Bacterial community transcription patterns during a marine phytoplankton bloom
Identifieur interne : 000700 ( Istex/Corpus ); précédent : 000699; suivant : 000701Bacterial community transcription patterns during a marine phytoplankton bloom
Auteurs : Johanna M. Rinta-Kanto ; Shulei Sun ; Shalabh Sharma ; Ronald P. Kiene ; Mary Ann MoranSource :
- Environmental Microbiology [ 1462-2912 ] ; 2012-01.
Abstract
Bacterioplankton consume a large proportion of photosynthetically fixed carbon in the ocean and control its biogeochemical fate. We used an experimental metatranscriptomics approach to compare bacterial activities that route energy and nutrients during a phytoplankton bloom compared with non‐bloom conditions. mRNAs were sequenced from duplicate bloom and control microcosms 1 day after a phytoplankton biomass peak, and transcript copies per litre of seawater were calculated using an internal mRNA standard. Transcriptome analysis revealed a potential novel mechanism for enhanced efficiency during carbon‐limited growth, mediated through membrane‐bound pyrophosphatases [V‐type H(+)‐translocating; hppA]; bloom bacterioplankton participated less in this metabolic energy scavenging than non‐bloom bacterioplankton, with possible implications for differences in growth yields on organic substrates. Bloom bacterioplankton transcribed more copies of genes predicted to increase cell surface adhesiveness, mediated by changes in bacterial signalling molecules related to biofilm formation and motility; these may be important in microbial aggregate formation. Bloom bacterioplankton also transcribed more copies of genes for organic acid utilization, suggesting an increased importance of this compound class in the bioreactive organic matter released during phytoplankton blooms. Transcription patterns were surprisingly faithful within a taxon regardless of treatment, suggesting that phylogeny broadly predicts the ecological roles of bacterial groups across ‘boom’ and ‘bust’ environmental backgrounds.
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DOI: 10.1111/j.1462-2920.2011.02602.x
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Rinta-Kanto</name><affiliation><mods:affiliation>Department of Marine Sciences, University of Georgia, Athens, GA 30602, USA</mods:affiliation></affiliation></author><author><name sortKey="Sun, Shulei" sort="Sun, Shulei" uniqKey="Sun S" first="Shulei" last="Sun">Shulei Sun</name><affiliation><mods:affiliation>Department of Marine Sciences, University of Georgia, Athens, GA 30602, USA</mods:affiliation></affiliation></author><author><name sortKey="Sharma, Shalabh" sort="Sharma, Shalabh" uniqKey="Sharma S" first="Shalabh" last="Sharma">Shalabh Sharma</name><affiliation><mods:affiliation>Department of Marine Sciences, University of Georgia, Athens, GA 30602, USA</mods:affiliation></affiliation></author><author><name sortKey="Kiene, Ronald P" sort="Kiene, Ronald P" uniqKey="Kiene R" first="Ronald P." last="Kiene">Ronald P. Kiene</name><affiliation><mods:affiliation>Department of Marine Sciences, University of South Alabama, Mobile, AL 36688, USA</mods:affiliation></affiliation></author><author><name sortKey="Moran, Mary Ann" sort="Moran, Mary Ann" uniqKey="Moran M" first="Mary Ann" last="Moran">Mary Ann Moran</name><affiliation><mods:affiliation>Department of Marine Sciences, University of Georgia, Athens, GA 30602, USA</mods:affiliation></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">ISTEX</idno><idno type="RBID">ISTEX:E2841A5EC19CD5FE75F4C0385374EE232EF19DB5</idno><date when="2012" year="2012">2012</date><idno type="doi">10.1111/j.1462-2920.2011.02602.x</idno><idno type="url">https://api.istex.fr/document/E2841A5EC19CD5FE75F4C0385374EE232EF19DB5/fulltext/pdf</idno><idno type="wicri:Area/Istex/Corpus">000700</idno></publicationStmt><sourceDesc><biblStruct><analytic><title level="a" type="main" xml:lang="en">Bacterial community transcription patterns during a marine phytoplankton bloom</title><author><name sortKey="Rinta Anto, Johanna M" sort="Rinta Anto, Johanna M" uniqKey="Rinta Anto J" first="Johanna M." last="Rinta-Kanto">Johanna M. 