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

ABSTRACT: Microbial bromate reduction plays an important role in remediating bromate-contaminated waters as well as biogeochemical cycling of bromine. However, little is known about the molecular mechanism of microbial bromate reduction so far. Since the model strain Shewanella oneidensis MR-1 is capable of reducing a variety of oxyanions such as iodate, which has a high similarity to bromate, we hypothesize that S. oneidensis MR-1 can reduce bromate. Here, we conducted an experiment to investigate whether S. oneidensis MR-1 can reduce bromate, and report bromate reduction mediated by a dimethylsulfoxide reductase encoded with dmsA. S. oneidensis MR-1 is not a bromate-respiring bacterium but can reduce bromate to bromide under microaerobic conditions. When exposed to 0.15, 0.2, 0.25, 0.5, and 1 mM bromate, S. oneidensis MR-1 reduced bromate by around 100, 75, 64, 48, and 23%, respectively, within 12 h. In vivo evidence from gene deletion mutants and complemented strains of S. oneidensis MR-1 indicates that MtrB, MtrC, CymA, GspD, and DmsA are involved in bromate reduction, but not NapA, FccA, or SYE4. Based on our results as well as previous findings, a proposed molecular mechanism for bromate reduction is presented in this study. Moreover, a genomic survey indicates that 9 of the other 56 reported Shewanella species encode proteins highly homologous to CymA, GspD, and DmsA of S. oneidensis MR-1 by sequence alignment. The results of this study contribute to understanding a pathway for microbial bromate reduction.

SUBMITTER: Wang Y

PROVIDER: S-EPMC9468665 | biostudies-literature | 2022

REPOSITORIES: biostudies-literature

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

Wang Yicheng Y Fan Jiale J Shen Yonglin Y Ye Fan F Feng Zhiying Z Yang Qianning Q Wang Dan D Cai Xunchao X Mao Yanping Y

Frontiers in microbiology 20220830

Microbial bromate reduction plays an important role in remediating bromate-contaminated waters as well as biogeochemical cycling of bromine. However, little is known about the molecular mechanism of microbial bromate reduction so far. Since the model strain Shewanella oneidensis MR-1 is capable of reducing a variety of oxyanions such as iodate, which has a high similarity to bromate, we hypothesize that S. oneidensis MR-1 can reduce bromate. Here, we conducted an experiment to inve ...[more]

PMID: 36110297

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Project description: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.

Project description:In the absence of O(2) and other electron acceptors, the Gram-negative bacterium Shewanella oneidensis MR-1 can use ferric [Fe(III)] (oxy)(hydr)oxide minerals as the terminal electron acceptors for anaerobic respiration. At circumneutral pH and in the absence of strong complexing ligands, Fe(III) oxides are relatively insoluble and thus are external to the bacterial cells. S. oneidensis MR-1 and related strains of metal-reducing Shewanella have evolved machinery (i.e., metal-reducing or Mtr pathway) for transferring electrons from the inner-membrane, through the periplasm and across the outer-membrane to the surface of extracellular Fe(III) oxides. The protein components identified to date for the Mtr pathway include CymA, MtrA, MtrB, MtrC, and OmcA. CymA is an inner-membrane tetraheme c-type cytochrome (c-Cyt) that belongs to the NapC/NrfH family of quinol dehydrogenases. It is proposed that CymA oxidizes the quinol in the inner-membrane and transfers the released electrons to MtrA either directly or indirectly through other periplasmic proteins. A decaheme c-Cyt, MtrA is thought to be embedded in the trans outer-membrane and porin-like protein MtrB. Together, MtrAB deliver the electrons through the outer-membrane to the MtrC and OmcA on the outmost bacterial surface. MtrC and OmcA are the outer-membrane decaheme c-Cyts that are translocated across the outer-membrane by the bacterial type II secretion system. Functioning as terminal reductases, MtrC and OmcA can bind the surface of Fe(III) oxides and transfer electrons directly to these minerals via their solvent-exposed hemes. To increase their reaction rates, MtrC and OmcA can use the flavins secreted by S. oneidensis MR-1 cells as diffusible co-factors for reduction of Fe(III) oxides. Because of their extracellular location and broad redox potentials, MtrC and OmcA can also serve as the terminal reductases for soluble forms of Fe(III). In addition to Fe(III) oxides, Mtr pathway is also involved in reduction of manganese oxides and other metals. Although our understanding of the Mtr pathway is still far from complete, it is the best characterized microbial pathway used for extracellular electron exchange. Characterizations of the Mtr pathway have made significant contributions to the molecular understanding of microbial reduction of Fe(III) oxides.

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

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Bromate reduction by <i>Shewanella oneidensis</i> MR-1 is mediated by dimethylsulfoxide reductase.

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