Time-course transcriptomics reveals that amino acids catabolism plays a key role in toxinogenesis and morphology in Clostridium tetani.
Identifieur interne : 000050 ( Main/Exploration ); précédent : 000049; suivant : 000051Time-course transcriptomics reveals that amino acids catabolism plays a key role in toxinogenesis and morphology in Clostridium tetani.
Auteurs : Camila A. Orellana [Australie, Chili] ; Nicolas E. Zaragoza [Australie] ; Cuauhtemoc Licona-Cassani [Australie, Mexique] ; Robin W. Palfreyman [Australie] ; Nicholas Cowie [Australie] ; Glenn Moonen [Australie] ; George Moutafis [Australie] ; John Power [Australie] ; Lars K. Nielsen [Australie, Danemark] ; Esteban Marcellin [Australie]Source :
- Journal of industrial microbiology & biotechnology [ 1476-5535 ] ; 2020.
Abstract
Tetanus is a fatal disease caused by Clostridium tetani infections. To prevent infections, a toxoid vaccine, developed almost a century ago, is routinely used in humans and animals. The vaccine is listed in the World Health Organisation list of Essential Medicines and can be produced and administered very cheaply in the developing world for less than one US Dollar per dose. Recent developments in both analytical tools and frameworks for systems biology provide industry with an opportunity to gain a deeper understanding of the parameters that determine C. tetani virulence and physiological behaviour in bioreactors. Here, we compared a traditional fermentation process with a fermentation medium supplemented with five heavily consumed amino acids. The experiment demonstrated that amino acid catabolism plays a key role in the virulence of C. tetani. The addition of the five amino acids favoured growth, decreased toxin production and changed C. tetani morphology. Using time-course transcriptomics, we created a "fermentation map", which shows that the tetanus toxin transcriptional regulator BotR, P21 and the tetanus toxin gene was downregulated. Moreover, this in-depth analysis revealed potential genes that might be involved in C. tetani virulence regulation. We observed differential expression of genes related to cell separation, surface/cell adhesion, pyrimidine biosynthesis and salvage, flagellar motility, and prophage genes. Overall, the fermentation map shows that, mediated by free amino acid concentrations, virulence in C. tetani is regulated at the transcriptional level and affects a plethora of metabolic functions.
DOI: 10.1007/s10295-020-02330-3
PubMed: 33175241
Affiliations:
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Lyngby, Denmark.</nlm:affiliation><country xml:lang="fr">Danemark</country><wicri:regionArea>The Novo Nordisk Foundation Centre for Biosustainability, Technical University of Denmark, Kgs. Lyngby</wicri:regionArea><wicri:noRegion>Kgs. Lyngby</wicri:noRegion></affiliation></author><author><name sortKey="Marcellin, Esteban" sort="Marcellin, Esteban" uniqKey="Marcellin E" first="Esteban" last="Marcellin">Esteban Marcellin</name><affiliation wicri:level="1"><nlm:affiliation>Australian Institute for Bioengineering and Nanotechnology (AIBN), The University of Queensland, Brisbane, QLD, 4072, Australia. e.marcellin@uq.edu.au.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Australian Institute for Bioengineering and Nanotechnology (AIBN), The University of Queensland, Brisbane, QLD, 4072</wicri:regionArea><wicri:noRegion>4072</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Metabolomics Australia, The University of Queensland, Brisbane, QLD, 4072, Australia. e.marcellin@uq.edu.au.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Metabolomics Australia, The University of Queensland, Brisbane, QLD, 4072</wicri:regionArea><wicri:noRegion>4072</wicri:noRegion></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2020">2020</date><idno type="RBID">pubmed:33175241</idno><idno type="pmid">33175241</idno><idno type="doi">10.1007/s10295-020-02330-3</idno><idno type="wicri:Area/Main/Corpus">000012</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000012</idno><idno type="wicri:Area/Main/Curation">000012</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Curation">000012</idno><idno type="wicri:Area/Main/Exploration">000012</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Time-course transcriptomics reveals that amino acids catabolism plays a key role in toxinogenesis and morphology in Clostridium tetani.