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Multi-omics reveal various potential antimonate reductases from phylogenetically diverse microorganisms
While previous work has demonstrated that antimonate (Sb(V)) can be bio-reduced with methane as the sole electron donor, the microorganisms responsible for Sb(V) reduction remain largely uncharacterized. Inspired by the recently reported Sb(V) reductase belonging to the dimethyl sulfoxide reductase...
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Published in: | Applied microbiology and biotechnology 2019-11, Vol.103 (21-22), p.9119-9129 |
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description | While previous work has demonstrated that antimonate (Sb(V)) can be bio-reduced with methane as the sole electron donor, the microorganisms responsible for Sb(V) reduction remain largely uncharacterized. Inspired by the recently reported Sb(V) reductase belonging to the dimethyl sulfoxide reductase (DMSOR) family, this study was undertaken to use metagenomics and metatranscriptomics to unravel whether any DMSOR family genes in the bioreactor had the potential for Sb(V) reduction. A search through metagenomic-assembled genomes recovered from the microbial community found that some DMSOR family genes, designated
sbrA
(
Sb
(V)
r
eductase gene), were highly transcribed in four phylogenetically disparate assemblies. The putative catalytic subunits were found to be representatives of two distinct phylogenetic clades of reductases that were most closely related to periplasmic nitrate reductases and respiratory arsenate reductases, respectively. Putative operons containing
sbrA
possessed many other components, including genes encoding
c
-type cytochromes, response regulators, and ferredoxins, which together implement Sb(V) reduction. This predicted ability was confirmed by incubating the enrichment culture with
13
C-labeled CH
4
and Sb(V) in serum bottles, where Sb(V) was reduced coincident with the production of
13
C-labeled CO
2
. Overall, these results increase our understanding of how Sb(V) can be bio-reduced in environments. |
doi_str_mv | 10.1007/s00253-019-10111-x |
format | article |
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sbrA
(
Sb
(V)
r
eductase gene), were highly transcribed in four phylogenetically disparate assemblies. The putative catalytic subunits were found to be representatives of two distinct phylogenetic clades of reductases that were most closely related to periplasmic nitrate reductases and respiratory arsenate reductases, respectively. Putative operons containing
sbrA
possessed many other components, including genes encoding
c
-type cytochromes, response regulators, and ferredoxins, which together implement Sb(V) reduction. This predicted ability was confirmed by incubating the enrichment culture with
13
C-labeled CH
4
and Sb(V) in serum bottles, where Sb(V) was reduced coincident with the production of
13
C-labeled CO
2
. Overall, these results increase our understanding of how Sb(V) can be bio-reduced in environments.</description><identifier>ISSN: 0175-7598</identifier><identifier>EISSN: 1432-0614</identifier><identifier>DOI: 10.1007/s00253-019-10111-x</identifier><identifier>PMID: 31501939</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer Berlin Heidelberg</publisher><subject>Analysis ; Antimony ; Antimony - metabolism ; Arsenates ; Bacteria - classification ; Bacteria - enzymology ; Bacteria - genetics ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Biomedical and Life Sciences ; Bioreactors ; Biotechnology ; Carbon dioxide ; Catalysis ; Catalytic subunits ; Cytochromes ; Dimethyl sulfoxide ; Dimethyl sulfoxide reductase ; Environmental Biotechnology ; Enzymes ; Genes ; Genetic aspects ; Genetic transcription ; Genomes ; Genomics ; Identification and classification ; Life Sciences ; Methane ; Microbial Genetics and Genomics ; Microbiology ; Microorganisms ; Multigene Family ; Operon ; Operons ; Oxidoreductases - genetics ; Oxidoreductases - metabolism ; Phylogeny ; Reductases ; Reduction ; Regulators</subject><ispartof>Applied microbiology and biotechnology, 2019-11, Vol.103 (21-22), p.9119-9129</ispartof><rights>Springer-Verlag GmbH Germany, part of Springer Nature 2019</rights><rights>COPYRIGHT 2019 Springer</rights><rights>Applied Microbiology and Biotechnology is a copyright of Springer, (2019). All Rights Reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c513t-f5cf5ad3c7424064c8b30f7282cb49eb0f945c041fbc5c6268217a82bb9193723</citedby><cites>FETCH-LOGICAL-c513t-f5cf5ad3c7424064c8b30f7282cb49eb0f945c041fbc5c6268217a82bb9193723</cites><orcidid>0000-0002-5177-8010</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2287211182/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$H</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2287211182?pq-origsite=primo$$EHTML$$P50$$Gproquest$$H</linktohtml><link.rule.ids>314,780,784,11686,27922,27923,36058,36059,44361,74665</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31501939$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Shi, Ling-Dong</creatorcontrib><creatorcontrib>Wang, Min</creatorcontrib><creatorcontrib>Han, Yu-Lin</creatorcontrib><creatorcontrib>Lai, Chun-Yu</creatorcontrib><creatorcontrib>Shapleigh, James P.</creatorcontrib><creatorcontrib>Zhao, He-Ping</creatorcontrib><title>Multi-omics reveal various potential antimonate reductases from phylogenetically diverse microorganisms</title><title>Applied microbiology and biotechnology</title><addtitle>Appl Microbiol Biotechnol</addtitle><addtitle>Appl Microbiol Biotechnol</addtitle><description>While previous work has demonstrated that antimonate (Sb(V)) can be bio-reduced with methane as the sole electron donor, the microorganisms responsible for Sb(V) reduction remain largely uncharacterized. Inspired by the recently reported Sb(V) reductase belonging to the dimethyl sulfoxide reductase (DMSOR) family, this study was undertaken to use metagenomics and metatranscriptomics to unravel whether any DMSOR family genes in the bioreactor had the potential for Sb(V) reduction. A search through metagenomic-assembled genomes recovered from the microbial community found that some DMSOR family genes, designated
sbrA
(
Sb
(V)
r
eductase gene), were highly transcribed in four phylogenetically disparate assemblies. The putative catalytic subunits were found to be representatives of two distinct phylogenetic clades of reductases that were most closely related to periplasmic nitrate reductases and respiratory arsenate reductases, respectively. Putative operons containing
sbrA
possessed many other components, including genes encoding
c
-type cytochromes, response regulators, and ferredoxins, which together implement Sb(V) reduction. This predicted ability was confirmed by incubating the enrichment culture with
13
C-labeled CH
4
and Sb(V) in serum bottles, where Sb(V) was reduced coincident with the production of
13
C-labeled CO
2
. Overall, these results increase our understanding of how Sb(V) can be bio-reduced in environments.</description><subject>Analysis</subject><subject>Antimony</subject><subject>Antimony - metabolism</subject><subject>Arsenates</subject><subject>Bacteria - classification</subject><subject>Bacteria - enzymology</subject><subject>Bacteria - genetics</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Biomedical and Life Sciences</subject><subject>Bioreactors</subject><subject>Biotechnology</subject><subject>Carbon dioxide</subject><subject>Catalysis</subject><subject>Catalytic subunits</subject><subject>Cytochromes</subject><subject>Dimethyl sulfoxide</subject><subject>Dimethyl sulfoxide reductase</subject><subject>Environmental Biotechnology</subject><subject>Enzymes</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genetic transcription</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Identification and classification</subject><subject>Life Sciences</subject><subject>Methane</subject><subject>Microbial Genetics and Genomics</subject><subject>Microbiology</subject><subject>Microorganisms</subject><subject>Multigene Family</subject><subject>Operon</subject><subject>Operons</subject><subject>Oxidoreductases - genetics</subject><subject>Oxidoreductases - metabolism</subject><subject>Phylogeny</subject><subject>Reductases</subject><subject>Reduction</subject><subject>Regulators</subject><issn>0175-7598</issn><issn>1432-0614</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>M0C</sourceid><recordid>eNp9kluLFDEQhYMo7rj6B3yQBl_0oddcu9OPy-JlYUXw8hzSmUqbpbszJulh5t9b46wuIyJ5KEi-U-ScKkKeM3rBKG3fZEq5EjVlXc0oY6zePSArJgWvacPkQ7KirFV1qzp9Rp7kfEsp47ppHpMzwRSqRLciw8dlLKGOU3C5SrAFO1Zbm0JccrWJBeYS8MZimeJsCyCzXlyxGXLlU5yqzff9GAeYoQRnx3FfrcMWUoYKO6YY02DnkKf8lDzydszw7K6ek2_v3n69-lDffHp_fXV5UzvFRKm9cl7ZtXCt5JI20uleUN9yzV0vO-ip76RyVDLfO-Ua3mjOWqt533fop-XinLw69t2k-GOBXMwUsoNxtDOgJ8O51pRiJALRl3-ht3FJM_7uQLUcE9X8nhrsCCbMPpZk3aGpuWyoapTUQiJ18Q8KzxowhziDD3h_Inh9IkCmwK4MdsnZXH_5fMryI4uB5pzAm00Kk017w6g5bII5boLBmZpfm2B2KHpx527pJ1j_kfwePQLiCGR8mgdI9_b_0_YnJTe96Q</recordid><startdate>20191101</startdate><enddate>20191101</enddate><creator>Shi, Ling-Dong</creator><creator>Wang, Min</creator><creator>Han, Yu-Lin</creator><creator>Lai, Chun-Yu</creator><creator>Shapleigh, James P.</creator><creator>Zhao, He-Ping</creator><general>Springer Berlin Heidelberg</general><general>Springer</general><general>Springer Nature B.V</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>ISR</scope><scope>3V.</scope><scope>7QL</scope><scope>7T7</scope><scope>7WY</scope><scope>7WZ</scope><scope>7X7</scope><scope>7XB</scope><scope>87Z</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8FL</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BEZIV</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FRNLG</scope><scope>FYUFA</scope><scope>F~G</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K60</scope><scope>K6~</scope><scope>K9.</scope><scope>L.-</scope><scope>LK8</scope><scope>M0C</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PQBIZ</scope><scope>PQBZA</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-5177-8010</orcidid></search><sort><creationdate>20191101</creationdate><title>Multi-omics reveal various potential antimonate reductases from phylogenetically diverse microorganisms</title><author>Shi, Ling-Dong ; Wang, Min ; Han, Yu-Lin ; Lai, Chun-Yu ; Shapleigh, James P. ; Zhao, He-Ping</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c513t-f5cf5ad3c7424064c8b30f7282cb49eb0f945c041fbc5c6268217a82bb9193723</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Analysis</topic><topic>Antimony</topic><topic>Antimony - metabolism</topic><topic>Arsenates</topic><topic>Bacteria - classification</topic><topic>Bacteria - enzymology</topic><topic>Bacteria - genetics</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - metabolism</topic><topic>Biomedical and Life Sciences</topic><topic>Bioreactors</topic><topic>Biotechnology</topic><topic>Carbon dioxide</topic><topic>Catalysis</topic><topic>Catalytic subunits</topic><topic>Cytochromes</topic><topic>Dimethyl sulfoxide</topic><topic>Dimethyl sulfoxide reductase</topic><topic>Environmental Biotechnology</topic><topic>Enzymes</topic><topic>Genes</topic><topic>Genetic aspects</topic><topic>Genetic transcription</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Identification and classification</topic><topic>Life Sciences</topic><topic>Methane</topic><topic>Microbial Genetics and Genomics</topic><topic>Microbiology</topic><topic>Microorganisms</topic><topic>Multigene Family</topic><topic>Operon</topic><topic>Operons</topic><topic>Oxidoreductases - genetics</topic><topic>Oxidoreductases - metabolism</topic><topic>Phylogeny</topic><topic>Reductases</topic><topic>Reduction</topic><topic>Regulators</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Shi, Ling-Dong</creatorcontrib><creatorcontrib>Wang, Min</creatorcontrib><creatorcontrib>Han, Yu-Lin</creatorcontrib><creatorcontrib>Lai, Chun-Yu</creatorcontrib><creatorcontrib>Shapleigh, James P.