Phenotypic Heterogeneity of Genomically-Diverse Isolates of Streptococcus mutans
Identifieur interne : 000C60 ( Ncbi/Merge ); précédent : 000C59; suivant : 000C61Phenotypic Heterogeneity of Genomically-Diverse Isolates of Streptococcus mutans
Auteurs : Sara R. Palmer [États-Unis] ; James H. Miller [États-Unis] ; Jacqueline Abranches [États-Unis] ; Lin Zeng [États-Unis] ; Tristan Lefebure [France, États-Unis] ; Vincent P. Richards [États-Unis] ; José A. Lemos [États-Unis] ; Michael J. Stanhope [États-Unis] ; Robert A. Burne [États-Unis]Source :
- PLoS ONE [ 1932-6203 ] ; 2013.
Abstract
High coverage, whole genome shotgun (WGS) sequencing of 57 geographically- and genetically-diverse isolates of
Url:
DOI: 10.1371/journal.pone.0061358
PubMed: 23613838
PubMed Central: 3628994
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<front><div type="abstract" xml:lang="en"><p>High coverage, whole genome shotgun (WGS) sequencing of 57 geographically- and genetically-diverse isolates of <italic>Streptococcus mutans</italic>
from individuals of known dental caries status was recently completed. Of the 57 sequenced strains, fifteen isolates, were selected based primarily on differences in gene content and phenotypic characteristics known to affect virulence and compared with the reference strain UA159. A high degree of variability in these properties was observed between strains, with a broad spectrum of sensitivities to low pH, oxidative stress (air and paraquat) and exposure to competence stimulating peptide (CSP). Significant differences in autolytic behavior and in biofilm development in glucose or sucrose were also observed. Natural genetic competence varied among isolates, and this was correlated to the presence or absence of competence genes, <italic>comCDE</italic>
and <italic>comX</italic>
, and to bacteriocins. In general strains that lacked the ability to become competent possessed fewer genes for bacteriocins and immunity proteins or contained polymorphic variants of these genes. WGS sequence analysis of the pan-genome revealed, for the first time, components of a Type VII secretion system in several <italic>S. mutans</italic>
strains, as well as two putative ORFs that encode possible collagen binding proteins located upstream of the <italic>cnm</italic>
gene, which is associated with host cell invasiveness. The virulence of these particular strains was assessed in a wax-worm model. This is the first study to combine a comprehensive analysis of key virulence-related phenotypes with extensive genomic analysis of a pathogen that evolved closely with humans. Our analysis highlights the phenotypic diversity of <italic>S. mutans</italic>
isolates and indicates that the species has evolved a variety of adaptive strategies to persist in the human oral cavity and, when conditions are favorable, to initiate disease.</p>
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<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">23613838</article-id>
<article-id pub-id-type="pmc">3628994</article-id>
<article-id pub-id-type="publisher-id">PONE-D-12-36905</article-id>
<article-id pub-id-type="doi">10.1371/journal.pone.0061358</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
<subj-group subj-group-type="Discipline-v2"><subject>Biology</subject>
<subj-group><subject>Evolutionary Biology</subject>
<subj-group><subject>Evolutionary Processes</subject>
<subj-group><subject>Evolutionary Selection</subject>
</subj-group>
</subj-group>
<subj-group><subject>Organismal Evolution</subject>
<subj-group><subject>Microbial Evolution</subject>
</subj-group>
</subj-group>
</subj-group>
<subj-group><subject>Genomics</subject>
<subj-group><subject>Comparative Genomics</subject>
</subj-group>
</subj-group>
<subj-group><subject>Microbiology</subject>
<subj-group><subject>Bacterial Pathogens</subject>
<subj-group><subject>Gram Positive</subject>
<subject>Streptococci</subject>
</subj-group>
</subj-group>
<subj-group><subject>Bacteriology</subject>
<subj-group><subject>Bacterial Biofilms</subject>
<subject>Bacterial Evolution</subject>
<subject>Bacterial Physiology</subject>
</subj-group>
</subj-group>
