Evolution of Cariogenic Character in Streptococcus mutans: Horizontal Transmission of Glycosyl Hydrolase Family 70 Genes
Identifieur interne : 000B97 ( Ncbi/Merge ); précédent : 000B96; suivant : 000B98Evolution of Cariogenic Character in Streptococcus mutans: Horizontal Transmission of Glycosyl Hydrolase Family 70 Genes
Auteurs : Tomonori Hoshino [Japon] ; Taku Fujiwara [Japon] ; Shigetada Kawabata [Japon]Source :
- Scientific Reports [ 2045-2322 ] ; 2012.
Abstract
Acquisition of the ability to produce polysaccharides from sucrose, i.e. the
Url:
DOI: 10.1038/srep00518
PubMed: 22816041
PubMed Central: 3399136
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Evolution of Cariogenic Character in <italic>Streptococcus mutans</italic>
: Horizontal Transmission of Glycosyl Hydrolase Family 70 Genes</title>
<author><name sortKey="Hoshino, Tomonori" sort="Hoshino, Tomonori" uniqKey="Hoshino T" first="Tomonori" last="Hoshino">Tomonori Hoshino</name>
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<author><name sortKey="Fujiwara, Taku" sort="Fujiwara, Taku" uniqKey="Fujiwara T" first="Taku" last="Fujiwara">Taku Fujiwara</name>
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<author><name sortKey="Kawabata, Shigetada" sort="Kawabata, Shigetada" uniqKey="Kawabata S" first="Shigetada" last="Kawabata">Shigetada Kawabata</name>
<affiliation wicri:level="1"><nlm:aff id="a2"><institution>Department of Oral and Molecular Microbiology, Osaka University Graduate School of Dentistry</institution>
, 1–8 Yamadaoka, Suita, Osaka 565-0871,<country>Japan</country>
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<country xml:lang="fr">Japon</country>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Evolution of Cariogenic Character in <italic>Streptococcus mutans</italic>
: Horizontal Transmission of Glycosyl Hydrolase Family 70 Genes</title>
<author><name sortKey="Hoshino, Tomonori" sort="Hoshino, Tomonori" uniqKey="Hoshino T" first="Tomonori" last="Hoshino">Tomonori Hoshino</name>
<affiliation wicri:level="1"><nlm:aff id="a1"><institution>Department of Pediatric Dentistry, Nagasaki University Graduate School of Biomedical Sciences</institution>
, 1-7-1 Sakamoto, Nagasaki 852-8588,<country>Japan</country>
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<country xml:lang="fr">Japon</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<author><name sortKey="Fujiwara, Taku" sort="Fujiwara, Taku" uniqKey="Fujiwara T" first="Taku" last="Fujiwara">Taku Fujiwara</name>
<affiliation wicri:level="1"><nlm:aff id="a1"><institution>Department of Pediatric Dentistry, Nagasaki University Graduate School of Biomedical Sciences</institution>
, 1-7-1 Sakamoto, Nagasaki 852-8588,<country>Japan</country>
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<country xml:lang="fr">Japon</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<author><name sortKey="Kawabata, Shigetada" sort="Kawabata, Shigetada" uniqKey="Kawabata S" first="Shigetada" last="Kawabata">Shigetada Kawabata</name>
<affiliation wicri:level="1"><nlm:aff id="a2"><institution>Department of Oral and Molecular Microbiology, Osaka University Graduate School of Dentistry</institution>
, 1–8 Yamadaoka, Suita, Osaka 565-0871,<country>Japan</country>
</nlm:aff>
<country xml:lang="fr">Japon</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<series><title level="j">Scientific Reports</title>
<idno type="eISSN">2045-2322</idno>
<imprint><date when="2012">2012</date>
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<front><div type="abstract" xml:lang="en"><p>Acquisition of the ability to produce polysaccharides from sucrose, i.e. the <italic>gtf</italic>
gene encoding glucosyltransferase (GTF), is the key evolutionary event enabling dental biofilm formation by streptococci. To clarify the ancestry of streptococcal GTFs, time of its occurrence, and order of specific events, we investigated the distribution of GTFs among bacteria by phylogenetic analysis of the glycosyl hydrolase family 70 enzymes. We found that streptococcal GTFs were derived from other lactic acid bacteria such as <italic>Lactobacillus</italic>
and <italic>Leuconostoc,</italic>
