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Complete genome of Staphylococcus aureus Tager 104 provides evidence of its relation to modern systemic hospital-acquired strains

Identifieur interne : 000714 ( Ncbi/Merge ); précédent : 000713; suivant : 000715

Complete genome of Staphylococcus aureus Tager 104 provides evidence of its relation to modern systemic hospital-acquired strains

Auteurs : Richard W. Davis [États-Unis] ; Andrew D. Brannen [États-Unis] ; Mohammad J. Hossain [États-Unis] ; Scott Monsma [États-Unis] ; Paul E. Bock [États-Unis] ; Matthias Nahrendorf [États-Unis] ; David Mead [États-Unis] ; Michael Lodes [États-Unis] ; Mark R. Liles [États-Unis] ; Peter Panizzi [États-Unis]

Source :

RBID : PMC:4778325

Abstract

Background

Staphylococcus aureus (S. aureus) infections range in severity due to expression of certain virulence factors encoded on mobile genetic elements (MGE). As such, characterization of these MGE, as well as single nucleotide polymorphisms, is of high clinical and microbiological importance. To understand the evolution of these dangerous pathogens, it is paramount to define reference strains that may predate MGE acquisition. One such candidate is S. aureus Tager 104, a previously uncharacterized strain isolated from a patient with impetigo in 1947.

Results

We show here that S. aureus Tager 104 can survive in the bloodstream and infect naïve organs. We also demonstrate a procedure to construct and validate the assembly of S. aureus genomes, using Tager 104 as a proof-of-concept. In so doing, we bridged confounding gap regions that limited our initial attempts to close this 2.82 Mb genome, through integration of data from Illumina Nextera paired-end, PacBio RS, and Lucigen NxSeq mate-pair libraries. Furthermore, we provide independent confirmation of our segmental arrangement of the Tager 104 genome by the sole use of Lucigen NxSeq libraries filled by paired-end MiSeq reads and alignment with SPAdes software. Genomic analysis of Tager 104 revealed limited MGE, and a νSaβ island configuration that is reminiscent of other hospital acquired S. aureus genomes.

Conclusions

Tager 104 represents an early-branching ancestor of certain hospital-acquired strains. Combined with its earlier isolation date and limited content of MGE, Tager 104 can serve as a viable reference for future comparative genome studies.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-016-2433-8) contains supplementary material, which is available to authorized users.