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We used an experimental metatranscriptomics approach to compare bacterial activities that route energy and nutrients during a phytoplankton bloom compared with non‐bloom conditions. mRNAs were sequenced from duplicate bloom and control microcosms 1 day after a phytoplankton biomass peak, and transcript copies per litre of seawater were calculated using an internal mRNA standard. Transcriptome analysis revealed a potential novel mechanism for enhanced efficiency during carbon‐limited growth, mediated through membrane‐bound pyrophosphatases [V‐type H(+)‐translocating; hppA]; bloom bacterioplankton participated less in this metabolic energy scavenging than non‐bloom bacterioplankton, with possible implications for differences in growth yields on organic substrates. Bloom bacterioplankton transcribed more copies of genes predicted to increase cell surface adhesiveness, mediated by changes in bacterial signalling molecules related to biofilm formation and motility; these may be important in microbial aggregate formation. Bloom bacterioplankton also transcribed more copies of genes for organic acid utilization, suggesting an increased importance of this compound class in the bioreactive organic matter released during phytoplankton blooms. Transcription patterns were surprisingly faithful within a taxon regardless of treatment, suggesting that phylogeny broadly predicts the ecological roles of bacterial groups across ‘boom’ and ‘bust’ environmental backgrounds.</div></front></TEI><istex><corpusName>wiley</corpusName><author><json:item><name>Johanna M. 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(+1) 706 542 6481; Fax (+1) 706 542 5888.</p></note><affiliation>Department of Marine Sciences, University of Georgia, Athens, GA 30602, USA</affiliation></author></analytic><monogr><title level="j">Environmental Microbiology</title><idno type="pISSN">1462-2912</idno><idno type="eISSN">1462-2920</idno><idno type="DOI">10.1111/(ISSN)1462-2920</idno><imprint><publisher>Blackwell Publishing Ltd</publisher><pubPlace>Oxford, UK</pubPlace><date type="published" when="2012-01"></date><biblScope unit="volume">14</biblScope><biblScope unit="issue">1</biblScope><biblScope unit="page" from="228">228</biblScope><biblScope unit="page" to="239">239</biblScope></imprint></monogr><idno type="istex">E2841A5EC19CD5FE75F4C0385374EE232EF19DB5</idno><idno type="DOI">10.1111/j.1462-2920.2011.02602.x</idno><idno type="ArticleID">EMI2602</idno></biblStruct></sourceDesc></fileDesc><profileDesc><creation><date>2012</date></creation><langUsage><language ident="en">en</language></langUsage><abstract xml:lang="en"><p>Bacterioplankton consume a large proportion of photosynthetically fixed carbon in the ocean and control its biogeochemical fate. 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Bloom bacterioplankton transcribed more copies of genes predicted to increase cell surface adhesiveness, mediated by changes in bacterial signalling molecules related to biofilm formation and motility; these may be important in microbial aggregate formation. Bloom bacterioplankton also transcribed more copies of genes for organic acid utilization, suggesting an increased importance of this compound class in the bioreactive organic matter released during phytoplankton blooms. 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(+1) 706 542 6481; Fax (+1) 706 542 5888. </correspondenceTo><linkGroup><link type="toTypesetVersion" href="file:EMI.EMI2602.pdf"></link></linkGroup></publicationMeta><contentMeta><unparsedEditorialHistory>Received 26 January, 2011; revised 25 August, 2011; accepted 2 September, 2011.</unparsedEditorialHistory><countGroup><count type="figureTotal" number="6"></count><count type="tableTotal" number="1"></count><count type="formulaTotal" number="0"></count><count type="referenceTotal" number="48"></count><count type="wordTotal" number="6871"></count><count type="linksPubMed" number="0"></count><count type="linksCrossRef" number="0"></count></countGroup><titleGroup><title type="main">Bacterial community transcription patterns during a marine phytoplankton bloom</title><title type="shortAuthors">J. M. Rinta‐Kanto <i>et al</i>.</title><title type="short">Phytoplankton bloom metatranscriptome</title></titleGroup><creators><creator creatorRole="author" xml:id="cr1" affiliationRef="#a1" noteRef="#fn2"><personName><givenNames>Johanna M.