanella oneidensis MR-1 is mediated by dimethylsulfoxide reductase

“…Shewanella oneidensis MR-1 did not exhibit the characteristic of bromate-respiring under anaerobic conditions (Supplementary Figures 1A,B), indicating that S. oneidensis MR-1 may not respire a high concentration of bromate under the anaerobic conditions of this study. However, according to previous findings (Toporek et al, 2019;Guo et al, 2022;Shin et al, 2022), when S. oneidensis MR-1 has sufficient biomass, it is still possible to perform anaerobic reduction of bromate at low concentrations. As expected, it was found that S. oneidensis MR-1 and the bromate-reducing bacterium S. decolorationis Ni1-3 have a similar bromate-reducing ability, and that both of them can reduce bromate to bromide with high efficiency Figures 1A,B).…”

“…The purified reductases of bacteria (i.e., PcrA, ClrA, NarG, SerA, and TorA) with bromate-reducing activity all belong to the DMSO reductase family ( Miralles-Robledillo et al, 2019 ). DmsEFAB, the complex protein of S. oneidensis MR-1, has been proved to mediate the dissimilatory reduction of DMSO and the extracellular reduction of iodate ( Gralnick et al, 2006 ; Guo et al, 2022 ; Shin et al, 2022 ). DmsA is located in the outer membrane and is the catalytic subunit; it also belongs to the DMSO reductase family ( Gralnick et al, 2006 ).…”

“…The Shewanella genus currently includes around 70 species that are widely distributed in aquatic environments such as freshwater and marine sediments around the world ( Lemaire et al, 2020 ). Knowledge of the respiratory diversity of Shewanella species is mainly derived from the model strain Shewanella oneidensis MR-1, which can reduce diverse oxyanions including iodate, sulfite, nitrate, U(VI), Cr(VI), and selenite ( Shirodkar et al, 2011 ; Li et al, 2014 ; Beblawy et al, 2018 ; Lemaire et al, 2020 ; Vettese et al, 2020 ; Guo et al, 2022 ; Shin et al, 2022 ). Bromate is a halogen oxyanion with a molecular structure and chemical properties similar to iodate.…”