Url:
DOI: 10.1186/s12864-016-2433-8
PubMed: 26940863
PubMed Central: 4778325

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PMC:4778325

Le document en format XML

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Tager 104 provides evidence of its relation to modern systemic hospital-acquired strains</title>
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<name sortKey="Davis, Richard W" sort="Davis, Richard W" uniqKey="Davis R" first="Richard W." last="Davis">Richard W. Davis</name>
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<name sortKey="Bock, Paul E" sort="Bock, Paul E" uniqKey="Bock P" first="Paul E." last="Bock">Paul E. Bock</name>
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<name sortKey="Nahrendorf, Matthias" sort="Nahrendorf, Matthias" uniqKey="Nahrendorf M" first="Matthias" last="Nahrendorf">Matthias Nahrendorf</name>
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<region type="state">Massachusetts</region>
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<name sortKey="Liles, Mark R" sort="Liles, Mark R" uniqKey="Liles M" first="Mark R." last="Liles">Mark R. Liles</name>
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<title>Background</title>
<p>
<italic>Staphylococcus aureus</italic>
(
<italic>S. aureus</italic>
) infections range in severity due to expression of certain virulence factors encoded on mobile genetic elements (MGE). As such, characterization of these MGE, as well as single nucleotide polymorphisms, is of high clinical and microbiological importance. To understand the evolution of these dangerous pathogens, it is paramount to define reference strains that may predate MGE acquisition. One such candidate is
<italic>S. aureus</italic>
Tager 104, a previously uncharacterized strain isolated from a patient with impetigo in 1947.</p>
</sec>
<sec>
<title>Results</title>
<p>We show here that
<italic>S. aureus</italic>
Tager 104 can survive in the bloodstream and infect naïve organs. We also demonstrate a procedure to construct and validate the assembly of
<italic>S. aureus</italic>
genomes, using Tager 104 as a proof-of-concept. In so doing, we bridged confounding gap regions that limited our initial attempts to close this 2.82 Mb genome, through integration of data from Illumina Nextera paired-end, PacBio RS, and Lucigen NxSeq mate-pair libraries. Furthermore, we provide independent confirmation of our segmental arrangement of the Tager 104 genome by the sole use of Lucigen NxSeq libraries filled by paired-end MiSeq reads and alignment with SPAdes software. Genomic analysis of Tager 104 revealed limited MGE, and a νSaβ island configuration that is reminiscent of other hospital acquired
<italic>S. aureus</italic>
genomes.</p>
</sec>
<sec>
<title>Conclusions</title>
<p>Tager 104 represents an early-branching ancestor of certain hospital-acquired strains. Combined with its earlier isolation date and limited content of MGE, Tager 104 can serve as a viable reference for future comparative genome studies.</p>
</sec>
<sec>
<title>Electronic supplementary material</title>
<p>The online version of this article (doi:10.1186/s12864-016-2433-8) contains supplementary material, which is available to authorized users.</p>
</sec>
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<name sortKey="Tager, M" uniqKey="Tager M">M Tager</name>
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<author>
<name sortKey="Tager, M" uniqKey="Tager M">M Tager</name>
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</author>
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<name sortKey="Edwards, Ge" uniqKey="Edwards G">GE Edwards</name>
</author>
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<name sortKey="Pennycott, Tw" uniqKey="Pennycott T">TW Pennycott</name>
</author>
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<name sortKey="Foster, G" uniqKey="Foster G">G Foster</name>
</author>
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<name sortKey="Mot, D" uniqKey="Mot D">D Mot</name>
</author>
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<name sortKey="Hermans, K" uniqKey="Hermans K">K Hermans</name>
</author>
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<name sortKey="Baert, K" uniqKey="Baert K">K Baert</name>
</author>
<author>
<name sortKey="Peacock, Sj" uniqKey="Peacock S">SJ Peacock</name>
</author>
</analytic>
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<analytic>
<author>
<name sortKey="Winstel, V" uniqKey="Winstel V">V Winstel</name>
</author>
<author>
<name sortKey="Liang, C" uniqKey="Liang C">C Liang</name>
</author>
<author>
<name sortKey="Sanchez Carballo, P" uniqKey="Sanchez Carballo P">P Sanchez-Carballo</name>
</author>
<author>
<name sortKey="Steglich, M" uniqKey="Steglich M">M Steglich</name>
</author>
<author>
<name sortKey="Munar, M" uniqKey="Munar M">M Munar</name>
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<name sortKey="Broker, Bm" uniqKey="Broker B">BM Broker</name>
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</analytic>
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</back>
</TEI>
<pmc article-type="research-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">BMC Genomics</journal-id>
