SecDF as Part of the Sec-Translocase Facilitates Efficient Secretion of Bacillus cereus Toxins and Cell Wall-Associated Proteins
Identifieur interne : 000353 ( Pmc/Curation ); précédent : 000352; suivant : 000354SecDF as Part of the Sec-Translocase Facilitates Efficient Secretion of Bacillus cereus Toxins and Cell Wall-Associated Proteins
Auteurs : Aniko Vörös [Norvège] ; Roger Simm [Norvège] ; Leyla Slamti [France] ; Matthew J. Mckay [Australie] ; Ida K. Hegna [Norvège] ; Christina Nielsen-Leroux [France] ; Karl A. Hassan [Australie] ; Ian T. Paulsen [Australie] ; Didier Lereclus [France] ; Ole Andreas Kstad [Norvège] ; Mark P. Molloy [Australie] ; Anne-Brit Kolst [Norvège]Source :
- PLoS ONE [ 1932-6203 ] ; 2014.
Abstract
The aim of this study was to explore the role of SecDF in protein secretion in
Url:
DOI: 10.1371/journal.pone.0103326
PubMed: 25083861
PubMed Central: 4118872
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Toxins and Cell Wall-Associated Proteins</title>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">SecDF as Part of the Sec-Translocase Facilitates Efficient Secretion of <italic>Bacillus cereus</italic>
Toxins and Cell Wall-Associated Proteins</title>
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<front><div type="abstract" xml:lang="en"><p>The aim of this study was to explore the role of SecDF in protein secretion in <italic>Bacillus cereus</italic>
ATCC 14579 by in-depth characterization of a markerless <italic>secDF</italic>
knock out mutant. Deletion of <italic>secDF</italic>
resulted in pleiotropic effects characterized by a moderately slower growth rate, aberrant cell morphology, enhanced susceptibility to xenobiotics, reduced virulence and motility. Most toxins, including food poisoning-associated enterotoxins Nhe, Hbl, and cytotoxin K, as well as phospholipase C were less abundant in the secretome of the Δ<italic>secDF</italic>
mutant as determined by label-free mass spectrometry. Global transcriptome studies revealed profound transcriptional changes upon deletion of <italic>secDF</italic>
indicating cell envelope stress. Interestingly, the addition of glucose enhanced the described phenotypes. This study shows that SecDF is an important part of the Sec-translocase mediating efficient secretion of virulence factors in the Gram-positive opportunistic pathogen <italic>B. cereus</italic>
, and further supports the notion that <italic>B. cereus</italic>
enterotoxins are secreted by the Sec-system.</p>
</div>
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</TEI>
<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id>
<journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">plosone</journal-id>
<journal-title-group><journal-title>PLoS ONE</journal-title>
</journal-title-group>
<issn pub-type="epub">1932-6203</issn>
<publisher><publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">25083861</article-id>
<article-id pub-id-type="pmc">4118872</article-id>
<article-id pub-id-type="publisher-id">PONE-D-14-14114</article-id>
<article-id pub-id-type="doi">10.1371/journal.pone.0103326</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
<subj-group subj-group-type="Discipline-v2"><subject>Medicine and Health Sciences</subject>
<subj-group><subject>Pathology and Laboratory Medicine</subject>
<subj-group><subject>Pathogens</subject>
<subj-group><subject>Virulence Factors</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v2"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Biochemistry</subject>
<subj-group><subject>Proteomics</subject>
</subj-group>
</subj-group>
<subj-group><subject>Cell Biology</subject>
<subj-group><subject>Cellular Structures and Organelles</subject>
<subj-group><subject>Flagella</subject>
<subj-group><subject>Bacterial Flagella</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group><subject>Computational Biology</subject>
<subj-group><subject>Genome Analysis</subject>
<subj-group><subject>Transcriptome Analysis</subject>
<subj-group><subject>Genome Expression Analysis</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group><subject>Genetics</subject>
<subj-group><subject>Genomics</subject>
<subj-group><subject>Microbial Genomics</subject>
<subj-group><subject>Bacterial Genomics</subject>
<subj-group><subject>Bacterial Genomes</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group><subject>Gene Expression</subject>
</subj-group>
</subj-group>
<subj-group><subject>Microbiology</subject>
<subj-group><subject>Bacteriology</subject>
<subj-group><subject>Bacterial Physiology</subject>
<subj-group><subject>Secretion Systems</subject>
</subj-group>
</subj-group>
<subj-group><subject>Gram Positive Bacteria</subject>
</subj-group>
</subj-group>
<subj-group><subject>Medical Microbiology</subject>
<subj-group><subject>Microbial Pathogens</subject>
<subj-group><subject>Bacterial Pathogens</subject>
<subj-group><subject>Bacillus</subject>
<subj-group><subject>Bacillus Cereus</subject>
<subject>Bacillus Subtilis</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group><subject>Microbial Control</subject>
<subj-group><subject>Antimicrobials</subject>
</subj-group>
</subj-group>
<subj-group><subject>Microbial Physiology</subject>
</subj-group>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>SecDF as Part of the Sec-Translocase Facilitates Efficient Secretion of <italic>Bacillus cereus</italic>
Toxins and Cell Wall-Associated Proteins</article-title>
<alt-title alt-title-type="running-head">SecDF Facilitates Efficient Toxin Secretion</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Vörös</surname>
<given-names>Aniko</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Simm</surname>
<given-names>Roger</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn1"><sup>¤</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Slamti</surname>
<given-names>Leyla</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>McKay</surname>
<given-names>Matthew J.</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hegna</surname>
<given-names>Ida K.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Nielsen-LeRoux</surname>
