Cell morphology drives spatial patterning in microbial communities
Identifieur interne : 000A86 ( Pmc/Checkpoint ); précédent : 000A85; suivant : 000A87Cell 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 [ 0027-8424 ] ; 2016.
Abstract
Microbial communities contain cells of different shapes, and yet we know little about how these shapes affect community biology. We have developed a computational model to study the effects of microbial shape in communities. Our model predicts that shape will have strong effects on cells’ positioning, and, consequently, their survival and reproduction. Rod-shaped cells are better at colonizing the base of the community and its expanding edges, whereas round cells dominate the upper surface. We show that the same patterns occur in colonies of
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DOI: 10.1073/pnas.1613007114
PubMed: 28039436
PubMed Central: 5255625
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Smith</name><affiliation wicri:level="1"><nlm:aff id="aff1">Department of Computer Science,<institution>University of Oxford</institution>, Oxford OX1 3QD,<country>United Kingdom</country>;</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></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:aff id="aff2"><institution>Institut de Mécanique des Fluides de Toulouse (IMFT)</institution>, Université de Toulouse, Centre National de la Recherche Scientifique (CNRS), Institut National Polytechnique de Toulouse (INPT), Université Paul Sabatier (UPS), F-31400 Toulouse,<country>France</country>;</nlm:aff><country xml:lang="fr">France</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Osborne, James M" sort="Osborne, James M" uniqKey="Osborne J" first="James M." last="Osborne">James M. 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J." last="Smith">William P. J. Smith</name><affiliation wicri:level="1"><nlm:aff id="aff1">Department of Computer Science,<institution>University of Oxford</institution>, Oxford OX1 3QD,<country>United Kingdom</country>;</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></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:aff id="aff2"><institution>Institut de Mécanique des Fluides de Toulouse (IMFT)</institution>, Université de Toulouse, Centre National de la Recherche Scientifique (CNRS), Institut National Polytechnique de Toulouse (INPT), Université Paul Sabatier (UPS), F-31400 Toulouse,<country>France</country>;</nlm:aff><country xml:lang="fr">France</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></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="1"><nlm:aff id="aff3">School of Mathematics and Statistics,<institution>University of Melbourne</institution>, VIC 3010,<country>Australia</country>;</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Kim, Wook" sort="Kim, Wook" uniqKey="Kim W" first="Wook" last="Kim">Wook Kim</name><affiliation wicri:level="1"><nlm:aff id="aff4">Department of Zoology,<institution>University of Oxford</institution>, Oxford OX1 3PS,<country>United Kingdom</country></nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></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="1"><nlm:aff id="aff4">Department of Zoology,<institution>University of Oxford</institution>, Oxford OX1 3PS,<country>United Kingdom</country></nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></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="1"><nlm:aff id="aff1">Department of Computer Science,<institution>University of Oxford</institution>, Oxford OX1 3QD,<country>United Kingdom</country>;</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></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></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>Significance</title><p>Microbial communities contain cells of different shapes, and yet we know little about how these shapes affect community biology. We have developed a computational model to study the effects of microbial shape in communities. Our model predicts that shape will have strong effects on cells’ positioning, and, consequently, their survival and reproduction. Rod-shaped cells are better at colonizing the base of the community and its expanding edges, whereas round cells dominate the upper surface. We show that the same patterns occur in colonies of <italic>Escherichia coli</italic>, using strains with different shapes. Our work suggests that cell shape is a major determinant of patterning and evolutionary fitness within microbial communities.</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">28039436</article-id><article-id pub-id-type="pmc">5255625</article-id><article-id pub-id-type="publisher-id">201613007</article-id><article-id pub-id-type="doi">10.1073/pnas.1613007114</article-id><article-categories><subj-group subj-group-type="heading"><subject>PNAS Plus</subject></subj-group><subj-group subj-group-type="heading"><subject>Physical Sciences</subject><subj-group><subject>Biophysics and Computational Biology</subject></subj-group></subj-group><subj-group subj-group-type="heading"><subject>Biological Sciences</subject><subj-group><subject>Microbiology</subject></subj-group></subj-group><series-title>PNAS Plus</series-title></article-categories><title-group><article-title>Cell morphology drives spatial patterning in microbial communities</article-title><alt-title alt-title-type="short">Microbial shape drives patterning in communities</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Smith</surname><given-names>William P. J.