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

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 r...

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Main Authors: Yicheng Wang, Jiale Fan, Yonglin Shen, Fan Ye, Zhiying Feng, Qianning Yang, Dan Wang, Xunchao Cai, Yanping Mao
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-08-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.955249/full
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author Yicheng Wang
Jiale Fan
Yonglin Shen
Fan Ye
Zhiying Feng
Qianning Yang
Dan Wang
Xunchao Cai
Xunchao Cai
Yanping Mao
author_facet Yicheng Wang
Jiale Fan
Yonglin Shen
Fan Ye
Zhiying Feng
Qianning Yang
Dan Wang
Xunchao Cai
Xunchao Cai
Yanping Mao
author_sort Yicheng Wang
collection DOAJ
description 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.
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spelling doaj.art-727b0b2a30c34b8f9f0758f4531a46e82022-12-22T03:07:46ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-08-011310.3389/fmicb.2022.955249955249Bromate reduction by Shewanella oneidensis MR-1 is mediated by dimethylsulfoxide reductaseYicheng Wang0Jiale Fan1Yonglin Shen2Fan Ye3Zhiying Feng4Qianning Yang5Dan Wang6Xunchao Cai7Xunchao Cai8Yanping Mao9College of Chemistry and Environmental Engineering, Shenzhen University, Shenzhen, ChinaCollege of Chemistry and Environmental Engineering, Shenzhen University, Shenzhen, ChinaCollege of Chemistry and Environmental Engineering, Shenzhen University, Shenzhen, ChinaCollege of Chemistry and Environmental Engineering, Shenzhen University, Shenzhen, ChinaCollege of Chemistry and Environmental Engineering, Shenzhen University, Shenzhen, ChinaCollege of Chemistry and Environmental Engineering, Shenzhen University, Shenzhen, ChinaCollege of Chemistry and Environmental Engineering, Shenzhen University, Shenzhen, ChinaCollege of Chemistry and Environmental Engineering, Shenzhen University, Shenzhen, ChinaDepartment of Gastroenterology and Hepatology, Shenzhen University General Hospital, Shenzhen, ChinaCollege of Chemistry and Environmental Engineering, Shenzhen University, Shenzhen, ChinaMicrobial 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.https://www.frontiersin.org/articles/10.3389/fmicb.2022.955249/fullShewanella oneidensisbromate reductionbromatebromidemolecular mechanismDMSO reductase
spellingShingle Yicheng Wang
Jiale Fan
Yonglin Shen
Fan Ye
Zhiying Feng
Qianning Yang
Dan Wang
Xunchao Cai
Xunchao Cai
Yanping Mao
Bromate reduction by Shewanella oneidensis MR-1 is mediated by dimethylsulfoxide reductase
Frontiers in Microbiology
Shewanella oneidensis
bromate reduction
bromate
bromide
molecular mechanism
DMSO reductase
title Bromate reduction by Shewanella oneidensis MR-1 is mediated by dimethylsulfoxide reductase
title_full Bromate reduction by Shewanella oneidensis MR-1 is mediated by dimethylsulfoxide reductase
title_fullStr Bromate reduction by Shewanella oneidensis MR-1 is mediated by dimethylsulfoxide reductase
title_full_unstemmed Bromate reduction by Shewanella oneidensis MR-1 is mediated by dimethylsulfoxide reductase
title_short Bromate reduction by Shewanella oneidensis MR-1 is mediated by dimethylsulfoxide reductase
title_sort bromate reduction by shewanella oneidensis mr 1 is mediated by dimethylsulfoxide reductase
topic Shewanella oneidensis
bromate reduction
bromate
bromide
molecular mechanism
DMSO reductase
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.955249/full
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