</title><author><name sortKey="Orellana, Camila A" sort="Orellana, Camila A" uniqKey="Orellana C" first="Camila A" last="Orellana">Camila A. Orellana</name><affiliation wicri:level="1"><nlm:affiliation>Australian Institute for Bioengineering and Nanotechnology (AIBN), The University of Queensland, Brisbane, QLD, 4072, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Australian Institute for Bioengineering and Nanotechnology (AIBN), The University of Queensland, Brisbane, QLD, 4072</wicri:regionArea><wicri:noRegion>4072</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Department of Chemical and Bioprocess Engineering, School of Engineering, Pontificia Universidad Católica de Chile, Santiago, Chile.</nlm:affiliation><country xml:lang="fr">Chili</country><wicri:regionArea>Department of Chemical and Bioprocess Engineering, School of Engineering, Pontificia Universidad Católica de Chile, Santiago</wicri:regionArea><wicri:noRegion>Santiago</wicri:noRegion></affiliation></author><author><name sortKey="Zaragoza, Nicolas E" sort="Zaragoza, Nicolas E" uniqKey="Zaragoza N" first="Nicolas E" last="Zaragoza">Nicolas E. Zaragoza</name><affiliation wicri:level="1"><nlm:affiliation>Australian Institute for Bioengineering and Nanotechnology (AIBN), The University of Queensland, Brisbane, QLD, 4072, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Australian Institute for Bioengineering and Nanotechnology (AIBN), The University of Queensland, Brisbane, QLD, 4072</wicri:regionArea><wicri:noRegion>4072</wicri:noRegion></affiliation></author><author><name sortKey="Licona Cassani, Cuauhtemoc" sort="Licona Cassani, Cuauhtemoc" uniqKey="Licona Cassani C" first="Cuauhtemoc" last="Licona-Cassani">Cuauhtemoc Licona-Cassani</name><affiliation wicri:level="1"><nlm:affiliation>Australian Institute for Bioengineering and Nanotechnology (AIBN), The University of Queensland, Brisbane, QLD, 4072, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Australian Institute for Bioengineering and Nanotechnology (AIBN), The University of Queensland, Brisbane, QLD, 4072</wicri:regionArea><wicri:noRegion>4072</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Centro de Biotecnología FEMSA, Tecnológico de Monterrey, Nuevo León, Mexico.</nlm:affiliation><country xml:lang="fr">Mexique</country><wicri:regionArea>Centro de Biotecnología FEMSA, Tecnológico de Monterrey, Nuevo León</wicri:regionArea><wicri:noRegion>Nuevo León</wicri:noRegion></affiliation></author><author><name sortKey="Palfreyman, Robin W" sort="Palfreyman, Robin W" uniqKey="Palfreyman R" first="Robin W" last="Palfreyman">Robin W. Palfreyman</name><affiliation wicri:level="1"><nlm:affiliation>Metabolomics Australia, The University of Queensland, Brisbane, QLD, 4072, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Metabolomics Australia, The University of Queensland, Brisbane, QLD, 4072</wicri:regionArea><wicri:noRegion>4072</wicri:noRegion></affiliation></author><author><name sortKey="Cowie, Nicholas" sort="Cowie, Nicholas" uniqKey="Cowie N" first="Nicholas" last="Cowie">Nicholas Cowie</name><affiliation wicri:level="1"><nlm:affiliation>Australian Institute for Bioengineering and Nanotechnology (AIBN), The University of Queensland, Brisbane, QLD, 4072, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Australian Institute for Bioengineering and Nanotechnology (AIBN), The University of Queensland, Brisbane, QLD, 4072</wicri:regionArea><wicri:noRegion>4072</wicri:noRegion></affiliation></author><author><name sortKey="Moonen, Glenn" sort="Moonen, Glenn" uniqKey="Moonen G" first="Glenn" last="Moonen">Glenn Moonen</name><affiliation wicri:level="1"><nlm:affiliation>, Zoetis. 45 Poplar Road, Parkville, VIC, 3052, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>, Zoetis. 45 Poplar Road, Parkville, VIC, 3052</wicri:regionArea><wicri:noRegion>3052</wicri:noRegion></affiliation></author><author><name sortKey="Moutafis, George" sort="Moutafis, George" uniqKey="Moutafis G" first="George" last="Moutafis">George Moutafis</name><affiliation wicri:level="1"><nlm:affiliation>, Zoetis. 45 Poplar Road, Parkville, VIC, 3052, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>, Zoetis. 45 Poplar Road, Parkville, VIC, 3052</wicri:regionArea><wicri:noRegion>3052</wicri:noRegion></affiliation></author><author><name sortKey="Power, John" sort="Power, John" uniqKey="Power J" first="John" last="Power">John Power</name><affiliation wicri:level="1"><nlm:affiliation>, Zoetis. 45 Poplar Road, Parkville, VIC, 3052, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>, Zoetis. 