An Anomalous Type IV Secretion System in Rickettsia Is Evolutionarily Conserved
Identifieur interne : 000078 ( Ncbi/Merge ); précédent : 000077; suivant : 000079An Anomalous Type IV Secretion System in Rickettsia Is Evolutionarily Conserved
Auteurs : Joseph J. Gillespie [États-Unis] ; Nicole C. Ammerman [États-Unis] ; Sheila M. Dreher-Lesnick [États-Unis] ; M. Sayeedur Rahman [États-Unis] ; Micah J. Worley [États-Unis] ; Joao C. Setubal [États-Unis] ; Bruno S. Sobral [États-Unis] ; Abdu F. Azad [États-Unis]Source :
- PLoS ONE [ 1932-6203 ] ; 2009.
Abstract
Bacterial type IV secretion systems (T4SSs) comprise a diverse transporter family functioning in conjugation, competence, and effector molecule (DNA and/or protein) translocation. Thirteen genome sequences from
Superimposition of T4SS structural/functional information over previously identified
We present the
Url:
DOI: 10.1371/journal.pone.0004833
PubMed: 19279686
PubMed Central: 2653234
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PMC:2653234Le document en format XML
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<front><div type="abstract" xml:lang="en"><sec><title>Background</title>
<p>Bacterial type IV secretion systems (T4SSs) comprise a diverse transporter family functioning in conjugation, competence, and effector molecule (DNA and/or protein) translocation. Thirteen genome sequences from <italic>Rickettsia</italic>
, obligate intracellular symbionts/pathogens of a wide range of eukaryotes, have revealed a reduced T4SS relative to the <italic>Agrobacterium tumefaciens</italic>
archetype (<italic>vir</italic>
). However, the <italic>Rickettsia</italic>
T4SS has not been functionally characterized for its role in symbiosis/virulence, and none of its substrates are known.</p>
</sec>
<sec><title>Results</title>
<p>Superimposition of T4SS structural/functional information over previously identified <italic>Rickettsia</italic>
components implicate a functional <italic>Rickettsia</italic>
T4SS. <italic>virB4</italic>
, <italic>virB8</italic>
and <italic>virB9</italic>
are duplicated, yet only one copy of each has the conserved features of similar genes in other T4SSs. An extraordinarily duplicated VirB6 gene encodes five hydrophobic proteins conserved only in a short region known to be involved in DNA transfer in <italic>A. tumefaciens</italic>
. <italic>virB1</italic>
, <italic>virB2</italic>
and <italic>virB7</italic>
are newly identified, revealing a <italic>Rickettsia</italic>
T4SS lacking only <italic>virB5</italic>
relative to the <italic>vir</italic>
archetype. Phylogeny estimation suggests vertical inheritance of all components, despite gene rearrangements into an archipelago of five islets. Similarities of <italic>Rickettsia</italic>
VirB7/VirB9 to ComB7/ComB9 proteins of ε-proteobacteria, as well as phylogenetic affinities to the <italic>Legionella lvh</italic>
T4SS, imply the Rickettsiales ancestor acquired a <italic>vir</italic>
-like locus from distantly related bacteria, perhaps while residing in a protozoan host. Modern modifications of these systems likely reflect diversification with various eukaryotic host cells.</p>
</sec>
<sec><title>Conclusion</title>
<p>We present the <italic>rvh</italic>
(Rickettsiales <italic>vir</italic>
homolog) T4SS, an evolutionary conserved transporter with an unknown role in rickettsial biology. This work lays the foundation for future laboratory characterization of this system, and also identifies the <italic>Legionella lvh</italic>
T4SS as a suitable genetic model.</p>
</sec>
</div>
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</subj-group>
</article-categories>
<title-group><article-title>An Anomalous Type IV Secretion System in <italic>Rickettsia</italic>
Is Evolutionarily Conserved</article-title>
<alt-title alt-title-type="running-head"><italic>Rickettsia</italic>
Type IV Secretion</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Gillespie</surname>
<given-names>Joseph J.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>*</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ammerman</surname>
<given-names>Nicole C.</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Dreher-Lesnick</surname>
<given-names>Sheila M.</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Rahman</surname>
<given-names>M. Sayeedur</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Worley</surname>
<given-names>Micah J.</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Setubal</surname>
<given-names>Joao C.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff4"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Sobral</surname>
<given-names>Bruno S.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Azad</surname>
<given-names>Abdu F.</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>1</label>
<addr-line>Virginia Bioinformatics Institute at Virginia Tech, Blacksburg, Virginia, United States of America</addr-line>
</aff>
<aff id="aff2"><label>2</label>
<addr-line>Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, Maryland, United States of America</addr-line>
</aff>
<aff id="aff3"><label>3</label>
<addr-line>Department of Biology, University of Louisville, Louisville, Kentucky, United States of America</addr-line>
</aff>
<aff id="aff4"><label>4</label>