</givenNames><familyName>Rinta‐Kanto</familyName></personName></creator><creator creatorRole="author" xml:id="cr2" affiliationRef="#a1" noteRef="#fn1"><personName><givenNames>Shulei</givenNames><familyName>Sun</familyName></personName></creator><creator creatorRole="author" xml:id="cr3" affiliationRef="#a1"><personName><givenNames>Shalabh</givenNames><familyName>Sharma</familyName></personName></creator><creator creatorRole="author" xml:id="cr4" affiliationRef="#a2"><personName><givenNames>Ronald P.</givenNames><familyName>Kiene</familyName></personName></creator><creator creatorRole="author" xml:id="cr5" affiliationRef="#a1" corresponding="yes"><personName><givenNames>Mary Ann</givenNames><familyName>Moran</familyName></personName></creator></creators><affiliationGroup><affiliation xml:id="a1" countryCode="US"><unparsedAffiliation>Department of Marine Sciences, University of Georgia, Athens, GA 30602, USA</unparsedAffiliation></affiliation><affiliation xml:id="a2" countryCode="US"><unparsedAffiliation>Department of Marine Sciences, University of South Alabama, Mobile, AL 36688, USA</unparsedAffiliation></affiliation></affiliationGroup><supportingInformation><p><b>Fig. S1.</b> Relative abundance of bacterial taxa in control (top) and bloom (bottom) microcosms based on taxonomic analysis of PCR‐amplified 16S rRNA genes.</p><p><b>Fig. S2.</b> Rarefaction plot of functional gene categories (clusters of orthologous groups; COGs) in four experimental marine metatranscriptomes.</p><p><b>Fig. S3.</b> Taxonomic assignment of transcripts under bloom and non‐bloom conditions. There was only one sequence assigned to the GGDEF domain COG (COG2199) in the control library, and that sequence binned to a Deltaproteobacteria gene.</p><p><b>Fig. S4.</b> Membrane‐bound pyrophosphatases (COG3808; <i>hppA</i>) and proteorhodopsin proteins translocate protons across biological membranes; the resulting proton gradient is available for ATP generation via ATP synthase. Transcripts for both membrane‐bound inorganic pyrophosphatases and ATP synthase subunit A were significantly less abundant under bloom conditions.</p><p><b>Table S1.</b> Marine genomes containing an inorganic pyrophosphatase (<i>hppA</i>) homologue. The <i>R. rubrum</i> ATCC 11170 inorganic diphosphatase sequence (YP_425238) was used as a query in BLASTp analysis against the NCBI All Genomes database using an <i>E</i>‐value cut‐off of ≤ 10<sup>−5</sup>. Hits were manually checked by reanalysis against the NCBI RefSeq database.</p><supportingInfoItem><mediaResource alt="supporting info item" href="urn-x:wiley:14622912:media:emi2602:EMI_2602_sm_SuppInfor"></mediaResource><caption>Supporting info item</caption></supportingInfoItem></supportingInformation><abstractGroup><abstract type="main" xml:lang="en"><title type="main">Summary</title><p>Bacterioplankton consume a large proportion of photosynthetically fixed carbon in the ocean and control its biogeochemical fate. We used an experimental metatranscriptomics approach to compare bacterial activities that route energy and nutrients during a phytoplankton bloom compared with non‐bloom conditions. mRNAs were sequenced from duplicate bloom and control microcosms 1 day after a phytoplankton biomass peak, and transcript copies per litre of seawater were calculated using an internal mRNA standard. Transcriptome analysis revealed a potential novel mechanism for enhanced efficiency during carbon‐limited growth, mediated through membrane‐bound pyrophosphatases [V‐type H(+)‐translocating; <i>hppA</i>]; bloom bacterioplankton participated less in this metabolic energy scavenging than non‐bloom bacterioplankton, with possible implications for differences in growth yields on organic substrates. Bloom bacterioplankton transcribed more copies of genes predicted to increase cell surface adhesiveness, mediated by changes in bacterial signalling molecules related to biofilm formation and motility; these may be important in microbial aggregate formation. Bloom bacterioplankton also transcribed more copies of genes for organic acid utilization, suggesting an increased importance of this compound class in the bioreactive organic matter released during phytoplankton blooms. Transcription patterns were surprisingly faithful within a taxon regardless of treatment, suggesting that phylogeny broadly predicts the ecological roles of bacterial groups across ‘boom’ and ‘bust’ environmental backgrounds.