Global biogeography of SAR11 marine bacteria
Identifieur interne : 000338 ( Ncbi/Merge ); précédent : 000337; suivant : 000339Global biogeography of SAR11 marine bacteria
Auteurs : Mark V. Brown [Australie] ; Federico M. Lauro [Australie] ; Matthew Z. Demaere [Australie] ; Les Muir [Australie] ; David Wilkins [Australie] ; Torsten Thomas [Australie] ; Martin J. Riddle [Australie] ; Jed A. Fuhrman [États-Unis] ; Cynthia Andrews-Pfannkoch [États-Unis] ; Jeffrey M. Hoffman [États-Unis] ; Jeffrey B. Mcquaid [États-Unis] ; Andrew Allen [États-Unis] ; Stephen R. Rintoul [Australie] ; Ricardo Cavicchioli [Australie]Source :
- Molecular Systems Biology [ 1744-4292 ] ; 2012.
Abstract
Metagenomic samples from oceans around the globe were used to examine the biogeography of the dominant marine heterotrophic bacterial clade, SAR11. Analysis uncovers evidence of adaptive radiation in response to environmental parameters, particularly temperature.
Url:
DOI: 10.1038/msb.2012.28
PubMed: 22806143
PubMed Central: 3421443
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<author><name sortKey="Andrews Pfannkoch, Cynthia" sort="Andrews Pfannkoch, Cynthia" uniqKey="Andrews Pfannkoch C" first="Cynthia" last="Andrews-Pfannkoch">Cynthia Andrews-Pfannkoch</name>
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<front><div type="abstract" xml:lang="en"><p>Metagenomic samples from oceans around the globe were used to examine the biogeography of the dominant marine heterotrophic bacterial clade, SAR11. Analysis uncovers evidence of adaptive radiation in response to environmental parameters, particularly temperature.</p>
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<biblStruct><analytic><author><name sortKey="Wilhelm, Lj" uniqKey="Wilhelm L">LJ Wilhelm</name>
</author>
<author><name sortKey="Tripp, Hj" uniqKey="Tripp H">HJ Tripp</name>
</author>
<author><name sortKey="Givan, Sa" uniqKey="Givan S">SA Givan</name>
</author>
<author><name sortKey="Smith, Dp" uniqKey="Smith D">DP Smith</name>
</author>
<author><name sortKey="Giovannoni, Sj" uniqKey="Giovannoni S">SJ Giovannoni</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Williams, Tj" uniqKey="Williams T">TJ Williams</name>
</author>
<author><name sortKey="Burg, Dw" uniqKey="Burg D">DW Burg</name>
</author>
<author><name sortKey="Ertan, H" uniqKey="Ertan H">H Ertan</name>
</author>
<author><name sortKey="Raferty, Mj" uniqKey="Raferty M">MJ Raferty</name>
</author>
<author><name sortKey="Poljak, A" uniqKey="Poljak A">A Poljak</name>
</author>
<author><name sortKey="Guilhaus, M" uniqKey="Guilhaus M">M Guilhaus</name>
</author>
<author><name sortKey="Pilak, O" uniqKey="Pilak O">O Pilak</name>
</author>
<author><name sortKey="Cavicchioli, R" uniqKey="Cavicchioli R">R Cavicchioli</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Yang, Z" uniqKey="Yang Z">Z Yang</name>
</author>
</analytic>
</biblStruct>
</listBibl>
</div1>
</back>
</TEI>
<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Mol Syst Biol</journal-id>
<journal-id journal-id-type="iso-abbrev">Mol. Syst. Biol</journal-id>
<journal-title-group><journal-title>Molecular Systems Biology</journal-title>
</journal-title-group>
<issn pub-type="epub">1744-4292</issn>
<publisher><publisher-name>Nature Publishing Group</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">22806143</article-id>
<article-id pub-id-type="pmc">3421443</article-id>
<article-id pub-id-type="pii">msb201228</article-id>
<article-id pub-id-type="doi">10.1038/msb.2012.28</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Global biogeography of SAR11 marine bacteria</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Brown</surname>
<given-names>Mark V</given-names>
</name>
<xref ref-type="aff" rid="a1">1</xref>
<xref ref-type="aff" rid="a2">2</xref>
<xref ref-type="author-notes" rid="n1">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lauro</surname>
<given-names>Federico M</given-names>
</name>
<xref ref-type="aff" rid="a1">1</xref>