and propose the following evolutionary model: horizontal gene transfer via transposons occurred when streptococci encountered lactic acid bacteria contained in fermented food. Intra-genomic gene duplication occurred by a secondary selection pressure such as consumption of refined sugar. Our findings concerning this evolution in <italic>Streptococcus mutans</italic>
provide an important background for studies of the relationship between the historical spread of dental caries and anthropological factors.</p>
</div>
</front>
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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">Sci Rep</journal-id>
<journal-id journal-id-type="iso-abbrev">Sci Rep</journal-id>
<journal-title-group><journal-title>Scientific Reports</journal-title>
</journal-title-group>
<issn pub-type="epub">2045-2322</issn>
<publisher><publisher-name>Nature Publishing Group</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">22816041</article-id>
<article-id pub-id-type="pmc">3399136</article-id>
<article-id pub-id-type="pii">srep00518</article-id>
<article-id pub-id-type="doi">10.1038/srep00518</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Evolution of Cariogenic Character in <italic>Streptococcus mutans</italic>
: Horizontal Transmission of Glycosyl Hydrolase Family 70 Genes</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Hoshino</surname>
<given-names>Tomonori</given-names>
</name>
<xref ref-type="aff" rid="a1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Fujiwara</surname>
<given-names>Taku</given-names>
</name>
<xref ref-type="corresp" rid="c1">a</xref>
<xref ref-type="aff" rid="a1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kawabata</surname>
<given-names>Shigetada</given-names>
</name>
<xref ref-type="aff" rid="a2">2</xref>
</contrib>
<aff id="a1"><label>1</label>
<institution>Department of Pediatric Dentistry, Nagasaki University Graduate School of Biomedical Sciences</institution>
, 1-7-1 Sakamoto, Nagasaki 852-8588,<country>Japan</country>
</aff>
<aff id="a2"><label>2</label>
<institution>Department of Oral and Molecular Microbiology, Osaka University Graduate School of Dentistry</institution>
, 1–8 Yamadaoka, Suita, Osaka 565-0871,<country>Japan</country>
</aff>
</contrib-group>
<author-notes><corresp id="c1"><label>a</label>
<email>takufuji@nagasaki-u.ac.jp</email>
</corresp>
</author-notes>
<pub-date pub-type="epub"><day>18</day>
<month>07</month>
<year>2012</year>
</pub-date>
<pub-date pub-type="collection"><year>2012</year>
</pub-date>
<volume>2</volume>
<elocation-id>518</elocation-id>
<history><date date-type="received"><day>04</day>
<month>05</month>
<year>2012</year>
</date>
<date date-type="accepted"><day>03</day>
<month>07</month>
<year>2012</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2012, Macmillan Publishers Limited. All rights reserved</copyright-statement>
<copyright-year>2012</copyright-year>
<copyright-holder>Macmillan Publishers Limited. All rights reserved</copyright-holder>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by-nc-sa/3.0/"><pmc-comment>author-paid</pmc-comment>
<license-p>This work is licensed under a Creative Commons Attribution-NonCommercial-ShareALike 3.0 Unported License. To view a copy of this license, visit <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by-nc-sa/3.0/">http://creativecommons.org/licenses/by-nc-sa/3.0/</ext-link>
</license-p>
</license>
</permissions>
<abstract><p>Acquisition of the ability to produce polysaccharides from sucrose, i.e. the <italic>gtf</italic>
gene encoding glucosyltransferase (GTF), is the key evolutionary event enabling dental biofilm formation by streptococci. To clarify the ancestry of streptococcal GTFs, time of its occurrence, and order of specific events, we investigated the distribution of GTFs among bacteria by phylogenetic analysis of the glycosyl hydrolase family 70 enzymes. We found that streptococcal GTFs were derived from other lactic acid bacteria such as <italic>Lactobacillus</italic>
and <italic>Leuconostoc,</italic>
and propose the following evolutionary model: horizontal gene transfer via transposons occurred when streptococci encountered lactic acid bacteria contained in fermented food. Intra-genomic gene duplication occurred by a secondary selection pressure such as consumption of refined sugar. Our findings concerning this evolution in <italic>Streptococcus mutans</italic>
provide an important background for studies of the relationship between the historical spread of dental caries and anthropological factors.</p>
