Key experimental evidence of chromosomal DNA transfer among selected tuberculosis-causing mycobacteria
Identifieur interne : 001A62 ( Pmc/Curation ); précédent : 001A61; suivant : 001A63Key experimental evidence of chromosomal DNA transfer among selected tuberculosis-causing mycobacteria
Auteurs : Eva C. Boritsch [France] ; Varun Khanna [France] ; Alexandre Pawlik [France] ; Nadine Honoré [France] ; Victor H. Navas [France] ; Laurence Ma [France] ; Christiane Bouchier [France] ; Torsten Seemann [Australie] ; Philip Supply [France] ; Timothy P. Stinear [Australie] ; Roland Brosch [France]Source :
- Proceedings of the National Academy of Sciences of the United States of America [ 0027-8424 ] ; 2016.
Abstract
Whereas most of the more than 130 described mycobacterial species are harmless saprophytes,
Url:
DOI: 10.1073/pnas.1604921113
PubMed: 27528665
PubMed Central: 5024641
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<author><name sortKey="Supply, Philip" sort="Supply, Philip" uniqKey="Supply P" first="Philip" last="Supply">Philip Supply</name>
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<country xml:lang="fr">France</country>
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<author><name sortKey="Khanna, Varun" sort="Khanna, Varun" uniqKey="Khanna V" first="Varun" last="Khanna">Varun Khanna</name>
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;</nlm:aff>
<country xml:lang="fr">France</country>
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<author><name sortKey="Honore, Nadine" sort="Honore, Nadine" uniqKey="Honore N" first="Nadine" last="Honoré">Nadine Honoré</name>
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, Unit for Integrated Mycobacterial Pathogenomics, 75015 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
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<author><name sortKey="Navas, Victor H" sort="Navas, Victor H" uniqKey="Navas V" first="Victor H." last="Navas">Victor H. Navas</name>
<affiliation wicri:level="1"><nlm:aff id="aff3">IP, Lymphocyte Cell Biology Unit, 75015 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
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<author><name sortKey="Ma, Laurence" sort="Ma, Laurence" uniqKey="Ma L" first="Laurence" last="Ma">Laurence Ma</name>
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;</nlm:aff>
<country xml:lang="fr">France</country>
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<author><name sortKey="Bouchier, Christiane" sort="Bouchier, Christiane" uniqKey="Bouchier C" first="Christiane" last="Bouchier">Christiane Bouchier</name>
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;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<author><name sortKey="Seemann, Torsten" sort="Seemann, Torsten" uniqKey="Seemann T" first="Torsten" last="Seemann">Torsten Seemann</name>
<affiliation wicri:level="1"><nlm:aff id="aff5">Victorian Life Sciences Computation Initiative,<institution>University of Melbourne</institution>
, Carlton, VIC 3053,<country>Australia</country>
;</nlm:aff>
<country xml:lang="fr">Australie</country>
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<author><name sortKey="Supply, Philip" sort="Supply, Philip" uniqKey="Supply P" first="Philip" last="Supply">Philip Supply</name>
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, 59000 Lille,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
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<author><name sortKey="Stinear, Timothy P" sort="Stinear, Timothy P" uniqKey="Stinear T" first="Timothy P." last="Stinear">Timothy P. Stinear</name>
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, Melbourne, VIC 3000,<country>Australia</country>
</nlm:aff>
<country xml:lang="fr">Australie</country>
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<author><name sortKey="Brosch, Roland" sort="Brosch, Roland" uniqKey="Brosch R" first="Roland" last="Brosch">Roland Brosch</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Institut Pasteur (IP)</institution>
, Unit for Integrated Mycobacterial Pathogenomics, 75015 Paris,<country>France</country>
;</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<series><title level="j">Proceedings of the National Academy of Sciences of the United States of America</title>
<idno type="ISSN">0027-8424</idno>
<idno type="eISSN">1091-6490</idno>
<imprint><date when="2016">2016</date>
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<front><div type="abstract" xml:lang="en"><title>Significance</title>
<p>Whereas most of the more than 130 described mycobacterial species are harmless saprophytes, <italic>Mycobacterium tuberculosis</italic>