</p></abstract></abstractGroup></contentMeta><noteGroup><note xml:id="fn1"><p>Present addresses: Center for Research in Biological Systems, University of California San Diego, 9500 Gilman Drive #0446, La Jolla, CA 92093‐0446, USA;</p></note><note xml:id="fn2"><p> Department of Food and Environmental Sciences, Division of Microbiology, University of Helsinki, PO Box 56, FIN‐00014 Helsinki, Finland.</p></note></noteGroup></header></component></istex:document></istex:metadataXml><mods version="3.6"><titleInfo lang="en"><title>Bacterial community transcription patterns during a marine phytoplankton bloom</title></titleInfo><titleInfo type="abbreviated" lang="en"><title>Phytoplankton bloom metatranscriptome</title></titleInfo><titleInfo type="alternative" contentType="CDATA" lang="en"><title>Bacterial community transcription patterns during a marine phytoplankton bloom</title></titleInfo><name type="personal"><namePart type="given">Johanna M.</namePart><namePart type="family">Rinta‐Kanto</namePart><affiliation>Department of Marine Sciences, University of Georgia, Athens, GA 30602, USA</affiliation><description>Department of Food and Environmental Sciences, Division of Microbiology, University of Helsinki, PO Box 56, FIN‐00014 Helsinki, Finland.</description><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">Shulei</namePart><namePart type="family">Sun</namePart><affiliation>Department of Marine Sciences, University of Georgia, Athens, GA 30602, USA</affiliation><description>Present addresses: Center for Research in Biological Systems, University of California San Diego, 9500 Gilman Drive #0446, La Jolla, CA 92093‐0446, USA;</description><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">Shalabh</namePart><namePart type="family">Sharma</namePart><affiliation>Department of Marine Sciences, University of Georgia, Athens, GA 30602, USA</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">Ronald P.</namePart><namePart type="family">Kiene</namePart><affiliation>Department of Marine Sciences, University of South Alabama, Mobile, AL 36688, USA</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">Mary Ann</namePart><namePart type="family">Moran</namePart><affiliation>Department of Marine Sciences, University of Georgia, Athens, GA 30602, USA</affiliation><description>Correspondence: E‐mail ; Tel. (+1) 706 542 6481; Fax (+1) 706 542 5888.</description><role><roleTerm type="text">author</roleTerm></role></name><typeOfResource>text</typeOfResource><genre type="article" displayLabel="article"></genre><originInfo><publisher>Blackwell Publishing Ltd</publisher><place><placeTerm type="text">Oxford, UK</placeTerm></place><dateIssued encoding="w3cdtf">2012-01</dateIssued><edition>Received 26 January, 2011; revised 25 August, 2011; accepted 2 September, 2011.</edition><copyrightDate encoding="w3cdtf">2012</copyrightDate></originInfo><language><languageTerm type="code" authority="rfc3066">en</languageTerm><languageTerm type="code" authority="iso639-2b">eng</languageTerm></language><physicalDescription><internetMediaType>text/html</internetMediaType><extent unit="figures">6</extent><extent unit="tables">1</extent><extent unit="references">48</extent><extent unit="words">6871</extent></physicalDescription><abstract lang="en">Bacterioplankton consume a large proportion of photosynthetically fixed carbon in the ocean and control its biogeochemical fate. We used an experimental metatranscriptomics approach to compare bacterial activities that route energy and nutrients during a phytoplankton bloom compared with non‐bloom conditions. mRNAs were sequenced from duplicate bloom and control microcosms 1 day after a phytoplankton biomass peak, and transcript copies per litre of seawater were calculated using an internal mRNA standard. Transcriptome analysis revealed a potential novel mechanism for enhanced efficiency during carbon‐limited growth, mediated through membrane‐bound pyrophosphatases [V‐type H(+)‐translocating; hppA]; bloom bacterioplankton participated less in this metabolic energy scavenging