Loading…

NapB in excess inhibits growth of Shewanella oneidensis by dissipating electrons of the quinol pool

Shewanella , a group of ubiquitous bacteria renowned for respiratory versatility, thrive in environments where various electron acceptors (EAs) of different chemical and physiological characteristics coexist. Despite being extensively studied, we still know surprisingly little about strategies by wh...

Full description

Saved in:
Bibliographic Details
Published in:Scientific reports 2016-11, Vol.6 (1), p.37456, Article 37456
Main Authors: Jin, Miao, Zhang, Qianyun, Sun, Yijuan, Gao, Haichun
Format: Article
Language:English
Subjects:
Citations: Items that this one cites
Items that cite this one
Online Access:Get full text
Tags: Add Tag
No Tags, Be the first to tag this record!
cited_by cdi_FETCH-LOGICAL-c438t-34cd3d59f2a7419bd2d20e6a7f12aa605d3ae1ae2e1fb3419029a3a495da788b3
cites cdi_FETCH-LOGICAL-c438t-34cd3d59f2a7419bd2d20e6a7f12aa605d3ae1ae2e1fb3419029a3a495da788b3
container_end_page
container_issue 1
container_start_page 37456
container_title Scientific reports
container_volume 6
creator Jin, Miao
Zhang, Qianyun
Sun, Yijuan
Gao, Haichun
description Shewanella , a group of ubiquitous bacteria renowned for respiratory versatility, thrive in environments where various electron acceptors (EAs) of different chemical and physiological characteristics coexist. Despite being extensively studied, we still know surprisingly little about strategies by which multiple EAs and their interaction define ecophysiology of these bacteria. Previously, we showed that nitrite inhibits growth of the genus representative Shewanella oneidensis on fumarate and presumably some other CymA (quinol dehydrogenase)-dependent EAs by reducing cAMP production, which in turn leads to lowered expression of nitrite and fumarate reductases. In this study, we demonstrated that inhibition of fumarate growth by nitrite is also attributable to overproduction of NapB, the cytochrome c subunit of nitrate reductase. Further investigations revealed that excessive NapB per se inhibits growth on all EAs tested, including oxygen. When overproduced, NapB acts as an electron shuttle to dissipate electrons of the quinol pool, likely to extracellullar EAs, because the Mtr system, the major electron transport pathway for extracellular electron transport, is implicated. The study not only sheds light on mechanisms by which certain EAs, especially toxic ones, impact the bacterial ecophysiology, but also provides new insights into how electron shuttle c -type cytochromes regulate multi-branched respiratory networks.
doi_str_mv 10.1038/srep37456
format article
fullrecord <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_5114592</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>1899362830</sourcerecordid><originalsourceid>FETCH-LOGICAL-c438t-34cd3d59f2a7419bd2d20e6a7f12aa605d3ae1ae2e1fb3419029a3a495da788b3</originalsourceid><addsrcrecordid>eNplkU1LxDAQhoMoKurBPyABTwqr-Wi27UVQ8QtED-o5TJvpNlKTmnTV_fdGdl1WnEsG5pl3XvISss_ZCWeyOI0Be5lnarxGtgXL1EhIIdZX-i2yF-MrS6VEmfFyk2yJvFC5YGKb1A_QX1DrKH7VGGPqWlvZIdJJ8J9DS31Dn1r8BIddB9Q7tAZdtJFWM2psjLaHwboJxQ7rIXgXfzaGFun71Drf0d77bpdsNNBF3Fu8O-Tl-ur58nZ0_3hzd3l-P6ozWQwjmdVGGlU2AvJkszLCCIZjyBsuAMZMGQnIAQXyppKJYKIECVmpDORFUckdcjbX7afVG5oa3RCg032wbxBm2oPVfyfOtnriP7TiPFOlSAKHC4Hg36cYB_3qp8Elz5oXZSnHopAsUUdzqg4-pt9vlhc40z-R6GUkiT1YtbQkfwNIwPEciGnkJhhWTv5T-wbdrZeV</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1899362830</pqid></control><display><type>article</type><title>NapB in excess inhibits growth of Shewanella oneidensis by dissipating electrons of the quinol pool</title><source>PubMed Central Free</source><source>ProQuest - Publicly Available Content Database</source><source>Free Full-Text Journals in Chemistry</source><source>Springer Nature - nature.com Journals - Fully Open Access</source><creator>Jin, Miao ; Zhang, Qianyun ; Sun, Yijuan ; Gao, Haichun</creator><creatorcontrib>Jin, Miao ; Zhang, Qianyun ; Sun, Yijuan ; Gao, Haichun</creatorcontrib><description>Shewanella , a group of ubiquitous bacteria renowned for respiratory versatility, thrive in environments where various electron acceptors (EAs) of different chemical and physiological characteristics coexist. Despite being extensively studied, we still know surprisingly little about strategies by which multiple EAs and their interaction define ecophysiology of these bacteria. Previously, we showed that nitrite inhibits growth of the genus representative Shewanella oneidensis on fumarate and presumably some other CymA (quinol dehydrogenase)-dependent EAs by reducing cAMP production, which in turn leads to lowered expression of nitrite and fumarate reductases. In this study, we demonstrated that inhibition of fumarate growth by nitrite is also attributable to overproduction of NapB, the cytochrome c subunit of nitrate reductase. Further investigations revealed that excessive NapB per se inhibits growth on all EAs tested, including oxygen. When overproduced, NapB acts as an electron shuttle to dissipate electrons of the quinol pool, likely to extracellullar EAs, because the Mtr system, the major electron transport pathway for extracellular electron transport, is implicated. The study not only sheds light on mechanisms by which certain EAs, especially toxic ones, impact the bacterial ecophysiology, but also provides new insights into how electron shuttle c -type cytochromes regulate multi-branched respiratory networks.</description><identifier>ISSN: 2045-2322</identifier><identifier>EISSN: 2045-2322</identifier><identifier>DOI: 10.1038/srep37456</identifier><identifier>PMID: 27857202</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>38/44 ; 38/70 ; 631/326/1320 ; 631/326/47/4112 ; Antimicrobial agents ; Bacteria ; Cyclic AMP ; Cytochrome ; Cytochrome c ; E coli ; Ecophysiology ; Electron transport ; Enzymes ; Gene expression ; Genetic engineering ; Humanities and Social Sciences ; Hydroquinone ; multidisciplinary ; Mutagenesis ; Mutation ; Nitrate reductase ; Nitrates ; Nitrites ; Nitrogen dioxide ; Physiology ; Plasmids ; Respiration ; Science</subject><ispartof>Scientific reports, 2016-11, Vol.6 (1), p.37456, Article 37456</ispartof><rights>The Author(s) 2016</rights><rights>Copyright Nature Publishing Group Nov 2016</rights><rights>Copyright © 2016, The Author(s) 2016 The Author(s)</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c438t-34cd3d59f2a7419bd2d20e6a7f12aa605d3ae1ae2e1fb3419029a3a495da788b3</citedby><cites>FETCH-LOGICAL-c438t-34cd3d59f2a7419bd2d20e6a7f12aa605d3ae1ae2e1fb3419029a3a495da788b3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/1899362830/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1899362830?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27857202$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Jin, Miao</creatorcontrib><creatorcontrib>Zhang, Qianyun</creatorcontrib><creatorcontrib>Sun, Yijuan</creatorcontrib><creatorcontrib>Gao, Haichun</creatorcontrib><title>NapB in excess inhibits growth of Shewanella oneidensis by dissipating electrons of the quinol pool</title><title>Scientific reports</title><addtitle>Sci Rep</addtitle><addtitle>Sci Rep</addtitle><description>Shewanella , a group of ubiquitous bacteria renowned for respiratory versatility, thrive in environments where various electron acceptors (EAs) of different chemical and physiological characteristics coexist. Despite being extensively studied, we still know surprisingly little about strategies by which multiple EAs and their interaction define ecophysiology of these bacteria. Previously, we showed that nitrite inhibits growth of the genus representative Shewanella oneidensis on fumarate and presumably some other CymA (quinol dehydrogenase)-dependent EAs by reducing cAMP production, which in turn leads to lowered expression of nitrite and fumarate reductases. In this study, we demonstrated that inhibition of fumarate growth by nitrite is also attributable to overproduction of NapB, the cytochrome c subunit of nitrate reductase. Further investigations revealed that excessive NapB per se inhibits growth on all EAs tested, including oxygen. When overproduced, NapB acts as an electron shuttle to dissipate electrons of the quinol pool, likely to extracellullar EAs, because the Mtr system, the major electron transport pathway for extracellular electron transport, is implicated. The study not only sheds light on mechanisms by which certain EAs, especially toxic ones, impact the bacterial ecophysiology, but also provides new insights into how electron shuttle c -type cytochromes regulate multi-branched respiratory networks.