Cell morphology drives spatial patterning in microbial communities.
Identifieur interne : 001040 ( PubMed/Checkpoint ); précédent : 001039; suivant : 001041Cell morphology drives spatial patterning in microbial communities.
Auteurs : William P J. Smith [Royaume-Uni] ; Yohan Davit [France] ; James M. Osborne [Australie] ; Wook Kim [Royaume-Uni] ; Kevin R. Foster [Royaume-Uni] ; Joe M. Pitt-Francis [Royaume-Uni]Source :
- Proceedings of the National Academy of Sciences of the United States of America [ 1091-6490 ] ; 2017.
Abstract
The clearest phenotypic characteristic of microbial cells is their shape, but we do not understand how cell shape affects the dense communities, known as biofilms, where many microbes live. Here, we use individual-based modeling to systematically vary cell shape and study its impact in simulated communities. We compete cells with different cell morphologies under a range of conditions and ask how shape affects the patterning and evolutionary fitness of cells within a community. Our models predict that cell shape will strongly influence the fate of a cell lineage: we describe a mechanism through which coccal (round) cells rise to the upper surface of a community, leading to a strong spatial structuring that can be critical for fitness. We test our predictions experimentally using strains of Escherichia coli that grow at a similar rate but differ in cell shape due to single amino acid changes in the actin homolog MreB. As predicted by our model, cell types strongly sort by shape, with round cells at the top of the colony and rod cells dominating the basal surface and edges. Our work suggests that cell morphology has a strong impact within microbial communities and may offer new ways to engineer the structure of synthetic communities.
DOI: 10.1073/pnas.1613007114
PubMed: 28039436
Affiliations:
- Australie, France, Royaume-Uni
- Angleterre, Oxfordshire, Victoria (État)
- Melbourne, Oxford
- Université d'Oxford, Université de Melbourne
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Smith</name><affiliation wicri:level="4"><nlm:affiliation>Department of Computer Science, University of Oxford, Oxford OX1 3QD, United Kingdom.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Department of Computer Science, University of Oxford, Oxford OX1 3QD</wicri:regionArea><orgName type="university">Université d'Oxford</orgName><placeName><settlement type="city">Oxford</settlement><region type="nation">Angleterre</region><region type="région" nuts="1">Oxfordshire</region></placeName></affiliation></author><author><name sortKey="Davit, Yohan" sort="Davit, Yohan" uniqKey="Davit Y" first="Yohan" last="Davit">Yohan Davit</name><affiliation wicri:level="1"><nlm:affiliation>Institut de Mécanique des Fluides de Toulouse (IMFT), Université de Toulouse, Centre National de la Recherche Scientifique (CNRS), Institut National Polytechnique de Toulouse (INPT), Université Paul Sabatier (UPS), F-31400 Toulouse, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Institut de Mécanique des Fluides de Toulouse (IMFT), Université de Toulouse, Centre National de la Recherche Scientifique (CNRS), Institut National Polytechnique de Toulouse (INPT), Université Paul Sabatier (UPS), F-31400 Toulouse</wicri:regionArea><wicri:noRegion>31400 Toulouse</wicri:noRegion><wicri:noRegion>31400 Toulouse</wicri:noRegion></affiliation></author><author><name sortKey="Osborne, James M" sort="Osborne, James M" uniqKey="Osborne J" first="James M" last="Osborne">James M. Osborne</name><affiliation wicri:level="4"><nlm:affiliation>School of Mathematics and Statistics, University of Melbourne, VIC 3010, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>School of Mathematics and Statistics, University of Melbourne, VIC 3010</wicri:regionArea><orgName type="university">Université de Melbourne</orgName><placeName><settlement type="city">Melbourne</settlement><region type="état">Victoria (État)</region></placeName></affiliation></author><author><name sortKey="Kim, Wook" sort="Kim, Wook" uniqKey="Kim W" first="Wook" last="Kim">Wook Kim</name><affiliation wicri:level="4"><nlm:affiliation>Department of Zoology, University of Oxford, Oxford OX1 3PS, United Kingdom.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Department of Zoology, University of Oxford, Oxford OX1 3PS</wicri:regionArea><orgName type="university">Université d'Oxford</orgName><placeName><settlement type="city">Oxford</settlement><region type="nation">Angleterre</region><region type="région" nuts="1">Oxfordshire</region></placeName></affiliation></author><author><name sortKey="Foster, Kevin R" sort="Foster, Kevin R" uniqKey="Foster K" first="Kevin R" last="Foster">Kevin R. Foster</name><affiliation wicri:level="4"><nlm:affiliation>Department of Zoology, University of Oxford, Oxford OX1 3PS, United Kingdom kevin.foster@zoo.ox.ac.uk joe.pitt-francis@cs.ox.ac.uk.