than non‐bloom bacterioplankton, with possible implications for differences in growth yields on organic substrates. Bloom bacterioplankton transcribed more copies of genes predicted to increase cell surface adhesiveness, mediated by changes in bacterial signalling molecules related to biofilm formation and motility; these may be important in microbial aggregate formation. Bloom bacterioplankton also transcribed more copies of genes for organic acid utilization, suggesting an increased importance of this compound class in the bioreactive organic matter released during phytoplankton blooms. Transcription patterns were surprisingly faithful within a taxon regardless of treatment, suggesting that phylogeny broadly predicts the ecological roles of bacterial groups across ‘boom’ and ‘bust’ environmental backgrounds.</abstract><relatedItem type="host"><titleInfo><title>Environmental Microbiology</title></titleInfo><genre type="journal">journal</genre><note type="content"> Fig. S1. Relative abundance of bacterial taxa in control (top) and bloom (bottom) microcosms based on taxonomic analysis of PCR‐amplified 16S rRNA genes. Fig. S2. Rarefaction plot of functional gene categories (clusters of orthologous groups; COGs) in four experimental marine metatranscriptomes. Fig. S3. Taxonomic assignment of transcripts under bloom and non‐bloom conditions. There was only one sequence assigned to the GGDEF domain COG (COG2199) in the control library, and that sequence binned to a Deltaproteobacteria gene. Fig. S4. Membrane‐bound pyrophosphatases (COG3808; hppA) and proteorhodopsin proteins translocate protons across biological membranes; the resulting proton gradient is available for ATP generation via ATP synthase. Transcripts for both membrane‐bound inorganic pyrophosphatases and ATP synthase subunit A were significantly less abundant under bloom conditions. Table S1. Marine genomes containing an inorganic pyrophosphatase (hppA) homologue. The R. rubrum ATCC 11170 inorganic diphosphatase sequence (YP_425238) was used as a query in BLASTp analysis against the NCBI All Genomes database using an E‐value cut‐off of ≤ 10−5. Hits were manually checked by reanalysis against the NCBI RefSeq database. Fig. S1. Relative abundance of bacterial taxa in control (top) and bloom (bottom) microcosms based on taxonomic analysis of PCR‐amplified 16S rRNA genes. Fig. S2. Rarefaction plot of functional gene categories (clusters of orthologous groups; COGs) in four experimental marine metatranscriptomes. Fig. S3. Taxonomic assignment of transcripts under bloom and non‐bloom conditions. There was only one sequence assigned to the GGDEF domain COG (COG2199) in the control library, and that sequence binned to a Deltaproteobacteria gene. Fig. S4. Membrane‐bound pyrophosphatases (COG3808; hppA) and proteorhodopsin proteins translocate protons across biological membranes; the resulting proton gradient is available for ATP generation via ATP synthase. Transcripts for both membrane‐bound inorganic pyrophosphatases and ATP synthase subunit A were significantly less abundant under bloom conditions. Table S1. Marine genomes containing an inorganic pyrophosphatase (hppA) homologue. The R. rubrum ATCC 11170 inorganic diphosphatase sequence (YP_425238) was used as a query in BLASTp analysis against the NCBI All Genomes database using an E‐value cut‐off of ≤ 10−5. Hits were manually checked by reanalysis against the NCBI RefSeq database. Fig. S1. Relative abundance of bacterial taxa in control (top) and bloom (bottom) microcosms based on taxonomic analysis of PCR‐amplified 16S rRNA genes. Fig. S2. Rarefaction plot of functional gene categories (clusters of orthologous groups; COGs) in four experimental marine metatranscriptomes. Fig. S3. Taxonomic assignment of transcripts under bloom and non‐bloom conditions. There was only one sequence assigned to the GGDEF domain COG (COG2199) in the control library, and that sequence binned to a Deltaproteobacteria gene. Fig. S4. Membrane‐bound pyrophosphatases (COG3808; hppA) and proteorhodopsin proteins translocate protons across biological membranes; the resulting proton gradient is available for ATP generation via ATP synthase. Transcripts for both membrane‐bound inorganic pyrophosphatases and ATP