<journal-id journal-id-type="iso-abbrev">BMC Genomics</journal-id>
<journal-title-group>
<journal-title>BMC Genomics</journal-title>
</journal-title-group>
<issn pub-type="epub">1471-2164</issn>
<publisher>
<publisher-name>BioMed Central</publisher-name>
<publisher-loc>London</publisher-loc>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">26940863</article-id>
<article-id pub-id-type="pmc">4778325</article-id>
<article-id pub-id-type="publisher-id">2433</article-id>
<article-id pub-id-type="doi">10.1186/s12864-016-2433-8</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>Complete genome of
<italic>Staphylococcus aureus</italic>
Tager 104 provides evidence of its relation to modern systemic hospital-acquired strains</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Davis</surname>
<given-names>Richard W.</given-names>
<suffix>IV</suffix>
</name>
<address>
<email>davisri@auburn.edu</email>
</address>
<xref ref-type="aff" rid="Aff1"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Brannen</surname>
<given-names>Andrew D.</given-names>
</name>
<address>
<email>adb0009@auburn.edu</email>
</address>
<xref ref-type="aff" rid="Aff1"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Hossain</surname>
<given-names>Mohammad J.</given-names>
</name>
<address>
<email>mjh0007@auburn.edu</email>
</address>
<xref ref-type="aff" rid="Aff2"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Monsma</surname>
<given-names>Scott</given-names>
</name>
<address>
<email>smonsma@lucigen.com</email>
</address>
<xref ref-type="aff" rid="Aff3"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Bock</surname>
<given-names>Paul E.</given-names>
</name>
<address>
<email>paul.bock@vanderbilt.edu</email>
</address>
<xref ref-type="aff" rid="Aff4"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Nahrendorf</surname>
<given-names>Matthias</given-names>
</name>
<address>
<email>mnahrendorf@mgh.harvard.edu</email>
</address>
<xref ref-type="aff" rid="Aff5"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Mead</surname>
<given-names>David</given-names>
</name>
<address>
<email>dmead@lucigen.com</email>
</address>
<xref ref-type="aff" rid="Aff3"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Lodes</surname>
<given-names>Michael</given-names>
</name>
<address>
<email>mlodes@lucigen.com</email>
</address>
<xref ref-type="aff" rid="Aff3"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Liles</surname>
<given-names>Mark R.</given-names>
</name>
<address>
<email>lilesma@auburn.edu</email>
</address>
<xref ref-type="aff" rid="Aff2"></xref>
</contrib>
<contrib contrib-type="author" corresp="yes">
<contrib-id contrib-id-type="orcid">http://orcid.org/0000-0003-0141-8807</contrib-id>
<name>
<surname>Panizzi</surname>
<given-names>Peter</given-names>
</name>
<address>
<phone>334-844-7941</phone>
<email>panizzi@auburn.edu</email>
</address>
<xref ref-type="aff" rid="Aff1"></xref>
</contrib>
<aff id="Aff1">
<label></label>
Department of Drug Discovery and Development, Harrison School of Pharmacy, Auburn University, 4306 Walker Building, Auburn, AL 36849 USA</aff>
<aff id="Aff2">
<label></label>
Department of Biological Sciences, Auburn University, 101 Rouse Life Science Building, Auburn, AL 36849 USA</aff>
<aff id="Aff3">
<label></label>
Lucigen Corporation, 2905 Parmenter St, Middleton, WI 53562 USA</aff>
<aff id="Aff4">
<label></label>
Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, TN 37232 USA</aff>
<aff id="Aff5">
<label></label>
Center for Systems Biology, Massachusetts General Hospital and Harvard Medical School, Simches Research Building, 185 Cambridge St., Boston, MA 02114 USA</aff>
</contrib-group>
<pub-date pub-type="epub">
<day>3</day>
<month>3</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="pmc-release">
<day>3</day>
<month>3</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="collection">
<year>2016</year>
</pub-date>
<volume>17</volume>
<elocation-id>179</elocation-id>
<history>
<date date-type="received">
<day>28</day>
<month>9</month>
<year>2015</year>
</date>
<date date-type="accepted">
<day>3</day>
<month>2</month>
<year>2016</year>
</date>
</history>
<permissions>
<copyright-statement>© Davis et al. 2016</copyright-statement>
<license license-type="OpenAccess">
<license-p>
<bold>Open Access</bold>
This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (
<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>
), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (
<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/publicdomain/zero/1.0/">http://creativecommons.org/publicdomain/zero/1.0/</ext-link>
) applies to the data made available in this article, unless otherwise stated.</license-p>
</license>
</permissions>
<abstract id="Abs1">
<sec>
<title>Background</title>
<p>
<italic>Staphylococcus aureus</italic>
(
<italic>S. aureus</italic>
) infections range in severity due to expression of certain virulence factors encoded on mobile genetic elements (MGE). As such, characterization of these MGE, as well as single nucleotide polymorphisms, is of high clinical and microbiological importance. To understand the evolution of these dangerous pathogens, it is paramount to define reference strains that may predate MGE acquisition. One such candidate is