</nlm:affiliation><country wicri:rule="url">Royaume-Uni</country><wicri:regionArea>Department of Zoology, University of Oxford, Oxford OX1 3PS</wicri:regionArea><orgName type="university">Université d'Oxford</orgName><placeName><settlement type="city">Oxford</settlement><region type="nation">Angleterre</region><region type="région" nuts="1">Oxfordshire</region></placeName></affiliation></author><author><name sortKey="Pitt Francis, Joe M" sort="Pitt Francis, Joe M" uniqKey="Pitt Francis J" first="Joe M" last="Pitt-Francis">Joe M. Pitt-Francis</name><affiliation wicri:level="4"><nlm:affiliation>Department of Computer Science, University of Oxford, Oxford OX1 3QD, United Kingdom; kevin.foster@zoo.ox.ac.uk joe.pitt-francis@cs.ox.ac.uk.</nlm:affiliation><country wicri:rule="url">Royaume-Uni</country><wicri:regionArea>Department of Computer Science, University of Oxford, Oxford OX1 3QD</wicri:regionArea><orgName type="university">Université d'Oxford</orgName><placeName><settlement type="city">Oxford</settlement><region type="nation">Angleterre</region><region type="région" nuts="1">Oxfordshire</region></placeName></affiliation></author></analytic><series><title level="j">Proceedings of the National Academy of Sciences of the United States of America</title><idno type="eISSN">1091-6490</idno><imprint><date when="2017" type="published">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">The clearest phenotypic characteristic of microbial cells is their shape, but we do not understand how cell shape affects the dense communities, known as biofilms, where many microbes live. Here, we use individual-based modeling to systematically vary cell shape and study its impact in simulated communities. We compete cells with different cell morphologies under a range of conditions and ask how shape affects the patterning and evolutionary fitness of cells within a community. Our models predict that cell shape will strongly influence the fate of a cell lineage: we describe a mechanism through which coccal (round) cells rise to the upper surface of a community, leading to a strong spatial structuring that can be critical for fitness. We test our predictions experimentally using strains of Escherichia coli that grow at a similar rate but differ in cell shape due to single amino acid changes in the actin homolog MreB. As predicted by our model, cell types strongly sort by shape, with round cells at the top of the colony and rod cells dominating the basal surface and edges. Our work suggests that cell morphology has a strong impact within microbial communities and may offer new ways to engineer the structure of synthetic communities.</div></front></TEI><pubmed><MedlineCitation Status="In-Data-Review" Owner="NLM"><PMID Version="1">28039436</PMID><DateCreated><Year>2016</Year><Month>12</Month><Day>31</Day></DateCreated><DateRevised><Year>2017</Year><Month>09</Month><Day>22</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1091-6490</ISSN><JournalIssue CitedMedium="Internet"><Volume>114</Volume><Issue>3</Issue><PubDate><Year>2017</Year><Month>Jan</Month><Day>17</Day></PubDate></JournalIssue><Title>Proceedings of the National Academy of Sciences of the United States of America</Title><ISOAbbreviation>Proc. Natl. Acad. Sci. U.S.A.</ISOAbbreviation></Journal><ArticleTitle>Cell morphology drives spatial patterning in microbial communities.</ArticleTitle><Pagination><MedlinePgn>E280-E286</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1073/pnas.1613007114</ELocationID><Abstract><AbstractText>The clearest phenotypic characteristic of microbial cells is their shape, but we do not understand how cell shape affects the dense communities, known as biofilms, where many microbes live. Here, we use individual-based modeling to systematically vary cell shape and study its impact in simulated communities. We compete cells with different cell morphologies under a range of conditions and ask how shape affects the patterning and evolutionary fitness of cells within a community. Our models predict that cell shape will strongly influence the fate of a cell lineage: we describe a mechanism through which coccal (round) cells rise to the upper surface of a community, leading to a strong spatial structuring that can be critical for fitness. We test our predictions experimentally using strains of Escherichia coli that grow at a similar rate but differ in cell shape due to single amino acid changes in the actin homolog MreB. As predicted by our model, cell types strongly sort by shape, with round cells at the top of the colony and rod cells dominating the basal surface and edges. Our work suggests that cell morphology has a strong impact within microbial communities and may offer new ways to engineer the structure of synthetic communities.