<xref ref-type="author-notes" rid="n1">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>DeMaere</surname>
<given-names>Matthew Z</given-names>
</name>
<xref ref-type="aff" rid="a1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Muir</surname>
<given-names>Les</given-names>
</name>
<xref ref-type="aff" rid="a3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wilkins</surname>
<given-names>David</given-names>
</name>
<xref ref-type="aff" rid="a1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Thomas</surname>
<given-names>Torsten</given-names>
</name>
<xref ref-type="aff" rid="a1">1</xref>
<xref ref-type="aff" rid="a4">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Riddle</surname>
<given-names>Martin J</given-names>
</name>
<xref ref-type="aff" rid="a5">5</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Fuhrman</surname>
<given-names>Jed A</given-names>
</name>
<xref ref-type="aff" rid="a6">6</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Andrews-Pfannkoch</surname>
<given-names>Cynthia</given-names>
</name>
<xref ref-type="aff" rid="a7">7</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hoffman</surname>
<given-names>Jeffrey M</given-names>
</name>
<xref ref-type="aff" rid="a7">7</xref>
</contrib>
<contrib contrib-type="author"><name><surname>McQuaid</surname>
<given-names>Jeffrey B</given-names>
</name>
<xref ref-type="aff" rid="a7">7</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Allen</surname>
<given-names>Andrew</given-names>
</name>
<xref ref-type="aff" rid="a7">7</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Rintoul</surname>
<given-names>Stephen R</given-names>
</name>
<xref ref-type="aff" rid="a8">8</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Cavicchioli</surname>
<given-names>Ricardo</given-names>
</name>
<xref ref-type="corresp" rid="c1">a</xref>
<xref ref-type="aff" rid="a1">1</xref>
</contrib>
<aff id="a1"><label>1</label>
<institution>School of Biotechnology and Biomolecular Sciences, The University of New South Wales</institution>
, Sydney, New South Wales,<country>Australia</country>
</aff>
<aff id="a2"><label>2</label>
<institution>Evolution and Ecology Research Centre, The University of New South Wales</institution>
, Sydney, New South Wales,<country>Australia</country>
</aff>
<aff id="a3"><label>3</label>
<institution>CSIRO Marine and Atmospheric Research, Castray Esplanade</institution>
, Hobart, Tasmania,<country>Australia</country>
</aff>
<aff id="a4"><label>4</label>
<institution>Centre for Marine Bio-Innovation, The University of New South Wales</institution>
, Sydney, New South Wales,<country>Australia</country>
</aff>
<aff id="a5"><label>5</label>
<institution>Australian Antarctic Division, Channel Highway</institution>
, Kingston, Tasmania,<country>Australia</country>
</aff>
<aff id="a6"><label>6</label>
<institution>Department of Biological Sciences, Wrigley Institute for Environmental Studies, University of Southern California</institution>
, Los Angeles, CA,<country>USA</country>
</aff>
<aff id="a7"><label>7</label>
<institution>J. Craig Venter Institute</institution>
, Rockville, MD,<country>USA</country>
</aff>
<aff id="a8"><label>8</label>
<institution>CSIRO Marine and Atmospheric Research, Centre for Australian Weather and Climate Research—A partnership of the Bureau of Meteorology and CSIRO, and CSIRO Wealth from Oceans National Research Flagship, and the Antarctic Climate and Ecosystems Cooperative Research Centre, Castray Esplanade</institution>
, Hobart, Tasmania,<country>Australia</country>
</aff>
</contrib-group>
<author-notes><corresp id="c1"><label>a</label>
<institution>School of Biotechnology and Biomolecular Sciences, The University of New South Wales</institution>
, Sydney, New South Wales 2052, <country>Australia</country>
. Tel.: +61 2 9385 3516; Fax: +61 2 9385 2742; <email>r.cavicchioli@unsw.edu.au</email>
</corresp>
<fn id="n1"><label>*</label>
<p>These authors contributed equally to this work</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><year>2012</year>
</pub-date>