<given-names>Christina</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hassan</surname>
<given-names>Karl A.</given-names>
</name>
<xref ref-type="aff" rid="aff5"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Paulsen</surname>
<given-names>Ian T.</given-names>
</name>
<xref ref-type="aff" rid="aff5"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lereclus</surname>
<given-names>Didier</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
<xref ref-type="aff" rid="aff4"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Økstad</surname>
<given-names>Ole Andreas</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Molloy</surname>
<given-names>Mark P.</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kolstø</surname>
<given-names>Anne-Brit</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>*</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>1</label>
<addr-line>Laboratory for Microbial Dynamics (LaMDa), Department of Pharmaceutical Biosciences, School of Pharmacy, University of Oslo, Oslo, Norway</addr-line>
</aff>
<aff id="aff2"><label>2</label>
<addr-line>Australian Proteome Analysis Facility (APAF), Macquarie University, Sydney, Australia</addr-line>
</aff>
<aff id="aff3"><label>3</label>
<addr-line>INRA, UMR1319 Micalis, Domaine de La Minière, Guyancourt, France</addr-line>
</aff>
<aff id="aff4"><label>4</label>
<addr-line>AgroParistech, UMR Micalis, Jouy-en-Josas, France</addr-line>
</aff>
<aff id="aff5"><label>5</label>
<addr-line>Department of Chemistry and Biomolecular Sciences, Macquarie University, Sydney, Australia</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Freitag</surname>
<given-names>Nancy E.</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1"><addr-line>University of Illinois at Chicago College of Medicine, United States of America</addr-line>
</aff>
<author-notes><corresp id="cor1">* E-mail: <email>a.b.kolsto@farmasi.uio.no</email>
</corresp>
<fn fn-type="conflict"><p><bold>Competing Interests: </bold>
The authors have declared no competing interests exist.</p>
</fn>
<fn fn-type="con"><p>Conceived and designed the experiments: AV RS ABK. Performed the experiments: AV RS LS IH CNL MJM KH. Analyzed the data: AV RS KH ITP DL OAØ MPM ABK. Contributed reagents/materials/analysis tools: KH MPM CNL DL ITP ABK. Contributed to the writing of the manuscript: AV RS OAØ ABK. Revising the article for important intellectual content: AV LS IKH CNL KH ITP DL MPM ABK. Final approval: AV RS LS MJM IH CNL KH ITP DL OAØ MPM ABK.</p>
</fn>
<fn id="fn1" fn-type="current-aff"><label>¤</label>
<p>Current address: Department of Biochemistry, Institute for Cancer Research, Norwegian Radium Hospital, Oslo, Norway and Centre for Cancer Biomedicine, Faculty of Medicine, University of Oslo, Oslo, Norway</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><year>2014</year>
</pub-date>
<pub-date pub-type="epub"><day>1</day>
<month>8</month>
<year>2014</year>
</pub-date>
<volume>9</volume>
<issue>8</issue>
<elocation-id>e103326</elocation-id>
<history><date date-type="received"><day>29</day>
<month>3</month>
<year>2014</year>
</date>
<date date-type="accepted"><day>26</day>
<month>6</month>
<year>2014</year>
</date>
</history>
<permissions><copyright-year>2014</copyright-year>
<copyright-holder>Vörös et al</copyright-holder>
<license><license-p>This is an open-access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>
, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p>
</license>
</permissions>
<abstract><p>The aim of this study was to explore the role of SecDF in protein secretion in <italic>Bacillus cereus</italic>
ATCC 14579 by in-depth characterization of a markerless <italic>secDF</italic>
knock out mutant. Deletion of <italic>secDF</italic>
resulted in pleiotropic effects characterized by a moderately slower growth rate, aberrant cell morphology, enhanced susceptibility to xenobiotics, reduced virulence and motility. Most toxins, including food poisoning-associated enterotoxins Nhe, Hbl, and cytotoxin K, as well as phospholipase C were less abundant in the secretome of the Δ<italic>secDF</italic>
mutant as determined by label-free mass spectrometry. Global transcriptome studies revealed profound transcriptional changes upon deletion of <italic>secDF</italic>
indicating cell envelope stress. Interestingly, the addition of glucose enhanced the described phenotypes. This study shows that SecDF is an important part of the Sec-translocase mediating efficient secretion of virulence factors in the Gram-positive opportunistic pathogen <italic>B. cereus</italic>
, and further supports the notion that <italic>B. cereus</italic>
enterotoxins are secreted by the Sec-system.</p>
</abstract>
<funding-group><funding-statement>The work was funded by The Norwegian Research Council (FUGE II) and EU grant IRSES-GA-2009_247634. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement>
</funding-group>
<counts><page-count count="17"></page-count>
</counts>
<custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name>
<meta-value>The authors confirm that all data underlying the findings are fully available without restriction. All detailed procedures and raw data relating to the microarray analyses were deposited according to MIAME guidelines in the Arrayexpress database accession number E-MTAB-1759. <ext-link ext-link-type="uri" xlink:href="https://www.ebi.ac.uk/arrayexpress/arrays/browse.html?directsub=on">https://www.ebi.ac.uk/arrayexpress/arrays/browse.html?directsub=on</ext-link>
.</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
<notes><title>Data Availability</title>
<p>The authors confirm that all data underlying the findings are fully available without restriction. All detailed procedures and raw data relating to the microarray analyses were deposited according to MIAME guidelines in the Arrayexpress database accession number E-MTAB-1759. <ext-link ext-link-type="uri" xlink:href="https://www.ebi.ac.uk/arrayexpress/arrays/browse.html?directsub=on">https://www.ebi.ac.uk/arrayexpress/arrays/browse.html?directsub=on</ext-link>
.</p>
</notes>
</front>
</pmc>
</record>
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