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<title xml:lang="en">Delineating ecologically significant taxonomic units from global patterns of marine picocyanobacteria</title>
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<name sortKey="Farrant, Gregory K" sort="Farrant, Gregory K" uniqKey="Farrant G" first="Gregory K." last="Farrant">Gregory K. Farrant</name>
<affiliation>
<nlm:aff id="aff1">
<institution>Sorbonne Universités</institution>
, Université Paris 06, CNRS, UMR 7144, Station Biologique, CS 90074 Roscoff,
<country>France</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Dore, Hugo" sort="Dore, Hugo" uniqKey="Dore H" first="Hugo" last="Doré">Hugo Doré</name>
<affiliation>
<nlm:aff id="aff1">
<institution>Sorbonne Universités</institution>
, Université Paris 06, CNRS, UMR 7144, Station Biologique, CS 90074 Roscoff,
<country>France</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Cornejo Castillo, Francisco M" sort="Cornejo Castillo, Francisco M" uniqKey="Cornejo Castillo F" first="Francisco M." last="Cornejo-Castillo">Francisco M. Cornejo-Castillo</name>
<affiliation>
<nlm:aff id="aff2">Department of Marine Biology and Oceanography, Institute of Marine Sciences (ICM),
<institution>Consejo Superior de Investigaciones Científicas (CSIC)</institution>
, Barcelona ES-08003,
<country>Spain</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Partensky, Frederic" sort="Partensky, Frederic" uniqKey="Partensky F" first="Frédéric" last="Partensky">Frédéric Partensky</name>
<affiliation>
<nlm:aff id="aff1">
<institution>Sorbonne Universités</institution>
, Université Paris 06, CNRS, UMR 7144, Station Biologique, CS 90074 Roscoff,
<country>France</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Ratin, Morgane" sort="Ratin, Morgane" uniqKey="Ratin M" first="Morgane" last="Ratin">Morgane Ratin</name>
<affiliation>
<nlm:aff id="aff1">
<institution>Sorbonne Universités</institution>
, Université Paris 06, CNRS, UMR 7144, Station Biologique, CS 90074 Roscoff,
<country>France</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Ostrowski, Martin" sort="Ostrowski, Martin" uniqKey="Ostrowski M" first="Martin" last="Ostrowski">Martin Ostrowski</name>
<affiliation>
<nlm:aff id="aff3">Department of Chemistry and Biomolecular Sciences,
<institution>Macquarie University</institution>
, Sydney, NSW 2109,
<country>Australia</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Pitt, Frances D" sort="Pitt, Frances D" uniqKey="Pitt F" first="Frances D." last="Pitt">Frances D. Pitt</name>
<affiliation>
<nlm:aff id="aff4">School of Life Sciences,
<institution>University of Warwick</institution>
, Coventry CV4 7AL,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Wincker, Patrick" sort="Wincker, Patrick" uniqKey="Wincker P" first="Patrick" last="Wincker">Patrick Wincker</name>
<affiliation>
<nlm:aff id="aff5">Commissariat à l'Energie Atomique et aux Energies Alternatives (CEA), Institut de Génomique,
<institution>Genoscope</institution>
, 91057 Evry,
<country>France</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Scanlan, David J" sort="Scanlan, David J" uniqKey="Scanlan D" first="David J." last="Scanlan">David J. Scanlan</name>
<affiliation>
<nlm:aff id="aff4">School of Life Sciences,
<institution>University of Warwick</institution>
, Coventry CV4 7AL,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Iudicone, Daniele" sort="Iudicone, Daniele" uniqKey="Iudicone D" first="Daniele" last="Iudicone">Daniele Iudicone</name>
<affiliation>
<nlm:aff id="aff6">
<institution>Stazione Zoologica Anton Dohrn</institution>
, 80121 Naples,
<country>Italy</country>
</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Acinas, Silvia G" sort="Acinas, Silvia G" uniqKey="Acinas S" first="Silvia G." last="Acinas">Silvia G. Acinas</name>
<affiliation>
<nlm:aff id="aff2">Department of Marine Biology and Oceanography, Institute of Marine Sciences (ICM),
<institution>Consejo Superior de Investigaciones Científicas (CSIC)</institution>
, Barcelona ES-08003,
<country>Spain</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Garczarek, Laurence" sort="Garczarek, Laurence" uniqKey="Garczarek L" first="Laurence" last="Garczarek">Laurence Garczarek</name>
<affiliation>
<nlm:aff id="aff1">
<institution>Sorbonne Universités</institution>
, Université Paris 06, CNRS, UMR 7144, Station Biologique, CS 90074 Roscoff,
<country>France</country>
;</nlm:aff>
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<title xml:lang="en" level="a" type="main">Delineating ecologically significant taxonomic units from global patterns of marine picocyanobacteria</title>
<author>
<name sortKey="Farrant, Gregory K" sort="Farrant, Gregory K" uniqKey="Farrant G" first="Gregory K." last="Farrant">Gregory K. Farrant</name>