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Smith</LastName><ForeName>William P J</ForeName><Initials>WP</Initials><AffiliationInfo><Affiliation>Department of Computer Science, University of Oxford, Oxford OX1 3QD, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Davit</LastName><ForeName>Yohan</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Institut de Mécanique des Fluides de Toulouse (IMFT), Université de Toulouse, Centre National de la Recherche Scientifique (CNRS), Institut National Polytechnique de Toulouse (INPT), Université Paul Sabatier (UPS), F-31400 Toulouse, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Osborne</LastName><ForeName>James M</ForeName><Initials>JM</Initials><AffiliationInfo><Affiliation>School of Mathematics and Statistics, University of Melbourne, VIC 3010, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kim</LastName><ForeName>Wook</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>Department of Zoology, University of Oxford, Oxford OX1 3PS, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Foster</LastName><ForeName>Kevin R</ForeName><Initials>KR</Initials><Identifier Source="ORCID">http://orcid.org/0000-0003-4687-6633</Identifier><AffiliationInfo><Affiliation>Department of Zoology, University of Oxford, Oxford OX1 3PS, United Kingdom kevin.foster@zoo.ox.ac.uk joe.pitt-francis@cs.ox.ac.uk.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Pitt-Francis</LastName><ForeName>Joe M</ForeName><Initials>JM</Initials><AffiliationInfo><Affiliation>Department of Computer Science, University of Oxford, Oxford OX1 3QD, United Kingdom; kevin.foster@zoo.ox.ac.uk joe.pitt-francis@cs.ox.ac.uk.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>242670</GrantID><Agency>European Research Council</Agency><Country>International</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2016</Year><Month>12</Month><Day>30</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Proc Natl Acad Sci U S A</MedlineTA><NlmUniqueID>7505876</NlmUniqueID><ISSNLinking>0027-8424</ISSNLinking></MedlineJournalInfo><CommentsCorrectionsList><CommentsCorrections RefType="Cites"><RefSource>Nat Rev Microbiol. 2008 Feb;6(2):162-8</RefSource><PMID Version="1">18157153</PMID></CommentsCorrections><CommentsCorrections RefType="Cites"><RefSource>Proc Natl Acad Sci U S A. 2015 Apr 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Version="1">18843299</PMID></CommentsCorrections></CommentsCorrectionsList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">biofilms</Keyword><Keyword MajorTopicYN="N">biophysics</Keyword><Keyword MajorTopicYN="N">cell morphology</Keyword><Keyword MajorTopicYN="N">self-organization</Keyword><Keyword MajorTopicYN="N">synthetic biology</Keyword></KeywordList><CoiStatement>The authors declare no conflict of interest.</CoiStatement></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="pubmed"><Year>2017</Year><Month>1</Month><Day>1</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2017</Year><Month>1</Month><Day>1</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2017</Year><Month>1</Month><Day>1</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">28039436</ArticleId><ArticleId IdType="pii">1613007114</ArticleId><ArticleId IdType="doi">10.1073/pnas.1613007114</ArticleId><ArticleId IdType="pmc">PMC5255625</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>Australie</li><li>France</li><li>Royaume-Uni</li></country><region><li>Angleterre</li><li>Oxfordshire</li><li>Victoria (État)</li></region><settlement><li>Melbourne</li><li>Oxford</li></settlement><orgName><li>Université d'Oxford</li><li>Université de Melbourne</li></orgName></list><tree><country name="Royaume-Uni"><region name="Angleterre"><name sortKey="Smith, William P J" sort="Smith, William P J" uniqKey="Smith W" first="William P J" last="Smith">William P J. Smith</name></region><name sortKey="Foster, Kevin R" sort="Foster, Kevin R" uniqKey="Foster K" first="Kevin R" last="Foster">Kevin R. Foster</name><name sortKey="Kim, Wook" sort="Kim, Wook" uniqKey="Kim W" first="Wook" last="Kim">Wook Kim</name><name sortKey="Pitt Francis, Joe M" sort="Pitt Francis, Joe M" uniqKey="Pitt Francis J" first="Joe M" last="Pitt-Francis">Joe M. Pitt-Francis</name></country><country name="France"><noRegion><name sortKey="Davit, Yohan" sort="Davit, Yohan" uniqKey="Davit Y" first="Yohan" last="Davit">Yohan Davit</name></noRegion></country><country name="Australie"><region name="Victoria (État)"><name sortKey="Osborne, James M" sort="Osborne, James M" uniqKey="Osborne J" first="James M" last="Osborne">James M. Osborne</name></region></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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