<subj-group><subject>Microbial Evolution</subject>
<subject>Microbial Growth and Development</subject>
<subject>Microbial Pathogens</subject>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v2"><subject>Medicine</subject>
<subj-group><subject>Oral Medicine</subject>
<subj-group><subject>Oral Diseases</subject>
</subj-group>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>Phenotypic Heterogeneity of Genomically-Diverse Isolates of <italic>Streptococcus mutans</italic>
</article-title>
<alt-title alt-title-type="running-head">Virulence Properties of a Diverse Caries Pathogen</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Palmer</surname>
<given-names>Sara R.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Miller</surname>
<given-names>James H.</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Abranches</surname>
<given-names>Jacqueline</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>4</sup>
</xref>
<xref ref-type="aff" rid="aff5"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Zeng</surname>
<given-names>Lin</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lefebure</surname>
<given-names>Tristan</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Richards</surname>
<given-names>Vincent P.</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lemos</surname>
<given-names>José A.</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>4</sup>
</xref>
<xref ref-type="aff" rid="aff5"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Stanhope</surname>
<given-names>Michael J.</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Burne</surname>
<given-names>Robert A.</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>Department of Oral Biology, University of Florida, Gainesville, Florida, United States of America</addr-line>
</aff>
<aff id="aff2"><label>2</label>
<addr-line>Université de Lyon, CNRS, Ecologie des Hydrosystèmes Naturels et Anthropisés; Université Lyon, Villeurbanne, France</addr-line>
</aff>
<aff id="aff3"><label>3</label>
<addr-line>Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York, United States of America</addr-line>
</aff>
<aff id="aff4"><label>4</label>
<addr-line>Center for Oral Biology, University of Rochester Medical Center, Rochester, New York, United States of America</addr-line>
</aff>
<aff id="aff5"><label>5</label>
<addr-line>Department of Microbiology and Immunology, University of Rochester Medical Center, Rochester, New York, United States of America</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Biswas</surname>
<given-names>Indranil</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1"><addr-line>University of Kansas Medical Center, United States of America</addr-line>
</aff>
<author-notes><corresp id="cor1">* E-mail: <email>rburne@dental.ufl.edu</email>
</corresp>
<fn fn-type="conflict"><p><bold>Competing Interests: </bold>
Robert A. Burne is a PLOS ONE editorial board member. This does not alter the authors’ adherence to all PLOS ONE policies on sharing data and materials.</p>
</fn>
<fn fn-type="con"><p>Conceived and designed the experiments: SRP LZ JA JL RAB. Performed the experiments: SRP JA JM LZ. Analyzed the data: SRP JA VR LZ RAB TL. Contributed reagents/materials/analysis tools: JL MJS RAB. Wrote the paper: SRP JL JA MJS RAB.</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><year>2013</year>
</pub-date>
<pub-date pub-type="epub"><day>16</day>
<month>4</month>
<year>2013</year>
</pub-date>
<volume>8</volume>
<issue>4</issue>
<elocation-id>e61358</elocation-id>
<history><date date-type="received"><day>26</day>
<month>11</month>
<year>2012</year>
</date>
<date date-type="accepted"><day>7</day>
<month>3</month>
<year>2013</year>
</date>
</history>
<permissions><copyright-year>2013</copyright-year>
<copyright-holder>Palmer et al</copyright-holder>
<license><license-p>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.</license-p>
</license>
</permissions>
<abstract><p>High coverage, whole genome shotgun (WGS) sequencing of 57 geographically- and genetically-diverse isolates of <italic>Streptococcus mutans</italic>