</creatorcontrib><creatorcontrib>Zhao, He-Ping</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>ABI/INFORM Collection</collection><collection>ABI/INFORM Global (PDF only)</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>ABI/INFORM Global (Alumni Edition)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ABI/INFORM Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Business Premium Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Business Premium Collection (Alumni)</collection><collection>Health Research Premium Collection</collection><collection>ABI/INFORM Global (Corporate)</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Business Collection (Alumni Edition)</collection><collection>ProQuest Business Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ABI/INFORM Professional Advanced</collection><collection>ProQuest Biological Science Collection</collection><collection>ABI/INFORM Global</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Science Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Business</collection><collection>ProQuest One Business (Alumni)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><jtitle>Applied microbiology and biotechnology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Shi, Ling-Dong</au><au>Wang, Min</au><au>Han, Yu-Lin</au><au>Lai, Chun-Yu</au><au>Shapleigh, James P.</au><au>Zhao, He-Ping</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Multi-omics reveal various potential antimonate reductases from phylogenetically diverse microorganisms</atitle><jtitle>Applied microbiology and biotechnology</jtitle><stitle>Appl Microbiol Biotechnol</stitle><addtitle>Appl Microbiol Biotechnol</addtitle><date>2019-11-01</date><risdate>2019</risdate><volume>103</volume><issue>21-22</issue><spage>9119</spage><epage>9129</epage><pages>9119-9129</pages><issn>0175-7598</issn><eissn>1432-0614</eissn><abstract>While previous work has demonstrated that antimonate (Sb(V)) can be bio-reduced with methane as the sole electron donor, the microorganisms responsible for Sb(V) reduction remain largely uncharacterized. Inspired by the recently reported Sb(V) reductase belonging to the dimethyl sulfoxide reductase (DMSOR) family, this study was undertaken to use metagenomics and metatranscriptomics to unravel whether any DMSOR family genes in the bioreactor had the potential for Sb(V) reduction. A search through metagenomic-assembled genomes recovered from the microbial community found that some DMSOR family genes, designated
sbrA
(
Sb
(V)
r
eductase gene), were highly transcribed in four phylogenetically disparate assemblies. The putative catalytic subunits were found to be representatives of two distinct phylogenetic clades of reductases that were most closely related to periplasmic nitrate reductases and respiratory arsenate reductases, respectively. Putative operons containing
sbrA
possessed many other components, including genes encoding
c
-type cytochromes, response regulators, and ferredoxins, which together implement Sb(V) reduction. This predicted ability was confirmed by incubating the enrichment culture with
13
C-labeled CH
4
and Sb(V) in serum bottles, where Sb(V) was reduced coincident with the production of
13
C-labeled CO
2
. Overall, these results increase our understanding of how Sb(V) can be bio-reduced in environments.</abstract><cop>Berlin/Heidelberg</cop><pub>Springer Berlin Heidelberg</pub><pmid>31501939</pmid><doi>10.1007/s00253-019-10111-x</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0002-5177-8010</orcidid></addata></record> |
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source | ABI/INFORM Global; Springer Nature:Jisc Collections:Springer Nature Read and Publish 2023-2025: Springer Reading List |
subjects | Analysis Antimony Antimony - metabolism Arsenates Bacteria - classification Bacteria - enzymology Bacteria - genetics Bacterial Proteins - genetics Bacterial Proteins - metabolism Biomedical and Life Sciences Bioreactors Biotechnology Carbon dioxide Catalysis Catalytic subunits Cytochromes Dimethyl sulfoxide Dimethyl sulfoxide reductase Environmental Biotechnology Enzymes Genes Genetic aspects Genetic transcription Genomes Genomics Identification and classification Life Sciences Methane Microbial Genetics and Genomics Microbiology Microorganisms Multigene Family Operon Operons Oxidoreductases - genetics Oxidoreductases - metabolism Phylogeny Reductases Reduction Regulators |
title | Multi-omics reveal various potential antimonate reductases from phylogenetically diverse microorganisms |
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