</abstract>
</article-meta>
</front>
<floats-group><fig id="f1"><label>Figure 1</label>
<caption><title>Phylogenetic analysis of glycosyl hydrolase family 70 enzymes.</title>
<p>A phylogenetic tree of the amino acid sequences of glycosyl hydrolase family 70 enzymes was constructed using the maximum parsimony (MP) method. Genes bracketed with bold lines are adjacent to each other in the bacterial genome. The value on each branch is the estimated confidence limit (expressed as a percentage) for the position of the branches, as determined by bootstrap analysis. Only values exceeding 50% are shown.</p>
</caption>
<graphic xlink:href="srep00518-f1"></graphic>
</fig>
<fig id="f2"><label>Figure 2</label>
<caption><title>Schema of sequences surrounding the <italic>gtf</italic>
gene.</title>
<p>(A) Genomic location mapping of the <italic>gtf</italic>
gene. (a) <italic>gtf</italic>
180 from <italic>Lcb. reuteri</italic>
, (b) <italic>gtf</italic>
Kg15 from <italic>Lcb. sakei</italic>
, (c) <italic>gtfR</italic>
from <italic>Str. oralis</italic>
, (d) <italic>gtfB and gtfC</italic>
from <italic>Str. mutans</italic>
, and (e) <italic>gtfD</italic>
from <italic>Str. mutans.</italic>
(B) Sequence of the transposase-homologous downstream of <italic>gtfR</italic>
. The region enclosed by the broken line in A (c) is shown in detail in B. FR00720602 and AE007317 are NCBI accession number of <italic>Str. oralis</italic>
Uo5 and <italic>Str. pneumoniae</italic>
R6 genome, respectively. The number after the accession number indicates the location in the genome.</p>
</caption>
<graphic xlink:href="srep00518-f2"></graphic>
</fig>
<fig id="f3"><label>Figure 3</label>
<caption><title>Phylogenetic analysis of the functional regions of streptococcal GTF.</title>
<p>Phylogenetic trees based on the gene encoding the catalytic region (A), the deduced amino acid sequence of the catalytic region (B), the gene encoding the first unit of the glucan-binding region constructed of 6 direct repeat units (C), and the deduced amino acid sequence of the first unit of the glucan-binding region were constructed by the neighbor-joining (NJ) method. In A and B, the streptococcal <italic>gtf</italic>
gene family can be classified into 3 clusters: the water-soluble glucan synthesizing group (WSG), the water-insoluble glucan synthesizing group (WIG), and the intermediate group (INT). In D, GTFs from same or closely related species could be divided into the same cluster. The value on each branch is the estimated confidence limit (expressed as a percentage) for the position of the branches, as determined by bootstrap analysis. Only values exceeding 50% are shown. The scale bar ([NJ] distance) represents a 5% difference in nucleotide sequence.</p>
</caption>
<graphic xlink:href="srep00518-f3"></graphic>
</fig>
<fig id="f4"><label>Figure 4</label>
<caption><title>Hypothetical model of GTF enzyme acquisition by oral <italic>Streptococci</italic>
.</title>
<p>The genus <italic>Streptococcus</italic>
acquired the <italic>gtf</italic>
gene via horizontal gene transfer when it encountered lactic acid bacteria, such as <italic>Lactobacillus</italic>
and <italic>Leuconostoc,</italic>
in the human oral cavity. This event coincided with the introduction of fermented foods into the human diet, which was brought about by the development of agricultural practices and food preservation methods.</p>
</caption>
<graphic xlink:href="srep00518-f4"></graphic>
</fig>
<table-wrap position="float" id="t1"><label>Table 1</label>
<caption><title>Mean phylogenetic distances (lower triangle) and standard error (upper triangle) of the catalytic regions among <italic>Lcb. reuteri</italic>
GTFB (LR GTFB), streptococcal GTF groups, and 3 <italic>gtf</italic>
genes from <italic>Str. mutans</italic>
</title>
</caption>
<table frame="hsides" rules="groups" border="1"><colgroup><col align="left"></col>
<col align="center"></col>
<col align="center"></col>
<col align="center"></col>
<col align="center"></col>
<col align="center"></col>
<col align="center"></col>
<col align="center"></col>
</colgroup>
<thead valign="bottom"><tr><th align="left" valign="top" charoff="50"> </th>
<th align="justify" valign="top" charoff="50">root</th>
<th align="justify" valign="top" charoff="50">WSG</th>
<th align="justify" valign="top" charoff="50">WIG</th>