from individuals of known dental caries status was recently completed. Of the 57 sequenced strains, fifteen isolates, were selected based primarily on differences in gene content and phenotypic characteristics known to affect virulence and compared with the reference strain UA159. A high degree of variability in these properties was observed between strains, with a broad spectrum of sensitivities to low pH, oxidative stress (air and paraquat) and exposure to competence stimulating peptide (CSP). Significant differences in autolytic behavior and in biofilm development in glucose or sucrose were also observed. Natural genetic competence varied among isolates, and this was correlated to the presence or absence of competence genes, <italic>comCDE</italic>
and <italic>comX</italic>
, and to bacteriocins. In general strains that lacked the ability to become competent possessed fewer genes for bacteriocins and immunity proteins or contained polymorphic variants of these genes. WGS sequence analysis of the pan-genome revealed, for the first time, components of a Type VII secretion system in several <italic>S. mutans</italic>
strains, as well as two putative ORFs that encode possible collagen binding proteins located upstream of the <italic>cnm</italic>
gene, which is associated with host cell invasiveness. The virulence of these particular strains was assessed in a wax-worm model. This is the first study to combine a comprehensive analysis of key virulence-related phenotypes with extensive genomic analysis of a pathogen that evolved closely with humans. Our analysis highlights the phenotypic diversity of <italic>S. mutans</italic>
isolates and indicates that the species has evolved a variety of adaptive strategies to persist in the human oral cavity and, when conditions are favorable, to initiate disease.</p>
</abstract>
<funding-group><funding-statement>This research was funded by the following NIH grants: NIDAID RO1 AI073368, NIDCR R01 DE013239, and NIDCR T90 DE021990. 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>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>France</li>
<li>États-Unis</li>
</country>
<region><li>Auvergne-Rhône-Alpes</li>
<li>Floride</li>
<li>Rhône-Alpes</li>
<li>État de New York</li>
</region>
<settlement><li>Ithaca (New York)</li>
<li>Lyon</li>
<li>Villeurbanne</li>
</settlement>
<orgName><li>Université Cornell</li>
</orgName>
</list>
<tree><country name="États-Unis"><region name="Floride"><name sortKey="Palmer, Sara R" sort="Palmer, Sara R" uniqKey="Palmer S" first="Sara R." last="Palmer">Sara R. Palmer</name>
</region>
<name sortKey="Abranches, Jacqueline" sort="Abranches, Jacqueline" uniqKey="Abranches J" first="Jacqueline" last="Abranches">Jacqueline Abranches</name>
<name sortKey="Abranches, Jacqueline" sort="Abranches, Jacqueline" uniqKey="Abranches J" first="Jacqueline" last="Abranches">Jacqueline Abranches</name>
<name sortKey="Burne, Robert A" sort="Burne, Robert A" uniqKey="Burne R" first="Robert A." last="Burne">Robert A. Burne</name>
<name sortKey="Lefebure, Tristan" sort="Lefebure, Tristan" uniqKey="Lefebure T" first="Tristan" last="Lefebure">Tristan Lefebure</name>
<name sortKey="Lemos, Jose A" sort="Lemos, Jose A" uniqKey="Lemos J" first="José A." last="Lemos">José A. Lemos</name>
<name sortKey="Lemos, Jose A" sort="Lemos, Jose A" uniqKey="Lemos J" first="José A." last="Lemos">José A. Lemos</name>
<name sortKey="Miller, James H" sort="Miller, James H" uniqKey="Miller J" first="James H." last="Miller">James H. Miller</name>
<name sortKey="Richards, Vincent P" sort="Richards, Vincent P" uniqKey="Richards V" first="Vincent P." last="Richards">Vincent P. Richards</name>
<name sortKey="Stanhope, Michael J" sort="Stanhope, Michael J" uniqKey="Stanhope M" first="Michael J." last="Stanhope">Michael J. Stanhope</name>
<name sortKey="Zeng, Lin" sort="Zeng, Lin" uniqKey="Zeng L" first="Lin" last="Zeng">Lin Zeng</name>
</country>
<country name="France"><region name="Auvergne-Rhône-Alpes"><name sortKey="Lefebure, Tristan" sort="Lefebure, Tristan" uniqKey="Lefebure T" first="Tristan" last="Lefebure">Tristan Lefebure</name>
</region>
</country>
</tree>
</affiliations>
</record>
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