<pub-date pub-type="epub"><day>17</day>
<month>07</month>
<year>2012</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>17</day>
<month>07</month>
<year>2012</year>
</pub-date>
<volume>8</volume>
<fpage>595</fpage>
<lpage>595</lpage>
<history><date date-type="received"><day>15</day>
<month>03</month>
<year>2012</year>
</date>
<date date-type="accepted"><day>18</day>
<month>06</month>
<year>2012</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2012, EMBO and Macmillan Publishers Limited</copyright-statement>
<copyright-year>2012</copyright-year>
<copyright-holder>EMBO and Macmillan Publishers Limited</copyright-holder>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by-nc-nd/3.0/"><pmc-comment>author-paid</pmc-comment>
<license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution Noncommercial No Derivative Works 3.0 Unported License, which permits distribution and reproduction in any medium, provided the original author and source are credited. This license does not permit commercial exploitation or the creation of derivative works without specific permission.</license-p>
</license>
</permissions>
<abstract abstract-type="hidden-editorial-summary"><p>Metagenomic samples from oceans around the globe were used to examine the biogeography of the dominant marine heterotrophic bacterial clade, SAR11. Analysis uncovers evidence of adaptive radiation in response to environmental parameters, particularly temperature.</p>
</abstract>
<abstract abstract-type="hidden-synopsis"><p><disp-formula id="illus1"><graphic xlink:href="msb201228-i1.jpg"></graphic>
</disp-formula>
</p>
<p><list id="l1" list-type="bullet"><list-item><p>By generating 37 new Antarctic metagenomes and analysing the internal transcribed spacer (ITS) regions of the SAR11 clade in a total of 128 surface marine metagenomes, we identified phylotype distributions that strongly correlated with temperature and latitude.</p>
</list-item>
<list-item><p>By assembling SAR11 genomes from Antarctic metagenome data, we identified specific genes, biases in gene functions and signatures of positive selection in the genomes of the polar SAR11—genomic signatures of adaptive radiation.</p>
</list-item>
<list-item><p>Our data demonstrate the importance of adaptive radiation in an organism's ability to proliferate throughout the world's oceans, and describe genomic traits characteristic of different phylotypes in specific marine biomes.</p>
</list-item>
<list-item><p>These bacteria are important marine heterotrophs and have a fundamental role in oceanic nutrient cycling. These findings, therefore, have important implications for our ability to predict how changes in ocean temperature may affect bacterial ecology.</p>
</list-item>
</list>
</p>
</abstract>
<abstract><p>The ubiquitous SAR11 bacterial clade is the most abundant type of organism in the world's oceans, but the reasons for its success are not fully elucidated. We analysed 128 surface marine metagenomes, including 37 new Antarctic metagenomes. The large size of the data set enabled internal transcribed spacer (ITS) regions to be obtained from the Southern polar region, enabling the first global characterization of the distribution of SAR11, from waters spanning temperatures −2 to 30°C. Our data show a stable co-occurrence of phylotypes within both ‘tropical' (>20°C) and ‘polar' (<10°C) biomes, highlighting ecological niche differentiation between major SAR11 subgroups. All phylotypes display transitions in abundance that are strongly correlated with temperature and latitude. By assembling SAR11 genomes from Antarctic metagenome data, we identified specific genes, biases in gene functions and signatures of positive selection in the genomes of the polar SAR11—genomic signatures of adaptive radiation. Our data demonstrate the importance of adaptive radiation in the organism's ability to proliferate throughout the world's oceans, and describe genomic traits characteristic of different phylotypes in specific marine biomes.</p>
</abstract>