<th align="justify" valign="top" charoff="50">INT</th>
<th align="justify" valign="top" charoff="50"><italic>gtfB</italic>
</th>
<th align="justify" valign="top" charoff="50"><italic>gtfC</italic>
</th>
<th align="justify" valign="top" charoff="50"><italic>gtfD</italic>
</th>
</tr>
</thead>
<tbody valign="top"><tr><td align="justify" valign="top" charoff="50">LR GTFB</td>
<td align="left" valign="top" charoff="50"> </td>
<td align="justify" valign="top" charoff="50">0.020</td>
<td align="justify" valign="top" charoff="50">0.021</td>
<td align="justify" valign="top" charoff="50">0.019</td>
<td align="justify" valign="top" charoff="50">0.024</td>
<td align="justify" valign="top" charoff="50">0.024</td>
<td align="justify" valign="top" charoff="50">0.024</td>
</tr>
<tr><td align="justify" valign="top" charoff="50">WSG</td>
<td align="justify" valign="top" charoff="50">0.558</td>
<td align="left" valign="top" charoff="50"> </td>
<td align="justify" valign="top" charoff="50">0.015</td>
<td align="justify" valign="top" charoff="50">0.014</td>
<td align="left" valign="top" charoff="50"> </td>
<td align="left" valign="top" charoff="50"> </td>
<td align="left" valign="top" charoff="50"> </td>
</tr>
<tr><td align="justify" valign="top" charoff="50">WIG</td>
<td align="justify" valign="top" charoff="50">0.555</td>
<td align="justify" valign="top" charoff="50">0.366</td>
<td align="left" valign="top" charoff="50"> </td>
<td align="justify" valign="top" charoff="50">0.015</td>
<td align="left" valign="top" charoff="50"> </td>
<td align="left" valign="top" charoff="50"> </td>
<td align="left" valign="top" charoff="50"> </td>
</tr>
<tr><td align="justify" valign="top" charoff="50">INT</td>
<td align="justify" valign="top" charoff="50">0.571</td>
<td align="justify" valign="top" charoff="50">0.393</td>
<td align="justify" valign="top" charoff="50">0.381</td>
<td align="left" valign="top" charoff="50"> </td>
<td align="left" valign="top" charoff="50"> </td>
<td align="left" valign="top" charoff="50"> </td>
<td align="left" valign="top" charoff="50"> </td>
</tr>
<tr><td align="justify" valign="top" charoff="50"><italic>gtfB</italic>
</td>
<td align="justify" valign="top" charoff="50">0.539</td>
<td align="left" valign="top" charoff="50"> </td>
<td align="left" valign="top" charoff="50"> </td>
<td align="left" valign="top" charoff="50"> </td>
<td align="left" valign="top" charoff="50"> </td>
<td align="justify" valign="top" charoff="50">0.017</td>
<td align="justify" valign="top" charoff="50">0.021</td>
</tr>
<tr><td align="justify" valign="top" charoff="50"><italic>gtfC</italic>
</td>
<td align="justify" valign="top" charoff="50">0.560</td>
<td align="left" valign="top" charoff="50"> </td>
<td align="left" valign="top" charoff="50"> </td>
<td align="left" valign="top" charoff="50"> </td>
<td align="justify" valign="top" charoff="50">0.144</td>
<td align="left" valign="top" charoff="50"> </td>
<td align="justify" valign="top" charoff="50">0.022</td>
</tr>
<tr><td align="justify" valign="top" charoff="50"><italic>gtfD</italic>
</td>
<td align="justify" valign="top" charoff="50">0.537</td>
<td align="left" valign="top" charoff="50"> </td>
<td align="left" valign="top" charoff="50"> </td>
<td align="left" valign="top" charoff="50"> </td>
<td align="justify" valign="top" charoff="50">0.397</td>
<td align="justify" valign="top" charoff="50">0.338</td>
<td align="left" valign="top" charoff="50"> </td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn id="t1-fn1"><p>Abbreviations: WSG, water-soluble glucan-synthesizing group; WIG, water-insoluble glucan synthesizing group; INT, intermediate group (INT).</p>
</fn>
</table-wrap-foot>
</table-wrap>
</floats-group>
</pmc>
<affiliations><list><country><li>Japon</li>
</country>
</list>
<tree><country name="Japon"><noRegion><name sortKey="Hoshino, Tomonori" sort="Hoshino, Tomonori" uniqKey="Hoshino T" first="Tomonori" last="Hoshino">Tomonori Hoshino</name>
</noRegion>
<name sortKey="Fujiwara, Taku" sort="Fujiwara, Taku" uniqKey="Fujiwara T" first="Taku" last="Fujiwara">Taku Fujiwara</name>
<name sortKey="Kawabata, Shigetada" sort="Kawabata, Shigetada" uniqKey="Kawabata S" first="Shigetada" last="Kawabata">Shigetada Kawabata</name>
</country>
</tree>
</affiliations>
</record>
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