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Davit</surname><given-names>Yohan</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref></contrib><contrib contrib-type="author"><name><surname>Osborne</surname><given-names>James M.</given-names></name><xref ref-type="aff" rid="aff3"><sup>c</sup></xref></contrib><contrib contrib-type="author"><name><surname>Kim</surname><given-names>Wook</given-names></name><xref ref-type="aff" rid="aff4"><sup>d</sup></xref><xref ref-type="author-notes" rid="fn1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0003-4687-6633</contrib-id><name><surname>Foster</surname><given-names>Kevin R.</given-names></name><xref ref-type="aff" rid="aff4"><sup>d</sup></xref><xref ref-type="corresp" rid="cor1"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Pitt-Francis</surname><given-names>Joe M.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="corresp" rid="cor1"><sup>2</sup></xref></contrib><aff id="aff1"><sup>a</sup>Department of Computer Science,<institution>University of Oxford</institution>, Oxford OX1 3QD,<country>United Kingdom</country>;</aff><aff id="aff2"><sup>b</sup><institution>Institut de Mécanique des Fluides de Toulouse (IMFT)</institution>, Université de Toulouse, Centre National de la Recherche Scientifique (CNRS), Institut National Polytechnique de Toulouse (INPT), Université Paul Sabatier (UPS), F-31400 Toulouse,<country>France</country>;</aff><aff id="aff3"><sup>c</sup>School of Mathematics and Statistics,<institution>University of Melbourne</institution>, VIC 3010,<country>Australia</country>;</aff><aff id="aff4"><sup>d</sup>Department of Zoology,<institution>University of Oxford</institution>, Oxford OX1 3PS,<country>United Kingdom</country></aff></contrib-group><author-notes><corresp id="cor1"><sup>2</sup>To whom correspondence may be addressed. Email: <email>kevin.foster@zoo.ox.ac.uk</email> or <email>joe.pitt-francis@cs.ox.ac.uk</email>.</corresp><fn fn-type="edited-by"><p>Edited by Roman Stocker, Eidgenössische Technische Hochschule Zürich, Zurich, Switzerland, and accepted by Editorial Board Member Edward F. DeLong November 15, 2016 (received for review August 5, 2016)</p></fn><fn fn-type="con"><p>Author contributions: W.P.J.S., Y.D., J.M.O., K.R.F., and J.M.P.-F. designed research; W.P.J.S. and W.K. performed research; W.P.J.S., Y.D., J.M.O., W.K., K.R.F., and J.M.P.-F. analyzed data; and W.P.J.S., Y.D., J.M.O., W.K., K.R.F., and J.M.P.-F. wrote the paper.</p></fn><fn fn-type="present-address" id="fn1"><p><sup>1</sup>Present address: Department of Biological Sciences, Duquesne University, Pittsburgh, PA 15282.</p></fn></author-notes><pub-date pub-type="ppub"><day>17</day><month>1</month><year>2017</year></pub-date><pub-date pub-type="epub"><day>30</day><month>12</month><year>2016</year></pub-date><volume>114</volume><issue>3</issue><fpage>E280</fpage><lpage>E286</lpage><permissions></permissions><self-uri xlink:title="pdf" xlink:href="pnas.201613007.pdf"></self-uri><abstract abstract-type="executive-summary"><title>Significance</title><p>Microbial communities contain cells of different shapes, and yet we know little about how these shapes affect community biology. We have developed a computational model to study the effects of microbial shape in communities. Our model predicts that shape will have strong effects on cells’ positioning, and, consequently, their survival and reproduction. Rod-shaped cells are better at colonizing the base of the community and its expanding edges, whereas round cells dominate the upper surface. We show that the same patterns occur in colonies of <italic>Escherichia coli</italic>, using strains with different shapes. Our work suggests that cell shape is a major determinant of patterning and evolutionary fitness within microbial communities.</p></abstract><abstract><p>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 <italic>Escherichia coli</italic> 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.</p></abstract><kwd-group><kwd>biofilms</kwd><kwd>cell morphology</kwd><kwd>biophysics</kwd><kwd>self-organization</kwd><kwd>synthetic biology</kwd></kwd-group><funding-group><award-group id="gs1"><funding-source id="sp1">Engineering and Physical Sciences Research Council (EPSRC)<named-content content-type="funder-id">501100000266</named-content></funding-source><award-id rid="sp1">EP/G03706X/1</award-id></award-group><award-group id="gs2"><funding-source id="sp2">EC | European Research Council (ERC)<named-content content-type="funder-id">501100000781</named-content></funding-source><award-id rid="sp2">242670</award-id></award-group><award-group id="gs3"><funding-source id="sp3">EC | European Research Council (ERC)<named-content content-type="funder-id">501100000781</named-content></funding-source><award-id rid="sp3">242670</award-id></award-group></funding-group><counts><page-count count="7"></page-count></counts></article-meta></front></pmc><affiliations><list><country><li>Australie</li><li>France</li><li>Royaume-Uni</li></country></list><tree><country name="Royaume-Uni"><noRegion><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></noRegion><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"><noRegion><name sortKey="Osborne, James M" sort="Osborne, James M" uniqKey="Osborne J" first="James M." last="Osborne">James M. Osborne</name></noRegion></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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