<addr-line>Department of Computer Science, Virginia Tech, Blacksburg, Virginia, United States of America</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Bereswill</surname>
<given-names>Stefan</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1">Charité-Universitätsmedizin Berlin, Germany</aff>
<author-notes><corresp id="cor1">* E-mail: <email>jgill@vbi.vt.edu</email>
</corresp>
<fn fn-type="con"><p>Conceived and designed the experiments: JJG NA SDL MSR MW JCS BWSS AA. Performed the experiments: JJG NA SDL. Analyzed the data: JJG. Contributed reagents/materials/analysis tools: JJG JCS BWSS AA. Wrote the paper: JJG NA SDL MSR MW JCS BWSS AA.</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><year>2009</year>
</pub-date>
<pub-date pub-type="epub"><day>12</day>
<month>3</month>
<year>2009</year>
</pub-date>
<volume>4</volume>
<issue>3</issue>
<elocation-id>e4833</elocation-id>
<history><date date-type="received"><day>16</day>
<month>1</month>
<year>2009</year>
</date>
<date date-type="accepted"><day>28</day>
<month>1</month>
<year>2009</year>
</date>
</history>
<copyright-statement>Gillespie et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</copyright-statement>
<copyright-year>2009</copyright-year>
<abstract><sec><title>Background</title>
<p>Bacterial type IV secretion systems (T4SSs) comprise a diverse transporter family functioning in conjugation, competence, and effector molecule (DNA and/or protein) translocation. Thirteen genome sequences from <italic>Rickettsia</italic>
, obligate intracellular symbionts/pathogens of a wide range of eukaryotes, have revealed a reduced T4SS relative to the <italic>Agrobacterium tumefaciens</italic>
archetype (<italic>vir</italic>
). However, the <italic>Rickettsia</italic>
T4SS has not been functionally characterized for its role in symbiosis/virulence, and none of its substrates are known.</p>
</sec>
<sec><title>Results</title>
<p>Superimposition of T4SS structural/functional information over previously identified <italic>Rickettsia</italic>
components implicate a functional <italic>Rickettsia</italic>
T4SS. <italic>virB4</italic>
, <italic>virB8</italic>
and <italic>virB9</italic>
are duplicated, yet only one copy of each has the conserved features of similar genes in other T4SSs. An extraordinarily duplicated VirB6 gene encodes five hydrophobic proteins conserved only in a short region known to be involved in DNA transfer in <italic>A. tumefaciens</italic>
. <italic>virB1</italic>
, <italic>virB2</italic>
and <italic>virB7</italic>
are newly identified, revealing a <italic>Rickettsia</italic>
T4SS lacking only <italic>virB5</italic>
relative to the <italic>vir</italic>
archetype. Phylogeny estimation suggests vertical inheritance of all components, despite gene rearrangements into an archipelago of five islets. Similarities of <italic>Rickettsia</italic>
VirB7/VirB9 to ComB7/ComB9 proteins of ε-proteobacteria, as well as phylogenetic affinities to the <italic>Legionella lvh</italic>
T4SS, imply the Rickettsiales ancestor acquired a <italic>vir</italic>
-like locus from distantly related bacteria, perhaps while residing in a protozoan host. Modern modifications of these systems likely reflect diversification with various eukaryotic host cells.</p>
</sec>
<sec><title>Conclusion</title>
<p>We present the <italic>rvh</italic>
(Rickettsiales <italic>vir</italic>
homolog) T4SS, an evolutionary conserved transporter with an unknown role in rickettsial biology. This work lays the foundation for future laboratory characterization of this system, and also identifies the <italic>Legionella lvh</italic>
T4SS as a suitable genetic model.</p>
</sec>
</abstract>
<counts><page-count count="24"></page-count>
</counts>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>États-Unis</li>
</country>
<region><li>Kentucky</li>
<li>Maryland</li>
<li>Virginie</li>
</region>
</list>
<tree><country name="États-Unis"><region name="Virginie"><name sortKey="Gillespie, Joseph J" sort="Gillespie, Joseph J" uniqKey="Gillespie J" first="Joseph J." last="Gillespie">Joseph J. Gillespie</name>
</region>
<name sortKey="Ammerman, Nicole C" sort="Ammerman, Nicole C" uniqKey="Ammerman N" first="Nicole C." last="Ammerman">Nicole C. Ammerman</name>
<name sortKey="Azad, Abdu F" sort="Azad, Abdu F" uniqKey="Azad A" first="Abdu F." last="Azad">Abdu F. Azad</name>
<name sortKey="Dreher Lesnick, Sheila M" sort="Dreher Lesnick, Sheila M" uniqKey="Dreher Lesnick S" first="Sheila M." last="Dreher-Lesnick">Sheila M. Dreher-Lesnick</name>
<name sortKey="Gillespie, Joseph J" sort="Gillespie, Joseph J" uniqKey="Gillespie J" first="Joseph J." last="Gillespie">Joseph J. Gillespie</name>
<name sortKey="Rahman, M Sayeedur" sort="Rahman, M Sayeedur" uniqKey="Rahman M" first="M. Sayeedur" last="Rahman">M. Sayeedur Rahman</name>
<name sortKey="Setubal, Joao C" sort="Setubal, Joao C" uniqKey="Setubal J" first="Joao C." last="Setubal">Joao C. Setubal</name>
<name sortKey="Setubal, Joao C" sort="Setubal, Joao C" uniqKey="Setubal J" first="Joao C." last="Setubal">Joao C. Setubal</name>
<name sortKey="Sobral, Bruno S" sort="Sobral, Bruno S" uniqKey="Sobral B" first="Bruno S." last="Sobral">Bruno S. Sobral</name>
<name sortKey="Worley, Micah J" sort="Worley, Micah J" uniqKey="Worley M" first="Micah J." last="Worley">Micah J. Worley</name>
</country>
</tree>
</affiliations>
</record>
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