<affiliation>
<nlm:aff id="aff1">
<institution>Sorbonne Universités</institution>
, Université Paris 06, CNRS, UMR 7144, Station Biologique, CS 90074 Roscoff,
<country>France</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Dore, Hugo" sort="Dore, Hugo" uniqKey="Dore H" first="Hugo" last="Doré">Hugo Doré</name>
<affiliation>
<nlm:aff id="aff1">
<institution>Sorbonne Universités</institution>
, Université Paris 06, CNRS, UMR 7144, Station Biologique, CS 90074 Roscoff,
<country>France</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Cornejo Castillo, Francisco M" sort="Cornejo Castillo, Francisco M" uniqKey="Cornejo Castillo F" first="Francisco M." last="Cornejo-Castillo">Francisco M. Cornejo-Castillo</name>
<affiliation>
<nlm:aff id="aff2">Department of Marine Biology and Oceanography, Institute of Marine Sciences (ICM),
<institution>Consejo Superior de Investigaciones Científicas (CSIC)</institution>
, Barcelona ES-08003,
<country>Spain</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Partensky, Frederic" sort="Partensky, Frederic" uniqKey="Partensky F" first="Frédéric" last="Partensky">Frédéric Partensky</name>
<affiliation>
<nlm:aff id="aff1">
<institution>Sorbonne Universités</institution>
, Université Paris 06, CNRS, UMR 7144, Station Biologique, CS 90074 Roscoff,
<country>France</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Ratin, Morgane" sort="Ratin, Morgane" uniqKey="Ratin M" first="Morgane" last="Ratin">Morgane Ratin</name>
<affiliation>
<nlm:aff id="aff1">
<institution>Sorbonne Universités</institution>
, Université Paris 06, CNRS, UMR 7144, Station Biologique, CS 90074 Roscoff,
<country>France</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Ostrowski, Martin" sort="Ostrowski, Martin" uniqKey="Ostrowski M" first="Martin" last="Ostrowski">Martin Ostrowski</name>
<affiliation>
<nlm:aff id="aff3">Department of Chemistry and Biomolecular Sciences,
<institution>Macquarie University</institution>
, Sydney, NSW 2109,
<country>Australia</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Pitt, Frances D" sort="Pitt, Frances D" uniqKey="Pitt F" first="Frances D." last="Pitt">Frances D. Pitt</name>
<affiliation>
<nlm:aff id="aff4">School of Life Sciences,
<institution>University of Warwick</institution>
, Coventry CV4 7AL,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Wincker, Patrick" sort="Wincker, Patrick" uniqKey="Wincker P" first="Patrick" last="Wincker">Patrick Wincker</name>
<affiliation>
<nlm:aff id="aff5">Commissariat à l'Energie Atomique et aux Energies Alternatives (CEA), Institut de Génomique,
<institution>Genoscope</institution>
, 91057 Evry,
<country>France</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Scanlan, David J" sort="Scanlan, David J" uniqKey="Scanlan D" first="David J." last="Scanlan">David J. Scanlan</name>
<affiliation>
<nlm:aff id="aff4">School of Life Sciences,
<institution>University of Warwick</institution>
, Coventry CV4 7AL,
<country>United Kingdom</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Iudicone, Daniele" sort="Iudicone, Daniele" uniqKey="Iudicone D" first="Daniele" last="Iudicone">Daniele Iudicone</name>
<affiliation>
<nlm:aff id="aff6">
<institution>Stazione Zoologica Anton Dohrn</institution>
, 80121 Naples,
<country>Italy</country>
</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Acinas, Silvia G" sort="Acinas, Silvia G" uniqKey="Acinas S" first="Silvia G." last="Acinas">Silvia G. Acinas</name>
<affiliation>
<nlm:aff id="aff2">Department of Marine Biology and Oceanography, Institute of Marine Sciences (ICM),
<institution>Consejo Superior de Investigaciones Científicas (CSIC)</institution>
, Barcelona ES-08003,
<country>Spain</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Garczarek, Laurence" sort="Garczarek, Laurence" uniqKey="Garczarek L" first="Laurence" last="Garczarek">Laurence Garczarek</name>
<affiliation>
<nlm:aff id="aff1">
<institution>Sorbonne Universités</institution>
, Université Paris 06, CNRS, UMR 7144, Station Biologique, CS 90074 Roscoff,
<country>France</country>
;</nlm:aff>
</affiliation>
</author>
</analytic>
<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>
</imprint>
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<front>
<div type="abstract" xml:lang="en">
<title>Significance</title>
<p>Metagenomics has become an accessible approach to study complex microbial communities thanks to the advent of high-throughput sequencing technologies. However, molecular ecology studies often face interpretation issues, notably due to the lack of reliable reference databases for assigning reads to the correct taxa and use of fixed cutoffs to delineate taxonomic groups. Here, we considerably refined the phylogeography of marine picocyanobacteria, responsible for about 25% of global marine productivity, by recruiting reads targeting a high-resolution marker from