<kwd-group><kwd>adaptive radiation</kwd>
<kwd>Antarctica</kwd>
<kwd>metagenome</kwd>
<kwd>Pelagibacter</kwd>
<kwd>phylotype distribution</kwd>
</kwd-group>
</article-meta>
</front>
<floats-group><fig id="f1"><label>Figure 1</label>
<caption><p>Phylogeny and temperature association with the biogeographic distribution of the SAR11 clade. ARB neighbour-joining trees generated by collapsing significant nodes in trees generated from representative 16S rRNA gene sequences (subgroups), and ITS sequences (phylotypes). Individual clones not included in triangulated clusters maintain the conserved motif of P1a.1 but have several base-pair deletions. These 14 sequences are designated as belonging to phylotype P1a.1 in our database. Expanded trees are shown in <xref ref-type="supplementary-material" rid="S1">Supplementary Figure S1</xref>
. The four lower graphs show relative contributions of the SAR11 phylotypes (coloured as for the ITS tree) to total SAR11 composition revealing phylotype distribution that closely relates to temperature. The data bars are arranged along the <italic>x</italic>
axis according to increasing temperature of the sampling location for each metagenome (from left to right), with relative phylotype abundance shown on the left <italic>y</italic>
axis and environmental temperature (indicated by black diamonds) shown on the right <italic>y</italic>
axis in °C.</p>
</caption>
<graphic xlink:href="msb201228-f1"></graphic>
</fig>
<fig id="f2"><label>Figure 2</label>
<caption><p>Clustering and geolocation of ocean samples based on SAR11 phylotype composition. (<bold>A</bold>
) dbRDA ordination for the fitted model of SAR11 ITS phylotype composition data (based on Bray-Curtis similarity after square root transformation of abundances) versus environmental variables. Clustering illustrates the strong separation of samples related to temperature bins <10°C (open circles), 10–20°C (black triangles) and >20°C (grey squares). (<bold>B</bold>
) Identical plot to (A), with sample icons changed to reflect the ‘coastal' (grey triangles) or ‘open ocean' (open squares) affiliation of each sample. (<bold>C</bold>
) Eigen vectors indicating the strength and direction of correlation for each environmental variable from (A). (<bold>D</bold>
) Eigen vectors indicating the strength and direction of correlation for each SAR11 phylotype from (A). (<bold>E</bold>
) nMDS based on between sample Bray-Curtis similarities calculated using square root transformed SAR11 community composition and abundance data (2D stress: 0.07). Clusters are coloured based on membership to groups identified as having >60% similarity in community composition (marked by green rings). Group number (1) blue diamonds, samples from polar regions; (2) light blue squares, temperate regions; (3) red triangles, tropical regions; (4) green triangles, Western Channel Observatory (UK), Monterey Bay (USA) and Botany Bay (Australia); (5) fuschia dots, Chesapeake Bay, Delaware Bay and nearby Nags Head; (6) black ‘x', GS037 and S_35139 (tropical Pacific Ocean) and NASB_179_2 and NASB_174_2 (Sargasso Sea) (contain only ‘tropical' phylotype P1a.3); (7) grey cross, Mont_bay_3 (contains only phylotype P2.1); (8) pink square, NASB-179_1 (Sargasso Sea) (contains only phylotype P1b). (<bold>F</bold>
) Geolocation of the groups shown in (E), depicted by stars (as coloured in E).</p>
</caption>
<graphic xlink:href="msb201228-f2"></graphic>
</fig>
<fig id="f3"><label>Figure 3</label>