45 Poplar Road, Parkville, VIC, 3052</wicri:regionArea><wicri:noRegion>3052</wicri:noRegion></affiliation></author><author><name sortKey="Nielsen, Lars K" sort="Nielsen, Lars K" uniqKey="Nielsen L" first="Lars K" last="Nielsen">Lars K. Nielsen</name><affiliation wicri:level="1"><nlm:affiliation>Australian Institute for Bioengineering and Nanotechnology (AIBN), The University of Queensland, Brisbane, QLD, 4072, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Australian Institute for Bioengineering and Nanotechnology (AIBN), The University of Queensland, Brisbane, QLD, 4072</wicri:regionArea><wicri:noRegion>4072</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Metabolomics Australia, The University of Queensland, Brisbane, QLD, 4072, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Metabolomics Australia, The University of Queensland, Brisbane, QLD, 4072</wicri:regionArea><wicri:noRegion>4072</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>The Novo Nordisk Foundation Centre for Biosustainability, Technical University of Denmark, Kgs. Lyngby, Denmark.</nlm:affiliation><country xml:lang="fr">Danemark</country><wicri:regionArea>The Novo Nordisk Foundation Centre for Biosustainability, Technical University of Denmark, Kgs. Lyngby</wicri:regionArea><wicri:noRegion>Kgs. Lyngby</wicri:noRegion></affiliation></author><author><name sortKey="Marcellin, Esteban" sort="Marcellin, Esteban" uniqKey="Marcellin E" first="Esteban" last="Marcellin">Esteban Marcellin</name><affiliation wicri:level="1"><nlm:affiliation>Australian Institute for Bioengineering and Nanotechnology (AIBN), The University of Queensland, Brisbane, QLD, 4072, Australia. e.marcellin@uq.edu.au.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Australian Institute for Bioengineering and Nanotechnology (AIBN), The University of Queensland, Brisbane, QLD, 4072</wicri:regionArea><wicri:noRegion>4072</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Metabolomics Australia, The University of Queensland, Brisbane, QLD, 4072, Australia. e.marcellin@uq.edu.au.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Metabolomics Australia, The University of Queensland, Brisbane, QLD, 4072</wicri:regionArea><wicri:noRegion>4072</wicri:noRegion></affiliation></author></analytic><series><title level="j">Journal of industrial microbiology & biotechnology</title><idno type="eISSN">1476-5535</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Tetanus is a fatal disease caused by Clostridium tetani infections. To prevent infections, a toxoid vaccine, developed almost a century ago, is routinely used in humans and animals. The vaccine is listed in the World Health Organisation list of Essential Medicines and can be produced and administered very cheaply in the developing world for less than one US Dollar per dose. Recent developments in both analytical tools and frameworks for systems biology provide industry with an opportunity to gain a deeper understanding of the parameters that determine C. tetani virulence and physiological behaviour in bioreactors. Here, we compared a traditional fermentation process with a fermentation medium supplemented with five heavily consumed amino acids. The experiment demonstrated that amino acid catabolism plays a key role in the virulence of C. tetani. The addition of the five amino acids favoured growth, decreased toxin production and changed C. tetani morphology. Using time-course transcriptomics, we created a "fermentation map", which shows that the tetanus toxin transcriptional regulator BotR, P21 and the tetanus toxin gene was downregulated. Moreover, this in-depth analysis revealed potential genes that might be involved in C. tetani virulence regulation. We observed differential expression of genes related to cell separation, surface/cell adhesion, pyrimidine biosynthesis and salvage, flagellar motility, and prophage genes. Overall, the fermentation map shows that, mediated by free amino acid concentrations, virulence in C. tetani is regulated at the transcriptional level and affects a plethora of metabolic functions.</div></front></TEI><pubmed><MedlineCitation Status="Publisher" Owner="NLM"><PMID Version="1">33175241</PMID><DateRevised><Year>2020</Year><Month>11</Month><Day>11</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1476-5535</ISSN><JournalIssue CitedMedium="Internet"><PubDate><Year>2020</Year><Month>Nov</Month><Day>11</Day></PubDate></JournalIssue><Title>Journal of industrial microbiology & biotechnology</Title><ISOAbbreviation>J Ind Microbiol Biotechnol</ISOAbbreviation></Journal><ArticleTitle>Time-course transcriptomics reveals that amino acids catabolism plays a key role in toxinogenesis and morphology in Clostridium tetani.