, the human tuberculosis-causing agent, represents one of the deadliest bacterial pathogens in the history of humankind. To explore the mechanisms behind this spectacular evolutionary trajectory toward pathogenicity, we have experimentally investigated the faculty of different tuberculosis-causing mycobacteria in conducting horizontal gene transfer (HGT). Our studies identified unique chromosomal DNA transfer between strains of the <italic>Mycobacterium canettii</italic>
clade, which resemble most closely the putative common ancestor of the <italic>M. tuberculosis</italic>
complex. This outstanding feature suggests that during the evolution of <italic>M. tuberculosis</italic>
, HGT might have represented the major mechanism for acquisition of genes that helped these mycobacteria to increasingly resist host defenses and become major pathogens.</p>
</div>
</front>
</TEI>
<pmc article-type="research-article"><pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Proc Natl Acad Sci U S A</journal-id>
<journal-id journal-id-type="iso-abbrev">Proc. Natl. Acad. Sci. U.S.A</journal-id>
<journal-id journal-id-type="hwp">pnas</journal-id>
<journal-id journal-id-type="pmc">pnas</journal-id>
<journal-id journal-id-type="publisher-id">PNAS</journal-id>
<journal-title-group><journal-title>Proceedings of the National Academy of Sciences of the United States of America</journal-title>
</journal-title-group>
<issn pub-type="ppub">0027-8424</issn>
<issn pub-type="epub">1091-6490</issn>
<publisher><publisher-name>National Academy of Sciences</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">27528665</article-id>
<article-id pub-id-type="pmc">5024641</article-id>
<article-id pub-id-type="publisher-id">201604921</article-id>
<article-id pub-id-type="doi">10.1073/pnas.1604921113</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Biological Sciences</subject>
<subj-group><subject>Microbiology</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>Key experimental evidence of chromosomal DNA transfer among selected tuberculosis-causing mycobacteria</article-title>
<alt-title alt-title-type="short">Gene transfer between <italic>Mycobacterium canettii</italic>
</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Boritsch</surname>
<given-names>Eva C.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Khanna</surname>
<given-names>Varun</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Pawlik</surname>
<given-names>Alexandre</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Honoré</surname>
<given-names>Nadine</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Navas</surname>
<given-names>Victor H.</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ma</surname>
<given-names>Laurence</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>d</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Bouchier</surname>
<given-names>Christiane</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>d</sup>
</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0001-6046-610X</contrib-id>
<name><surname>Seemann</surname>
<given-names>Torsten</given-names>
</name>
<xref ref-type="aff" rid="aff5"><sup>e</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Supply</surname>
<given-names>Philip</given-names>
</name>
<xref ref-type="aff" rid="aff6"><sup>f</sup>
</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0003-0150-123X</contrib-id>
<name><surname>Stinear</surname>
<given-names>Timothy P.</given-names>
</name>
<xref ref-type="aff" rid="aff7"><sup>g</sup>
</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0003-2587-3863</contrib-id>
<name><surname>Brosch</surname>
<given-names>Roland</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>1</sup>
</xref>
</contrib>
<aff id="aff1"><sup>a</sup>
<institution>Institut Pasteur (IP)</institution>
, Unit for Integrated Mycobacterial Pathogenomics, 75015 Paris,<country>France</country>
;</aff>
<aff id="aff2"><sup>b</sup>
IP, Hub Bioinformatique et Biostatistique, C3BI, Unité de Services et de Recherche, USR 3756, IP CNRS, 75015 Paris,<country>France</country>
;</aff>
<aff id="aff3"><sup>c</sup>
IP, Lymphocyte Cell Biology Unit, 75015 Paris,<country>France</country>
;</aff>
<aff id="aff4"><sup>d</sup>
IP, PF1-Plate-Forme Génomique, 75015 Paris,<country>France</country>
;</aff>
<aff id="aff5"><sup>e</sup>
Victorian Life Sciences Computation Initiative,<institution>University of Melbourne</institution>
, Carlton, VIC 3053,<country>Australia</country>
;</aff>
<aff id="aff6"><sup>f</sup>
INSERM U1019, CNRS UMR 8204, Center for Infection and Immunity, Institut Pasteur de Lille,<institution>Université de Lille</institution>