synthase subunit A were significantly less abundant under bloom conditions. Table S1. Marine genomes containing an inorganic pyrophosphatase (hppA) homologue. The R. rubrum ATCC 11170 inorganic diphosphatase sequence (YP_425238) was used as a query in BLASTp analysis against the NCBI All Genomes database using an E‐value cut‐off of ≤ 10−5. Hits were manually checked by reanalysis against the NCBI RefSeq database. Fig. S1. Relative abundance of bacterial taxa in control (top) and bloom (bottom) microcosms based on taxonomic analysis of PCR‐amplified 16S rRNA genes. Fig. S2. Rarefaction plot of functional gene categories (clusters of orthologous groups; COGs) in four experimental marine metatranscriptomes. Fig. S3. Taxonomic assignment of transcripts under bloom and non‐bloom conditions. There was only one sequence assigned to the GGDEF domain COG (COG2199) in the control library, and that sequence binned to a Deltaproteobacteria gene. Fig. S4. Membrane‐bound pyrophosphatases (COG3808; hppA) and proteorhodopsin proteins translocate protons across biological membranes; the resulting proton gradient is available for ATP generation via ATP synthase. Transcripts for both membrane‐bound inorganic pyrophosphatases and ATP synthase subunit A were significantly less abundant under bloom conditions. Table S1. Marine genomes containing an inorganic pyrophosphatase (hppA) homologue. The R. rubrum ATCC 11170 inorganic diphosphatase sequence (YP_425238) was used as a query in BLASTp analysis against the NCBI All Genomes database using an E‐value cut‐off of ≤ 10−5. Hits were manually checked by reanalysis against the NCBI RefSeq database. Fig. S1. Relative abundance of bacterial taxa in control (top) and bloom (bottom) microcosms based on taxonomic analysis of PCR‐amplified 16S rRNA genes. Fig. S2. Rarefaction plot of functional gene categories (clusters of orthologous groups; COGs) in four experimental marine metatranscriptomes. Fig. S3. Taxonomic assignment of transcripts under bloom and non‐bloom conditions. There was only one sequence assigned to the GGDEF domain COG (COG2199) in the control library, and that sequence binned to a Deltaproteobacteria gene. Fig. S4. Membrane‐bound pyrophosphatases (COG3808; hppA) and proteorhodopsin proteins translocate protons across biological membranes; the resulting proton gradient is available for ATP generation via ATP synthase. Transcripts for both membrane‐bound inorganic pyrophosphatases and ATP synthase subunit A were significantly less abundant under bloom conditions. Table S1. Marine genomes containing an inorganic pyrophosphatase (hppA) homologue. The R. rubrum ATCC 11170 inorganic diphosphatase sequence (YP_425238) was used as a query in BLASTp analysis against the NCBI All Genomes database using an E‐value cut‐off of ≤ 10−5. Hits were manually checked by reanalysis against the NCBI RefSeq database.Supporting Info Item: Supporting info item - </note><identifier type="ISSN">1462-2912</identifier><identifier type="eISSN">1462-2920</identifier><identifier type="DOI">10.1111/(ISSN)1462-2920</identifier><identifier type="PublisherID">EMI</identifier><part><date>2012</date><detail type="title"><title>OMICS Driven Microbial Ecology</title></detail><detail type="volume"><caption>vol.</caption><number>14</number></detail><detail type="issue"><caption>no.</caption><number>1</number></detail><extent unit="pages"><start>228</start><end>239</end><total>12</total></extent></part></relatedItem><identifier type="istex">E2841A5EC19CD5FE75F4C0385374EE232EF19DB5</identifier><identifier type="DOI">10.1111/j.1462-2920.2011.02602.x</identifier><identifier type="ArticleID">EMI2602</identifier><accessCondition type="use and reproduction" contentType="copyright">© 2011 Society for Applied Microbiology and Blackwell Publishing Ltd</accessCondition><recordInfo><recordContentSource>WILEY</recordContentSource><recordOrigin>Blackwell Publishing Ltd</recordOrigin></recordInfo></mods></metadata><enrichments><json:item><type>multicat</type><uri>https://api.istex.fr/document/E2841A5EC19CD5FE75F4C0385374EE232EF19DB5/enrichments/multicat</uri></json:item></enrichments><serie></serie></istex></record>Pour manipuler ce document sous Unix (Dilib)
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