<italic>Tara</italic>
Oceans metagenomes. By clustering lineages based on their distribution patterns, we showed that there is significant diversity at a finer resolution than the currently defined “ecotypes,” a diversity that is tightly controlled by environmental cues.</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">27302952</article-id>
<article-id pub-id-type="pmc">4914166</article-id>
<article-id pub-id-type="publisher-id">201524865</article-id>
<article-id pub-id-type="doi">10.1073/pnas.1524865113</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>PNAS Plus</subject>
</subj-group>
<subj-group subj-group-type="heading">
<subject>Biological Sciences</subject>
<subj-group>
<subject>Environmental Sciences</subject>
</subj-group>
</subj-group>
<series-title>PNAS Plus</series-title>
</article-categories>
<title-group>
<article-title>Delineating ecologically significant taxonomic units from global patterns of marine picocyanobacteria</article-title>
<alt-title alt-title-type="short">Global biogeography of marine picocyanobacteria</alt-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Farrant</surname>
<given-names>Gregory K.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
<xref ref-type="author-notes" rid="fn1">
<sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn2">
<sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Doré</surname>
<given-names>Hugo</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
<xref ref-type="author-notes" rid="fn1">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Cornejo-Castillo</surname>
<given-names>Francisco M.</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Partensky</surname>
<given-names>Frédéric</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Ratin</surname>
<given-names>Morgane</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Ostrowski</surname>
<given-names>Martin</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>c</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Pitt</surname>
<given-names>Frances D.</given-names>
</name>
<xref ref-type="aff" rid="aff4">
<sup>d</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Wincker</surname>
<given-names>Patrick</given-names>
</name>
<xref ref-type="aff" rid="aff5">
<sup>e</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Scanlan</surname>
<given-names>David J.</given-names>
</name>
<xref ref-type="aff" rid="aff4">
<sup>d</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Iudicone</surname>
<given-names>Daniele</given-names>
</name>
<xref ref-type="aff" rid="aff6">
<sup>f</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Acinas</surname>
<given-names>Silvia G.</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Garczarek</surname>
<given-names>Laurence</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
<xref ref-type="corresp" rid="cor1">
<sup>3</sup>
</xref>
</contrib>
<aff id="aff1">
<sup>a</sup>
<institution>Sorbonne Universités</institution>
, Université Paris 06, CNRS, UMR 7144, Station Biologique, CS 90074 Roscoff,
<country>France</country>
;</aff>
<aff id="aff2">
<sup>b</sup>
Department of Marine Biology and Oceanography, Institute of Marine Sciences (ICM),
<institution>Consejo Superior de Investigaciones Científicas (CSIC)</institution>
, Barcelona ES-08003,
<country>Spain</country>
;</aff>
<aff id="aff3">
<sup>c</sup>
Department of Chemistry and Biomolecular Sciences,
<institution>Macquarie University</institution>
, Sydney, NSW 2109,
<country>Australia</country>
;</aff>
<aff id="aff4">
<sup>d</sup>
School of Life Sciences,
<institution>University of Warwick</institution>
, Coventry CV4 7AL,
<country>United Kingdom</country>
;</aff>
<aff id="aff5">
<sup>e</sup>
Commissariat à l'Energie Atomique et aux Energies Alternatives (CEA), Institut de Génomique,
<institution>Genoscope</institution>
, 91057 Evry,
<country>France</country>
;</aff>
<aff id="aff6">
<sup>f</sup>
<institution>Stazione Zoologica Anton Dohrn</institution>
, 80121 Naples,
<country>Italy</country>
</aff>
</contrib-group>
<author-notes>
<corresp id="cor1">
<sup>3</sup>
To whom correspondence should be addressed. Email:
<email>laurence.garczarek@sb-roscoff.fr</email>
.</corresp>
<fn fn-type="edited-by">
<p>Edited by David M. Karl, University of Hawaii, Honolulu, HI, and approved May 6, 2016 (received for review January 5, 2016)</p>
</fn>
<fn fn-type="con">
<p>Author contributions: G.K.F. and L.G. designed research; G.K.F., H.D., and M.R. performed research; M.O., F.D.P., P.W., D.J.S., and S.G.A. contributed new reagents/analytic tools; M.O., F.D.P., and D.J.S. provided