</ArticleTitle><ELocationID EIdType="doi" ValidYN="Y">10.1007/s10295-020-02330-3</ELocationID><Abstract><AbstractText>Tetanus is a fatal disease caused by Clostridium tetani infections. To prevent infections, a toxoid vaccine, developed almost a century ago, is routinely used in humans and animals. The vaccine is listed in the World Health Organisation list of Essential Medicines and can be produced and administered very cheaply in the developing world for less than one US Dollar per dose. Recent developments in both analytical tools and frameworks for systems biology provide industry with an opportunity to gain a deeper understanding of the parameters that determine C. tetani virulence and physiological behaviour in bioreactors. Here, we compared a traditional fermentation process with a fermentation medium supplemented with five heavily consumed amino acids. The experiment demonstrated that amino acid catabolism plays a key role in the virulence of C. tetani. The addition of the five amino acids favoured growth, decreased toxin production and changed C. tetani morphology. Using time-course transcriptomics, we created a "fermentation map", which shows that the tetanus toxin transcriptional regulator BotR, P21 and the tetanus toxin gene was downregulated. Moreover, this in-depth analysis revealed potential genes that might be involved in C. tetani virulence regulation. We observed differential expression of genes related to cell separation, surface/cell adhesion, pyrimidine biosynthesis and salvage, flagellar motility, and prophage genes. Overall, the fermentation map shows that, mediated by free amino acid concentrations, virulence in C. tetani is regulated at the transcriptional level and affects a plethora of metabolic functions.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Orellana</LastName><ForeName>Camila A</ForeName><Initials>CA</Initials><AffiliationInfo><Affiliation>Australian Institute for Bioengineering and Nanotechnology (AIBN), The University of Queensland, Brisbane, QLD, 4072, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Chemical and Bioprocess Engineering, School of Engineering, Pontificia Universidad Católica de Chile, Santiago, Chile.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zaragoza</LastName><ForeName>Nicolas E</ForeName><Initials>NE</Initials><AffiliationInfo><Affiliation>Australian Institute for Bioengineering and Nanotechnology (AIBN), The University of Queensland, Brisbane, QLD, 4072, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Licona-Cassani</LastName><ForeName>Cuauhtemoc</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Australian Institute for Bioengineering and Nanotechnology (AIBN), The University of Queensland, Brisbane, QLD, 4072, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Centro de Biotecnología FEMSA, Tecnológico de Monterrey, Nuevo León, Mexico.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Palfreyman</LastName><ForeName>Robin W</ForeName><Initials>RW</Initials><AffiliationInfo><Affiliation>Metabolomics Australia, The University of Queensland, Brisbane, QLD, 4072, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Cowie</LastName><ForeName>Nicholas</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>Australian Institute for Bioengineering and Nanotechnology (AIBN), The University of Queensland, Brisbane, QLD, 4072, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Moonen</LastName><ForeName>Glenn</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>, Zoetis. 45 Poplar Road, Parkville, VIC, 3052, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Moutafis</LastName><ForeName>George</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>, Zoetis. 45 Poplar Road, Parkville, VIC, 3052, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Power</LastName><ForeName>John</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>, Zoetis. 45 Poplar Road, Parkville, VIC, 3052, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Nielsen</LastName><ForeName>Lars K</ForeName><Initials>LK</Initials><AffiliationInfo><Affiliation>Australian Institute for Bioengineering and Nanotechnology (AIBN), The University of Queensland, Brisbane, QLD, 4072, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Metabolomics Australia, The University of Queensland, Brisbane, QLD, 4072, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>The Novo Nordisk Foundation Centre for Biosustainability, Technical University of Denmark, Kgs. Lyngby, Denmark.