</description><subject>38/44</subject><subject>38/70</subject><subject>631/326/1320</subject><subject>631/326/47/4112</subject><subject>Antimicrobial agents</subject><subject>Bacteria</subject><subject>Cyclic AMP</subject><subject>Cytochrome</subject><subject>Cytochrome c</subject><subject>E coli</subject><subject>Ecophysiology</subject><subject>Electron transport</subject><subject>Enzymes</subject><subject>Gene expression</subject><subject>Genetic engineering</subject><subject>Humanities and Social Sciences</subject><subject>Hydroquinone</subject><subject>multidisciplinary</subject><subject>Mutagenesis</subject><subject>Mutation</subject><subject>Nitrate reductase</subject><subject>Nitrates</subject><subject>Nitrites</subject><subject>Nitrogen dioxide</subject><subject>Physiology</subject><subject>Plasmids</subject><subject>Respiration</subject><subject>Science</subject><issn>2045-2322</issn><issn>2045-2322</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><recordid>eNplkU1LxDAQhoMoKurBPyABTwqr-Wi27UVQ8QtED-o5TJvpNlKTmnTV_fdGdl1WnEsG5pl3XvISss_ZCWeyOI0Be5lnarxGtgXL1EhIIdZX-i2yF-MrS6VEmfFyk2yJvFC5YGKb1A_QX1DrKH7VGGPqWlvZIdJJ8J9DS31Dn1r8BIddB9Q7tAZdtJFWM2psjLaHwboJxQ7rIXgXfzaGFun71Drf0d77bpdsNNBF3Fu8O-Tl-ur58nZ0_3hzd3l-P6ozWQwjmdVGGlU2AvJkszLCCIZjyBsuAMZMGQnIAQXyppKJYKIECVmpDORFUckdcjbX7afVG5oa3RCg032wbxBm2oPVfyfOtnriP7TiPFOlSAKHC4Hg36cYB_3qp8Elz5oXZSnHopAsUUdzqg4-pt9vlhc40z-R6GUkiT1YtbQkfwNIwPEciGnkJhhWTv5T-wbdrZeV</recordid><startdate>20161118</startdate><enddate>20161118</enddate><creator>Jin, Miao</creator><creator>Zhang, Qianyun</creator><creator>Sun, Yijuan</creator><creator>Gao, Haichun</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><scope>C6C</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>5PM</scope></search><sort><creationdate>20161118</creationdate><title>NapB in excess inhibits growth of Shewanella oneidensis by dissipating electrons of the quinol pool</title><author>Jin, Miao ; Zhang, Qianyun ; Sun, Yijuan ; Gao, Haichun</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c438t-34cd3d59f2a7419bd2d20e6a7f12aa605d3ae1ae2e1fb3419029a3a495da788b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>38/44</topic><topic>38/70</topic><topic>631/326/1320</topic><topic>631/326/47/4112</topic><topic>Antimicrobial agents</topic><topic>Bacteria</topic><topic>Cyclic AMP</topic><topic>Cytochrome</topic><topic>Cytochrome c</topic><topic>E coli</topic><topic>Ecophysiology</topic><topic>Electron transport</topic><topic>Enzymes</topic><topic>Gene expression</topic><topic>Genetic engineering</topic><topic>Humanities and Social Sciences</topic><topic>Hydroquinone</topic><topic>multidisciplinary</topic><topic>Mutagenesis</topic><topic>Mutation</topic><topic>Nitrate reductase</topic><topic>Nitrates</topic><topic>Nitrites</topic><topic>Nitrogen dioxide</topic><topic>Physiology</topic><topic>Plasmids</topic><topic>Respiration</topic><topic>Science</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Jin, Miao</creatorcontrib><creatorcontrib>Zhang, Qianyun</creatorcontrib><creatorcontrib>Sun, Yijuan</creatorcontrib><creatorcontrib>Gao, Haichun</creatorcontrib><collection>SpringerOpen</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Health &amp; Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</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>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>AUTh Library subscriptions: ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Science