<italic>petB</italic>
reference sequences; P.W. provided sequencing of the metagenomic dataset; G.K.F., H.D., F.M.C.-C., D.I., and L.G. analyzed data; and G.K.F., H.D., F.P., and L.G. wrote the paper.</p>
</fn>
<fn fn-type="equal" id="fn1">
<p>
<sup>1</sup>
G.K.F. and H.D. contributed equally to this work.</p>
</fn>
<fn fn-type="present-address" id="fn2">
<p>
<sup>2</sup>
Present address: Food Safety, Environment, and Genetics, Matís Ltd., 113 Reykjavík, Iceland.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub">
<day>14</day>
<month>6</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="epub">
<day>2</day>
<month>6</month>
<year>2016</year>
</pub-date>
<volume>113</volume>
<issue>24</issue>
<fpage>E3365</fpage>
<lpage>E3374</lpage>
<permissions></permissions>
<self-uri xlink:title="pdf" xlink:href="pnas.201524865.pdf"></self-uri>
<abstract abstract-type="executive-summary">
<title>Significance</title>
<p>Metagenomics has become an accessible approach to study complex microbial communities thanks to the advent of high-throughput sequencing technologies. However, molecular ecology studies often face interpretation issues, notably due to the lack of reliable reference databases for assigning reads to the correct taxa and use of fixed cutoffs to delineate taxonomic groups. Here, we considerably refined the phylogeography of marine picocyanobacteria, responsible for about 25% of global marine productivity, by recruiting reads targeting a high-resolution marker from
<italic>Tara</italic>
Oceans metagenomes. By clustering lineages based on their distribution patterns, we showed that there is significant diversity at a finer resolution than the currently defined “ecotypes,” a diversity that is tightly controlled by environmental cues.</p>
</abstract>
<abstract>
<p>
<italic>Prochlorococcus</italic>
and
<italic>Synechococcus</italic>
are the two most abundant and widespread phytoplankton in the global ocean. To better understand the factors controlling their biogeography, a reference database of the high-resolution taxonomic marker
<italic>p</italic>
<italic>et</italic>
<italic>B</italic>
, encoding cytochrome
<italic>b</italic>
<sub>6</sub>
, was used to recruit reads out of 109 metagenomes from the
<italic>Tara</italic>
Oceans expedition. An unsuspected novel genetic diversity was unveiled within both genera, even for the most abundant and well-characterized clades, and 136 divergent
<italic>petB</italic>
sequences were successfully assembled from metagenomic reads, significantly enriching the reference database. We then defined Ecologically Significant Taxonomic Units (ESTUs)—that is, organisms belonging to the same clade and occupying a common oceanic niche. Three major ESTU assemblages were identified along the cruise transect for
<italic>Prochlorococcus</italic>
and eight for
<italic>Synechococcus</italic>
. Although
<italic>Prochlorococcus</italic>
HLIIIA and HLIVA ESTUs codominated in iron-depleted areas of the Pacific Ocean, CRD1 and the yet-to-be cultured EnvB were the prevalent
<italic>Synechococcus</italic>
clades in this area, with three different CRD1 and EnvB ESTUs occupying distinct ecological niches with regard to iron availability and temperature. Sharp community shifts were also observed over short geographic distances—for example, around the Marquesas Islands or between southern Indian and Atlantic Oceans—pointing to a tight correlation between ESTU assemblages and specific physico-chemical parameters. Together, this study demonstrates that there is a previously overlooked, ecologically meaningful, fine-scale diversity within some currently defined picocyanobacterial ecotypes, bringing novel insights into the ecology, diversity, and biology of the two most abundant phototrophs on Earth.</p>
</abstract>
<kwd-group>
<kwd>molecular ecology</kwd>
<kwd>metagenomics</kwd>
<kwd>
<italic>Tara</italic>
Oceans</kwd>
<kwd>
<italic>Synechococcus</italic>
</kwd>
<kwd>
<italic>Prochlorococcus</italic>
</kwd>
</kwd-group>
<funding-group>
<award-group id="gs1">
<funding-source id="sp1">Agence Nationale de la Recherche (L' Agence Nationale de la Recherche)
<named-content content-type="funder-id">501100001665</named-content>
</funding-source>
<award-id rid="sp1">ANR-13-ADAP-0010</award-id>
</award-group>
<award-group id="gs2">
<funding-source id="sp2">Agence Nationale de la Recherche (L' Agence Nationale de la Recherche)
<named-content content-type="funder-id">501100001665</named-content>
</funding-source>
<award-id rid="sp2">ANR-10-INBS-09</award-id>
</award-group>
<award-group id="gs3">
<funding-source id="sp3">Agence Nationale de la Recherche (L' Agence Nationale de la Recherche)
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