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Marcellin</LastName><ForeName>Esteban</ForeName><Initials>E</Initials><Identifier Source="ORCID">http://orcid.org/0000-0003-3173-7956</Identifier><AffiliationInfo><Affiliation>Australian Institute for Bioengineering and Nanotechnology (AIBN), The University of Queensland, Brisbane, QLD, 4072, Australia. e.marcellin@uq.edu.au.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Metabolomics Australia, The University of Queensland, Brisbane, QLD, 4072, Australia. e.marcellin@uq.edu.au.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>LP150100087</GrantID><Agency>Australian Research Council</Agency><Country></Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>11</Month><Day>11</Day></ArticleDate></Article><MedlineJournalInfo><Country>Germany</Country><MedlineTA>J Ind Microbiol Biotechnol</MedlineTA><NlmUniqueID>9705544</NlmUniqueID><ISSNLinking>1367-5435</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Amino acids</Keyword><Keyword MajorTopicYN="N">Clostridium tetani fermentation</Keyword><Keyword MajorTopicYN="N">Pathogenesis</Keyword><Keyword MajorTopicYN="N">Tetanus toxin regulation</Keyword><Keyword MajorTopicYN="N">Time-course transcriptomics</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>05</Month><Day>11</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>11</Month><Day>02</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>11</Month><Day>11</Day><Hour>12</Hour><Minute>13</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>11</Month><Day>12</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>11</Month><Day>12</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>aheadofprint</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">33175241</ArticleId><ArticleId IdType="doi">10.1007/s10295-020-02330-3</ArticleId><ArticleId IdType="pii">10.1007/s10295-020-02330-3</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>Australie</li><li>Chili</li><li>Danemark</li><li>Mexique</li></country></list><tree><country name="Australie"><noRegion><name sortKey="Orellana, Camila A" sort="Orellana, Camila A" uniqKey="Orellana C" first="Camila A" last="Orellana">Camila A. Orellana</name></noRegion><name sortKey="Cowie, Nicholas" sort="Cowie, Nicholas" uniqKey="Cowie N" first="Nicholas" last="Cowie">Nicholas Cowie</name><name sortKey="Licona Cassani, Cuauhtemoc" sort="Licona Cassani, Cuauhtemoc" uniqKey="Licona Cassani C" first="Cuauhtemoc" last="Licona-Cassani">Cuauhtemoc Licona-Cassani</name><name sortKey="Marcellin, Esteban" sort="Marcellin, Esteban" uniqKey="Marcellin E" first="Esteban" last="Marcellin">Esteban Marcellin</name><name sortKey="Marcellin, Esteban" sort="Marcellin, Esteban" uniqKey="Marcellin E" first="Esteban" last="Marcellin">Esteban Marcellin</name><name sortKey="Moonen, Glenn" sort="Moonen, Glenn" uniqKey="Moonen G" first="Glenn" last="Moonen">Glenn Moonen</name><name sortKey="Moutafis, George" sort="Moutafis, George" uniqKey="Moutafis G" first="George" last="Moutafis">George Moutafis</name><name sortKey="Nielsen, Lars K" sort="Nielsen, Lars K" uniqKey="Nielsen L" first="Lars K" last="Nielsen">Lars K. Nielsen</name><name sortKey="Nielsen, Lars K" sort="Nielsen, Lars K" uniqKey="Nielsen L" first="Lars K" last="Nielsen">Lars K. Nielsen</name><name sortKey="Palfreyman, Robin W" sort="Palfreyman, Robin W" uniqKey="Palfreyman R" first="Robin W" last="Palfreyman">Robin W. Palfreyman</name><name sortKey="Power, John" sort="Power, John" uniqKey="Power J" first="John" last="Power">John Power</name><name sortKey="Zaragoza, Nicolas E" sort="Zaragoza, Nicolas E" uniqKey="Zaragoza N" first="Nicolas E" last="Zaragoza">Nicolas E. Zaragoza</name></country><country name="Chili"><noRegion><name sortKey="Orellana, Camila A" sort="Orellana, Camila A" uniqKey="Orellana C" first="Camila A" last="Orellana">Camila A. Orellana</name></noRegion></country><country name="Mexique"><noRegion><name sortKey="Licona Cassani, Cuauhtemoc" sort="Licona Cassani, Cuauhtemoc" uniqKey="Licona Cassani C" first="Cuauhtemoc" last="Licona-Cassani">Cuauhtemoc Licona-Cassani</name></noRegion></country><country name="Danemark"><noRegion><name sortKey="Nielsen, Lars K" sort="Nielsen, Lars K" uniqKey="Nielsen L" first="Lars K" last="Nielsen">Lars K. Nielsen</name></noRegion></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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