<caption><p>Genome synteny and recruitment plots of SAR11 genomes. Whole genome alignments between genomes belonging to different SAR11 phylotypes: HIMB114 (P3.1), ACE_P3.2 (P3.2), HTCC1062 (P1a.1), ACE_P1a.1 (P1a.1) and HTCC7211 (P1a.3). In the synteny plots matches to the +strand (i.e., +/+) are in red, and matches to the −strand (i.e., +/−) in blue. blastn (run with standard parameters and the -m8 flag) matches of at least 30 nucleotides or longer are displayed. Interleaved among the synteny plots are the recruitments, with read-depth shown on a natural logarithmic scale, for each genome against representative metagenomes from Ace Lake (GS232, grey), polar (GS362, purple), temperate (GS368, orange) and tropical (S_35155+S_35163, red) zones. The recruitment appears mainly orange in colour for HIMB114 (P3.1) and HTCC7211 (P1a.3) because these genomes recruit more strongly to the temperate metagenomes, whereas the recruitment for ACE_P3.2 (P3.2) and ACE_P1a.1 (P1a.1) is mainly grey reflecting their origin and high numerical abundance in Ace lake. Black arrows show examples of regions with low recruitment.</p>
</caption>
<graphic xlink:href="msb201228-f3"></graphic>
</fig>
<fig id="f4"><label>Figure 4</label>
<caption><p>COG composition of genes specific, paralogous and positively selected in the polar SAR11 genomes. The pie chart represents the proportion of genes with (blue) or without (red) matches to the COG database. The matching genes were assigned to COG categories (from top to bottom): E—Amino-acid transport and metabolism (maroon); G—Carbohydrate transport and metabolism (green); M—Cell wall/membrane/envelope biogenesis (orange); H—Coenzyme transport and metabolism (violet); V—Defense mechanism (yellow); C—Energy production and conversion (dark blue); S—Function unknown (light green-grey); R—General function prediction only (dark purple); P—Inorganic ion transport and metabolism (light blue); K—Transcription (pink); J—Translation, ribosomal structure and biogenesis (salmon); Q—Secondary metabolites biosynthesis, transport and catabolism (light blue-grey); Other categories (light brown). An asterisk denotes the categories found to be statistically overrepresented when compared with the genome background.</p>
</caption>
<graphic xlink:href="msb201228-f4"></graphic>
</fig>
<fig id="f5"><label>Figure 5</label>
<caption><p>dN/dS ratios over the length of selected protein alignments, and genome synteny between phylotype P3.2 polar strains. (<bold>A</bold>
) Putative porin (ACE_P1a.1 feature: 167717860). (<inline-formula id="d32e1535"><inline-graphic id="d32e1536" xlink:href="msb201228-m1.jpg"></inline-graphic>
</inline-formula>
) dN/dS ratio over 60 codon sliding window, (<inline-formula id="d32e1538"><inline-graphic id="d32e1539" xlink:href="msb201228-m2.jpg"></inline-graphic>
</inline-formula>
) Hydrophobicity index, (<inline-formula id="d32e1541"><inline-graphic id="d32e1542" xlink:href="msb201228-m3.jpg"></inline-graphic>
</inline-formula>
) Antigenicity index. (<bold>B</bold>
) Putative porin (ACE_P3.2 feature: 167933090). (<inline-formula id="d32e1548"><inline-graphic id="d32e1549" xlink:href="msb201228-m4.jpg"></inline-graphic>
</inline-formula>
) dN/dS ratio over 60 codon sliding window, (<inline-formula id="d32e1551"><inline-graphic id="d32e1552" xlink:href="msb201228-m5.jpg"></inline-graphic>
</inline-formula>
) Hydrophobicity index (<inline-formula id="d32e1554"><inline-graphic id="d32e1555" xlink:href="msb201228-m6.jpg"></inline-graphic>
</inline-formula>
), Antigenicity index. (<bold>C</bold>
) dN/dS ratio over a 60 codon sliding window for the FtsZ of ACE_P1a.1 (blue; feature: 167713888) and ACE_P3.2 (red; feature: 167824744). (<bold>D</bold>
) dN/dS ratio over a 60 codon sliding window for lipid A biosynthesis lauroyl/palmitoleoyl acyltransferase of ACE_P1a.1 (blue; feature: 167719320) and ACE_P3.2 (red; feature: 167824936). (<bold>E</bold>
) Genome synteny between ACE_P1a.1 mosaic genome (as depicted in <xref ref-type="fig" rid="f3">Figure 3</xref>
), Arctic IMCC9063, and ACE_P3.2 scaffolds rearranged according to the structure of the IMCC9063 genome (bottom).</p>
</caption>
<graphic xlink:href="msb201228-f5"></graphic>
</fig>
<table-wrap position="float" id="t1"><label>Table 1</label>
<caption><title>Classification hierarchy of the SAR11 clade based on 16S rRNA gene subgroup and ITS phylotype analysis used in this study</title>
</caption>
<table frame="hsides" rules="groups" border="1"><colgroup><col align="left"></col>
<col align="left"></col>
<col align="left"></col>