, 59000 Lille,<country>France</country>
;</aff>
<aff id="aff7"><sup>g</sup>
Department of Microbiology and Immunology, Peter Doherty Institute for Infection and Immunity,<institution>University of Melbourne</institution>
, Melbourne, VIC 3000,<country>Australia</country>
</aff>
</contrib-group>
<author-notes><corresp id="cor1"><sup>1</sup>
To whom correspondence should be addressed. Email: <email>roland.brosch@pasteur.fr</email>
.</corresp>
<fn fn-type="edited-by"><p>Edited by Lalita Ramakrishnan, University of Cambridge, Cambridge, United Kingdom, and approved July 5, 2016 (received for review March 24, 2016)</p>
</fn>
<fn fn-type="con"><p>Author contributions: E.C.B. and R.B. designed research; E.C.B., A.P., N.H., and L.M. performed research; V.K., T.S., and T.P.S. contributed new reagents/analytic tools; E.C.B., V.K., A.P., N.H., V.H.N., L.M., C.B., T.S., P.S., T.P.S., and R.B. analyzed data; E.C.B. and R.B. wrote the paper; and V.K. performed bioinformatic analysis.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><day>30</day>
<month>8</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="epub"><day>15</day>
<month>8</month>
<year>2016</year>
</pub-date>
<volume>113</volume>
<issue>35</issue>
<fpage>9876</fpage>
<lpage>9881</lpage>
<permissions></permissions>
<self-uri xlink:title="pdf" xlink:href="pnas.201604921.pdf"></self-uri>
<abstract abstract-type="executive-summary"><title>Significance</title>
<p>Whereas most of the more than 130 described mycobacterial species are harmless saprophytes, <italic>Mycobacterium tuberculosis</italic>
, the human tuberculosis-causing agent, represents one of the deadliest bacterial pathogens in the history of humankind. To explore the mechanisms behind this spectacular evolutionary trajectory toward pathogenicity, we have experimentally investigated the faculty of different tuberculosis-causing mycobacteria in conducting horizontal gene transfer (HGT). Our studies identified unique chromosomal DNA transfer between strains of the <italic>Mycobacterium canettii</italic>
clade, which resemble most closely the putative common ancestor of the <italic>M. tuberculosis</italic>
complex. This outstanding feature suggests that during the evolution of <italic>M. tuberculosis</italic>
, HGT might have represented the major mechanism for acquisition of genes that helped these mycobacteria to increasingly resist host defenses and become major pathogens.</p>
</abstract>
<abstract><p>Horizontal gene transfer (HGT) is a major driving force of bacterial diversification and evolution. For tuberculosis-causing mycobacteria, the impact of HGT in the emergence and distribution of dominant lineages remains a matter of debate. Here, by using fluorescence-assisted mating assays and whole genome sequencing, we present unique experimental evidence of chromosomal DNA transfer between tubercle bacilli of the early-branching <italic>Mycobacterium canettii</italic>
clade. We found that the obtained recombinants had received multiple donor-derived DNA fragments in the size range of 100 bp to 118 kbp, fragments large enough to contain whole operons. Although the transfer frequency between <italic>M. canettii</italic>
strains was low and no transfer could be observed among classical <italic>Mycobacterium tuberculosis</italic>
complex (MTBC) strains, our study provides the proof of concept for genetic exchange in tubercle bacilli. This outstanding, now experimentally validated phenomenon presumably played a key role in the early evolution of the MTBC toward pathogenicity. Moreover, our findings also provide important information for the risk evaluation of potential transfer of drug resistance and fitness mutations among clinically relevant mycobacterial strains.</p>
</abstract>
<kwd-group><kwd>recombination</kwd>
<kwd>DNA transfer</kwd>
<kwd>tuberculosis</kwd>
<kwd><italic>Mycobacterium canettii</italic>
</kwd>
<kwd>evolution</kwd>
</kwd-group>
<funding-group><award-group id="gs1"><funding-source id="sp1">European Commission Directorate-General for Research and Innovation<named-content content-type="funder-id">100004431</named-content>
</funding-source>
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<award-group id="gs2"><funding-source id="sp2">European Commission Directorate-General for Research and Innovation<named-content content-type="funder-id">100004431</named-content>
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</award-group>
</funding-group>
<counts><page-count count="6"></page-count>
</counts>
</article-meta>
</front>
</pmc>
</record>
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