Database</collection><collection>ProQuest Biological Science Journals</collection><collection>ProQuest - Publicly Available Content Database</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>PubMed Central (Full Participant titles)</collection><jtitle>Scientific reports</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Jin, Miao</au><au>Zhang, Qianyun</au><au>Sun, Yijuan</au><au>Gao, Haichun</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>NapB in excess inhibits growth of Shewanella oneidensis by dissipating electrons of the quinol pool</atitle><jtitle>Scientific reports</jtitle><stitle>Sci Rep</stitle><addtitle>Sci Rep</addtitle><date>2016-11-18</date><risdate>2016</risdate><volume>6</volume><issue>1</issue><spage>37456</spage><pages>37456-</pages><artnum>37456</artnum><issn>2045-2322</issn><eissn>2045-2322</eissn><abstract>Shewanella , a group of ubiquitous bacteria renowned for respiratory versatility, thrive in environments where various electron acceptors (EAs) of different chemical and physiological characteristics coexist. Despite being extensively studied, we still know surprisingly little about strategies by which multiple EAs and their interaction define ecophysiology of these bacteria. Previously, we showed that nitrite inhibits growth of the genus representative Shewanella oneidensis on fumarate and presumably some other CymA (quinol dehydrogenase)-dependent EAs by reducing cAMP production, which in turn leads to lowered expression of nitrite and fumarate reductases. In this study, we demonstrated that inhibition of fumarate growth by nitrite is also attributable to overproduction of NapB, the cytochrome c subunit of nitrate reductase. Further investigations revealed that excessive NapB per se inhibits growth on all EAs tested, including oxygen. When overproduced, NapB acts as an electron shuttle to dissipate electrons of the quinol pool, likely to extracellullar EAs, because the Mtr system, the major electron transport pathway for extracellular electron transport, is implicated. The study not only sheds light on mechanisms by which certain EAs, especially toxic ones, impact the bacterial ecophysiology, but also provides new insights into how electron shuttle c -type cytochromes regulate multi-branched respiratory networks.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>27857202</pmid><doi>10.1038/srep37456</doi><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 2045-2322
ispartof Scientific reports, 2016-11, Vol.6 (1), p.37456, Article 37456
issn 2045-2322
2045-2322
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_5114592
source PubMed Central Free; ProQuest - Publicly Available Content Database; Free Full-Text Journals in Chemistry; Springer Nature - nature.com Journals - Fully Open Access
subjects 38/44
38/70
631/326/1320
631/326/47/4112
Antimicrobial agents
Bacteria
Cyclic AMP
Cytochrome
Cytochrome c
E coli
Ecophysiology
Electron transport
Enzymes
Gene expression
Genetic engineering
Humanities and Social Sciences
Hydroquinone
multidisciplinary
Mutagenesis
Mutation
Nitrate reductase
Nitrates
Nitrites
Nitrogen dioxide
Physiology
Plasmids
Respiration
Science
title NapB in excess inhibits growth of Shewanella oneidensis by dissipating electrons of the quinol pool
url http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-02T17%3A07%3A59IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=NapB%20in%20excess%20inhibits%20growth%20of%20Shewanella%20oneidensis%20by%20dissipating%20electrons%20of%20the%20quinol%20pool&rft.jtitle=Scientific%20reports&rft.au=Jin,%20Miao&rft.date=2016-11-18&rft.volume=6&rft.issue=1&rft.spage=37456&rft.pages=37456-&rft.artnum=37456&rft.issn=2045-2322&rft.eissn=2045-2322&rft_id=info:doi/10.1038/srep37456&rft_dat=%3Cproquest_pubme%3E1899362830%3C/proquest_pubme%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c438t-34cd3d59f2a7419bd2d20e6a7f12aa605d3ae1ae2e1fb3419029a3a495da788b3%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=1899362830&rft_id=info:pmid/27857202&rfr_iscdi=true