<col align="left"></col>
<col align="left"></col>
<col align="left"></col>
</colgroup>
<thead valign="bottom"><tr><th align="left" valign="top" charoff="50">Subgroup (16S rRNA gene)</th>
<th align="left" valign="top" charoff="50">Designation origin</th>
<th align="left" valign="top" charoff="50">Phylotype (ITS)</th>
<th align="left" valign="top" charoff="50">Designation origin</th>
<th align="left" valign="top" charoff="50">Isolate</th>
<th align="left" valign="top" charoff="50">Reference</th>
</tr>
</thead>
<tfoot valign="top"><tr><th colspan="6" align="left" valign="top" charoff="50">Percentages relate to the range of pairwise distances, or phylogenetic diversity captured within each group based on full-length 16S rRNA gene sequences in <xref ref-type="supplementary-material" rid="S1">Supplementary Figure S1</xref>
.</th>
</tr>
</tfoot>
<tbody valign="top"><tr><td align="left" valign="top" charoff="50">S1a100–96.52%</td>
<td align="left" valign="top" charoff="50"><xref ref-type="bibr" rid="b27">Morris et al (2005)</xref>
</td>
<td align="left" valign="top" charoff="50">P1a.1100–98.15%</td>
<td align="left" valign="top" charoff="50"><xref ref-type="bibr" rid="b16">Garcia-Martinez and Rodriguez-Valera (2000)</xref>
</td>
<td align="left" valign="top" charoff="50">HTCC1062HTCC1002HTCC8010HTCC8022HTCC8040</td>
<td align="left" valign="top" charoff="50"><xref ref-type="bibr" rid="b35">Rappe et al (2002)</xref>
; <xref ref-type="bibr" rid="b42">Stingl et al (2007)</xref>
</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> </td>
<td align="left" valign="top" charoff="50"> </td>
<td align="left" valign="top" charoff="50">P1a.2100–98.88%</td>
<td align="left" valign="top" charoff="50"><xref ref-type="bibr" rid="b3">Brown and Fuhrman (2005)</xref>
</td>
<td align="left" valign="top" charoff="50">HTCC8038HTCC8041HTCC8045HTCC8046HTCC8049</td>
<td align="left" valign="top" charoff="50"><xref ref-type="bibr" rid="b42">Stingl et al (2007)</xref>
</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> </td>
<td align="left" valign="top" charoff="50"> </td>
<td align="left" valign="top" charoff="50">P1a.3100–97.73%</td>
<td align="left" valign="top" charoff="50"><xref ref-type="bibr" rid="b3">Brown and Fuhrman (2005)</xref>
</td>
<td align="left" valign="top" charoff="50">HTCC8051HTCC8047HTCC7211HTCC7215HTCC7216HTCC7217</td>
<td align="left" valign="top" charoff="50"><xref ref-type="bibr" rid="b42">Stingl et al (2007)</xref>
</td>
</tr>
<tr><td align="left" valign="top" charoff="50">S1b100–97.12%</td>
<td align="left" valign="top" charoff="50"><xref ref-type="bibr" rid="b27">Morris et al (2005)</xref>
</td>
<td align="left" valign="top" charoff="50">P1b99.78–97.12%</td>
<td align="left" valign="top" charoff="50">This study</td>
<td align="left" valign="top" charoff="50">N/A</td>
<td align="left" valign="top" charoff="50"> </td>
</tr>
<tr><td align="left" valign="top" charoff="50"> </td>
<td align="left" valign="top" charoff="50"> </td>
<td align="left" valign="top" charoff="50">NA1</td>
<td align="left" valign="top" charoff="50">This study</td>
<td align="left" valign="top" charoff="50">N/A</td>
<td align="left" valign="top" charoff="50"> </td>
</tr>
<tr><td align="left" valign="top" charoff="50"> </td>
<td align="left" valign="top" charoff="50"> </td>
<td align="left" valign="top" charoff="50">NA2</td>
<td align="left" valign="top" charoff="50">This Study</td>
<td align="left" valign="top" charoff="50">N/A</td>
<td align="left" valign="top" charoff="50"> </td>
</tr>
<tr><td align="left" valign="top" charoff="50">S2100–91.98%</td>
<td align="left" valign="top" charoff="50"><xref ref-type="bibr" rid="b27">Morris et al (2005)</xref>
</td>
<td align="left" valign="top" charoff="50">P2.1100–93.41%</td>
<td align="left" valign="top" charoff="50"><xref ref-type="bibr" rid="b3">Brown and Fuhrman (2005)</xref>
</td>
<td align="left" valign="top" charoff="50">N/A</td>
<td align="left" valign="top" charoff="50"> </td>
</tr>
<tr><td align="left" valign="top" charoff="50"> </td>
