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
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DOI: 10.1371/journal.pone.0004833
PubMed: 19279686
PubMed Central: 2653234
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Gillespie</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Virginia Bioinformatics Institute at Virginia Tech, Blacksburg, Virginia, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Virginia Bioinformatics Institute at Virginia Tech, Blacksburg, Virginia</wicri:regionArea><placeName><region type="state">Virginie</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff2"><addr-line>Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Ammerman, Nicole C" sort="Ammerman, Nicole C" uniqKey="Ammerman N" first="Nicole C." last="Ammerman">Nicole C. Ammerman</name><affiliation wicri:level="2"><nlm:aff id="aff2"><addr-line>Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><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><affiliation wicri:level="2"><nlm:aff id="aff2"><addr-line>Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Rahman, M Sayeedur" sort="Rahman, M Sayeedur" uniqKey="Rahman M" first="M. Sayeedur" last="Rahman">M. Sayeedur Rahman</name><affiliation wicri:level="2"><nlm:aff id="aff2"><addr-line>Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Worley, Micah J" sort="Worley, Micah J" uniqKey="Worley M" first="Micah J." last="Worley">Micah J. Worley</name><affiliation wicri:level="2"><nlm:aff id="aff3"><addr-line>Department of Biology, University of Louisville, Louisville, Kentucky, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biology, University of Louisville, Louisville, Kentucky</wicri:regionArea><placeName><region type="state">Kentucky</region></placeName></affiliation></author><author><name sortKey="Setubal, Joao C" sort="Setubal, Joao C" uniqKey="Setubal J" first="Joao C." last="Setubal">Joao C. Setubal</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Virginia Bioinformatics Institute at Virginia Tech, Blacksburg, Virginia, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Virginia Bioinformatics Institute at Virginia Tech, Blacksburg, Virginia</wicri:regionArea><placeName><region type="state">Virginie</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff4"><addr-line>Department of Computer Science, Virginia Tech, Blacksburg, Virginia, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Computer Science, Virginia Tech, Blacksburg, Virginia</wicri:regionArea><placeName><region type="state">Virginie</region></placeName></affiliation></author><author><name sortKey="Sobral, Bruno S" sort="Sobral, Bruno S" uniqKey="Sobral B" first="Bruno S." last="Sobral">Bruno S. Sobral</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Virginia Bioinformatics Institute at Virginia Tech, Blacksburg, Virginia, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Virginia Bioinformatics Institute at Virginia Tech, Blacksburg, Virginia</wicri:regionArea><placeName><region type="state">Virginie</region></placeName></affiliation></author><author><name sortKey="Azad, Abdu F" sort="Azad, Abdu F" uniqKey="Azad A" first="Abdu F." last="Azad">Abdu F. Azad</name><affiliation wicri:level="2"><nlm:aff id="aff2"><addr-line>Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">19279686</idno><idno type="pmc">2653234</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2653234</idno><idno type="RBID">PMC:2653234</idno><idno type="doi">10.1371/journal.pone.0004833</idno><date when="2009">2009</date><idno type="wicri:Area/Pmc/Corpus">000314</idno><idno type="wicri:Area/Pmc/Curation">000314</idno><idno type="wicri:Area/Pmc/Checkpoint">000650</idno><idno type="wicri:Area/Ncbi/Merge">000078</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">An Anomalous Type IV Secretion System in <italic>Rickettsia</italic> Is Evolutionarily Conserved</title><author><name sortKey="Gillespie, Joseph J" sort="Gillespie, Joseph J" uniqKey="Gillespie J" first="Joseph J." last="Gillespie">Joseph J. Gillespie</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Virginia Bioinformatics Institute at Virginia Tech, Blacksburg, Virginia, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Virginia Bioinformatics Institute at Virginia Tech, Blacksburg, Virginia</wicri:regionArea><placeName><region type="state">Virginie</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff2"><addr-line>Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Ammerman, Nicole C" sort="Ammerman, Nicole C" uniqKey="Ammerman N" first="Nicole C." last="Ammerman">Nicole C. Ammerman</name><affiliation wicri:level="2"><nlm:aff id="aff2"><addr-line>Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><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><affiliation wicri:level="2"><nlm:aff id="aff2"><addr-line>Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Rahman, M Sayeedur" sort="Rahman, M Sayeedur" uniqKey="Rahman M" first="M. Sayeedur" last="Rahman">M. Sayeedur Rahman</name><affiliation wicri:level="2"><nlm:aff id="aff2"><addr-line>Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Worley, Micah J" sort="Worley, Micah J" uniqKey="Worley M" first="Micah J." last="Worley">Micah J. Worley</name><affiliation wicri:level="2"><nlm:aff id="aff3"><addr-line>Department of Biology, University of Louisville, Louisville, Kentucky, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biology, University of Louisville, Louisville, Kentucky</wicri:regionArea><placeName><region type="state">Kentucky</region></placeName></affiliation></author><author><name sortKey="Setubal, Joao C" sort="Setubal, Joao C" uniqKey="Setubal J" first="Joao C." last="Setubal">Joao C. Setubal</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Virginia Bioinformatics Institute at Virginia Tech, Blacksburg, Virginia, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Virginia Bioinformatics Institute at Virginia Tech, Blacksburg, Virginia</wicri:regionArea><placeName><region type="state">Virginie</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff4"><addr-line>Department of Computer Science, Virginia Tech, Blacksburg, Virginia, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Computer Science, Virginia Tech, Blacksburg, Virginia</wicri:regionArea><placeName><region type="state">Virginie</region></placeName></affiliation></author><author><name sortKey="Sobral, Bruno S" sort="Sobral, Bruno S" uniqKey="Sobral B" first="Bruno S." last="Sobral">Bruno S. Sobral</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Virginia Bioinformatics Institute at Virginia Tech, Blacksburg, Virginia, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Virginia Bioinformatics Institute at Virginia Tech, Blacksburg, Virginia</wicri:regionArea><placeName><region type="state">Virginie</region></placeName></affiliation></author><author><name sortKey="Azad, Abdu F" sort="Azad, Abdu F" uniqKey="Azad A" first="Abdu F." last="Azad">Abdu F. Azad</name><affiliation wicri:level="2"><nlm:aff id="aff2"><addr-line>Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author></analytic><series><title level="j">PLoS ONE</title><idno type="eISSN">1932-6203</idno><imprint><date when="2009">2009</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><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></front><back><div1 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<front><journal-meta><journal-id journal-id-type="nlm-ta">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>PLoS ONE</journal-title><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">19279686</article-id><article-id pub-id-type="pmc">2653234</article-id><article-id pub-id-type="publisher-id">09-PONE-RA-08211</article-id><article-id pub-id-type="doi">10.1371/journal.pone.0004833</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline"><subject>Computational Biology</subject><subject>Evolutionary Biology</subject><subject>Microbiology</subject></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. 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