<italic>S. aureus</italic>
Tager 104, a previously uncharacterized strain isolated from a patient with impetigo in 1947.</p>
</sec>
<sec>
<title>Results</title>
<p>We show here that
<italic>S. aureus</italic>
Tager 104 can survive in the bloodstream and infect naïve organs. We also demonstrate a procedure to construct and validate the assembly of
<italic>S. aureus</italic>
genomes, using Tager 104 as a proof-of-concept. In so doing, we bridged confounding gap regions that limited our initial attempts to close this 2.82 Mb genome, through integration of data from Illumina Nextera paired-end, PacBio RS, and Lucigen NxSeq mate-pair libraries. Furthermore, we provide independent confirmation of our segmental arrangement of the Tager 104 genome by the sole use of Lucigen NxSeq libraries filled by paired-end MiSeq reads and alignment with SPAdes software. Genomic analysis of Tager 104 revealed limited MGE, and a νSaβ island configuration that is reminiscent of other hospital acquired
<italic>S. aureus</italic>
genomes.</p>
</sec>
<sec>
<title>Conclusions</title>
<p>Tager 104 represents an early-branching ancestor of certain hospital-acquired strains. Combined with its earlier isolation date and limited content of MGE, Tager 104 can serve as a viable reference for future comparative genome studies.</p>
</sec>
<sec>
<title>Electronic supplementary material</title>
<p>The online version of this article (doi:10.1186/s12864-016-2433-8) contains supplementary material, which is available to authorized users.</p>
</sec>
</abstract>
<funding-group>
<award-group>
<funding-source>
<institution-wrap>
<institution-id institution-id-type="FundRef">http://dx.doi.org/10.13039/100000050</institution-id>
<institution>National Heart, Lung, and Blood Institute (US)</institution>
</institution-wrap>
</funding-source>
<award-id>R00HL094533</award-id>
<principal-award-recipient>
<name>
<surname>Panizzi</surname>
<given-names>Peter</given-names>
</name>
</principal-award-recipient>
</award-group>
<award-group>
<funding-source>
<institution-wrap>
<institution-id institution-id-type="FundRef">http://dx.doi.org/10.13039/100000050</institution-id>
<institution>National Heart, Lung, and Blood Institute (US)</institution>
</institution-wrap>
</funding-source>
<award-id>R01HL114477</award-id>
<principal-award-recipient>
<name>
<surname>Panizzi</surname>
<given-names>Peter</given-names>
</name>
</principal-award-recipient>
</award-group>
<award-group>
<funding-source>
<institution-wrap>
<institution-id institution-id-type="FundRef">http://dx.doi.org/10.13039/100000060</institution-id>
<institution>National Institute of Allergy and Infectious Diseases (US)</institution>
</institution-wrap>
</funding-source>
<award-id>2R44AI085840</award-id>
<principal-award-recipient>
<name>
<surname>Mead</surname>
<given-names>David</given-names>
</name>
</principal-award-recipient>
</award-group>
<award-group>
<funding-source>
<institution-wrap>
<institution-id institution-id-type="FundRef">http://dx.doi.org/10.13039/100000050</institution-id>
<institution>National Heart, Lung, and Blood Institute (US)</institution>
</institution-wrap>
</funding-source>
<award-id>R01HL071544</award-id>
<principal-award-recipient>
<name>
<surname>Bock</surname>
<given-names>Paul E.</given-names>
</name>
</principal-award-recipient>
</award-group>
</funding-group>
<custom-meta-group>
<custom-meta>
<meta-name>issue-copyright-statement</meta-name>
<meta-value>© The Author(s) 2016</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
</front>
</pmc>
<affiliations>
<list>
<country>
<li>États-Unis</li>
</country>
<region>
<li>Alabama</li>
<li>Massachusetts</li>
<li>Tennessee</li>
<li>Wisconsin</li>
</region>
</list>
<tree>
<country name="États-Unis">
<region name="Alabama">
<name sortKey="Davis, Richard W" sort="Davis, Richard W" uniqKey="Davis R" first="Richard W." last="Davis">Richard W. Davis</name>
</region>
<name sortKey="Bock, Paul E" sort="Bock, Paul E" uniqKey="Bock P" first="Paul E." last="Bock">Paul E. Bock</name>
<name sortKey="Brannen, Andrew D" sort="Brannen, Andrew D" uniqKey="Brannen A" first="Andrew D." last="Brannen">Andrew D. Brannen</name>
<name sortKey="Hossain, Mohammad J" sort="Hossain, Mohammad J" uniqKey="Hossain M" first="Mohammad J." last="Hossain">Mohammad J. Hossain</name>
<name sortKey="Liles, Mark R" sort="Liles, Mark R" uniqKey="Liles M" first="Mark R." last="Liles">Mark R. Liles</name>
<name sortKey="Lodes, Michael" sort="Lodes, Michael" uniqKey="Lodes M" first="Michael" last="Lodes">Michael Lodes</name>
<name sortKey="Mead, David" sort="Mead, David" uniqKey="Mead D" first="David" last="Mead">David Mead</name>
<name sortKey="Monsma, Scott" sort="Monsma, Scott" uniqKey="Monsma S" first="Scott" last="Monsma">Scott Monsma</name>
<name sortKey="Nahrendorf, Matthias" sort="Nahrendorf, Matthias" uniqKey="Nahrendorf M" first="Matthias" last="Nahrendorf">Matthias Nahrendorf</name>
<name sortKey="Panizzi, Peter" sort="Panizzi, Peter" uniqKey="Panizzi P" first="Peter" last="Panizzi">Peter Panizzi</name>
</country>
</tree>
</affiliations>
</record>

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