<td align="left" valign="top" charoff="50"> </td>
<td align="left" valign="top" charoff="50">P2.2100–96.49%</td>
<td align="left" valign="top" charoff="50"><xref ref-type="bibr" rid="b16">Garcia-Martinez and Rodriguez-Valera (2000)</xref>
</td>
<td align="left" valign="top" charoff="50">N/A</td>
<td align="left" valign="top" charoff="50"> </td>
</tr>
<tr><td align="left" valign="top" charoff="50"> </td>
<td align="left" valign="top" charoff="50"> </td>
<td align="left" valign="top" charoff="50">P2.3100–96.00%</td>
<td align="left" valign="top" charoff="50"><xref ref-type="bibr" rid="b16">Garcia-Martinez and Rodriguez-Valera (2000)</xref>
</td>
<td align="left" valign="top" charoff="50">N/A</td>
<td align="left" valign="top" charoff="50"> </td>
</tr>
<tr><td align="left" valign="top" charoff="50">S3100–85.44%</td>
<td align="left" valign="top" charoff="50"><xref ref-type="bibr" rid="b27">Morris et al (2005)</xref>
</td>
<td align="left" valign="top" charoff="50">P3.1100–97.55%</td>
<td align="left" valign="top" charoff="50">This study</td>
<td align="left" valign="top" charoff="50">HIMB114</td>
<td align="left" valign="top" charoff="50"> </td>
</tr>
<tr><td align="left" valign="top" charoff="50"> </td>
<td align="left" valign="top" charoff="50"> </td>
<td align="left" valign="top" charoff="50">P3.2100–97.49%</td>
<td align="left" valign="top" charoff="50">This study</td>
<td align="left" valign="top" charoff="50">IMCC9063</td>
<td align="left" valign="top" charoff="50"><xref ref-type="bibr" rid="b31">Oh et al (2011)</xref>
</td>
</tr>
</tbody>
</table>
</table-wrap>
</floats-group>
</pmc>
<affiliations><list><country><li>Australie</li>
<li>États-Unis</li>
</country>
</list>
<tree><country name="Australie"><noRegion><name sortKey="Brown, Mark V" sort="Brown, Mark V" uniqKey="Brown M" first="Mark V" last="Brown">Mark V. Brown</name>
</noRegion>
<name sortKey="Brown, Mark V" sort="Brown, Mark V" uniqKey="Brown M" first="Mark V" last="Brown">Mark V. Brown</name>
<name sortKey="Cavicchioli, Ricardo" sort="Cavicchioli, Ricardo" uniqKey="Cavicchioli R" first="Ricardo" last="Cavicchioli">Ricardo Cavicchioli</name>
<name sortKey="Demaere, Matthew Z" sort="Demaere, Matthew Z" uniqKey="Demaere M" first="Matthew Z" last="Demaere">Matthew Z. Demaere</name>
<name sortKey="Lauro, Federico M" sort="Lauro, Federico M" uniqKey="Lauro F" first="Federico M" last="Lauro">Federico M. Lauro</name>
<name sortKey="Muir, Les" sort="Muir, Les" uniqKey="Muir L" first="Les" last="Muir">Les Muir</name>
<name sortKey="Riddle, Martin J" sort="Riddle, Martin J" uniqKey="Riddle M" first="Martin J" last="Riddle">Martin J. Riddle</name>
<name sortKey="Rintoul, Stephen R" sort="Rintoul, Stephen R" uniqKey="Rintoul S" first="Stephen R" last="Rintoul">Stephen R. Rintoul</name>
<name sortKey="Thomas, Torsten" sort="Thomas, Torsten" uniqKey="Thomas T" first="Torsten" last="Thomas">Torsten Thomas</name>
<name sortKey="Thomas, Torsten" sort="Thomas, Torsten" uniqKey="Thomas T" first="Torsten" last="Thomas">Torsten Thomas</name>
<name sortKey="Wilkins, David" sort="Wilkins, David" uniqKey="Wilkins D" first="David" last="Wilkins">David Wilkins</name>
</country>
<country name="États-Unis"><noRegion><name sortKey="Fuhrman, Jed A" sort="Fuhrman, Jed A" uniqKey="Fuhrman J" first="Jed A" last="Fuhrman">Jed A. Fuhrman</name>
</noRegion>
<name sortKey="Allen, Andrew" sort="Allen, Andrew" uniqKey="Allen A" first="Andrew" last="Allen">Andrew Allen</name>
<name sortKey="Andrews Pfannkoch, Cynthia" sort="Andrews Pfannkoch, Cynthia" uniqKey="Andrews Pfannkoch C" first="Cynthia" last="Andrews-Pfannkoch">Cynthia Andrews-Pfannkoch</name>
<name sortKey="Hoffman, Jeffrey M" sort="Hoffman, Jeffrey M" uniqKey="Hoffman J" first="Jeffrey M" last="Hoffman">Jeffrey M. Hoffman</name>
<name sortKey="Mcquaid, Jeffrey B" sort="Mcquaid, Jeffrey B" uniqKey="Mcquaid J" first="Jeffrey B" last="Mcquaid">Jeffrey B. Mcquaid</name>
</country>
</tree>
</affiliations>
</record>
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