Cell morphology drives spatial patterning in microbial communities
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 com...
Gespeichert in:
| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2017-01, Vol.114 (3), p.E280-E286 |
|---|---|
| Hauptverfasser: | , , , , , |
| Format: | Artikel |
| Sprache: | eng |
| Schlagworte: | |
| Online-Zugang: | Volltext |
| Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
| container_end_page | E286 |
|---|---|
| container_issue | 3 |
| container_start_page | E280 |
| container_title | Proceedings of the National Academy of Sciences - PNAS |
| container_volume | 114 |
| creator | Smith, William P. J. Davit, Yohan Osborne, James M. Kim, Wook Foster, Kevin R. Pitt-Francis, Joe M. |
| description | 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_str_mv | 10.1073/pnas.1613007114 |
| format | Article |
| fullrecord | <record><control><sourceid>jstor_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_5255625</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><jstor_id>26479004</jstor_id><sourcerecordid>26479004</sourcerecordid><originalsourceid>FETCH-LOGICAL-c477t-2f07664b4d3ebb6b41bc2fc4bc1dc8adf7880c7c5680b27615df233018bc0fa93</originalsourceid><addsrcrecordid>eNpdkc1v1DAQxS0EotvCmRMoEhc4pB1_J5dKZVUo0kpc4GzZjrPrVRIHO1mp_z2OUlroaaSZ3zyP30PoHYZLDJJejYNOl1hgCiAxZi_QBkONS8FqeIk2AESWFSPsDJ2ndASAmlfwGp2RCmjNqNigL1vXdUUf4ngIXdjfF030J5eKNOrJ667IZXJx8MO-8EPRexuDWfo29P08-Mm79Aa9anWX3NuHeoF-fb39ub0rdz--fd_e7ErLpJxK0oIUghnWUGeMMAwbS1rLjMWNrXTTyqoCKy0XFRgiBeZNSygFXBkLra7pBbpedcfZ9K6xbpii7tQYfa_jvQraq_8ngz-ofTgpTjgXhGeBz6vA4dna3c1OLT2gHHOQ5IQz--nhsRh-zy5NqvfJZq_04MKcFK44y7ZTwTL68Rl6DHMcshWZWhm8UFcrlR1MKbr28QIMaslSLVmqpyzzxod___vI_w0vA-9X4JimEJ_mgskagNE_Z7ykfw</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1861336414</pqid></control><display><type>article</type><title>Cell morphology drives spatial patterning in microbial communities</title><source>MEDLINE</source><source>JSTOR Archive Collection A-Z Listing</source><source>PubMed Central</source><source>Alma/SFX Local Collection</source><source>Free Full-Text Journals in Chemistry</source><creator>Smith, William P. J. ; Davit, Yohan ; Osborne, James M. ; Kim, Wook ; Foster, Kevin R. ; Pitt-Francis, Joe M.</creator><creatorcontrib>Smith, William P. J. ; Davit, Yohan ; Osborne, James M. ; Kim, Wook ; Foster, Kevin R. ; Pitt-Francis, Joe M.</creatorcontrib><description>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.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1613007114</identifier><identifier>PMID: 28039436</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Bioengineering ; Biofilms ; Biological Sciences ; Biophysical Phenomena ; Cells ; Computer Simulation ; Engineering Sciences ; Escherichia coli - cytology ; Escherichia coli - genetics ; Escherichia coli - growth & development ; Escherichia coli Proteins - genetics ; Fluids mechanics ; Mechanics ; Microbial Consortia - genetics ; Microbial Consortia - physiology ; Microorganisms ; Models, Biological ; Morphology ; Mutation ; Phenotype ; Physical Sciences ; PNAS Plus ; Synthetic Biology</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2017-01, Vol.114 (3), p.E280-E286</ispartof><rights>Volumes 1–89 and 106–113, copyright as a collective work only; author(s) retains copyright to individual articles</rights><rights>Copyright National Academy of Sciences Jan 17, 2017</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c477t-2f07664b4d3ebb6b41bc2fc4bc1dc8adf7880c7c5680b27615df233018bc0fa93</citedby><cites>FETCH-LOGICAL-c477t-2f07664b4d3ebb6b41bc2fc4bc1dc8adf7880c7c5680b27615df233018bc0fa93</cites><orcidid>0000-0003-4687-6633</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26479004$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26479004$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,803,885,27924,27925,53791,53793,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28039436$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-03515072$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Smith, William P. J.</creatorcontrib><creatorcontrib>Davit, Yohan</creatorcontrib><creatorcontrib>Osborne, James M.</creatorcontrib><creatorcontrib>Kim, Wook</creatorcontrib><creatorcontrib>Foster, Kevin R.</creatorcontrib><creatorcontrib>Pitt-Francis, Joe M.</creatorcontrib><title>Cell morphology drives spatial patterning in microbial communities</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>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.</description><subject>Bioengineering</subject><subject>Biofilms</subject><subject>Biological Sciences</subject><subject>Biophysical Phenomena</subject><subject>Cells</subject><subject>Computer Simulation</subject><subject>Engineering Sciences</subject><subject>Escherichia coli - cytology</subject><subject>Escherichia coli - genetics</subject><subject>Escherichia coli - growth & development</subject><subject>Escherichia coli Proteins - genetics</subject><subject>Fluids mechanics</subject><subject>Mechanics</subject><subject>Microbial Consortia - genetics</subject><subject>Microbial Consortia - physiology</subject><subject>Microorganisms</subject><subject>Models, Biological</subject><subject>Morphology</subject><subject>Mutation</subject><subject>Phenotype</subject><subject>Physical Sciences</subject><subject>PNAS Plus</subject><subject>Synthetic Biology</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkc1v1DAQxS0EotvCmRMoEhc4pB1_J5dKZVUo0kpc4GzZjrPrVRIHO1mp_z2OUlroaaSZ3zyP30PoHYZLDJJejYNOl1hgCiAxZi_QBkONS8FqeIk2AESWFSPsDJ2ndASAmlfwGp2RCmjNqNigL1vXdUUf4ngIXdjfF030J5eKNOrJ667IZXJx8MO-8EPRexuDWfo29P08-Mm79Aa9anWX3NuHeoF-fb39ub0rdz--fd_e7ErLpJxK0oIUghnWUGeMMAwbS1rLjMWNrXTTyqoCKy0XFRgiBeZNSygFXBkLra7pBbpedcfZ9K6xbpii7tQYfa_jvQraq_8ngz-ofTgpTjgXhGeBz6vA4dna3c1OLT2gHHOQ5IQz--nhsRh-zy5NqvfJZq_04MKcFK44y7ZTwTL68Rl6DHMcshWZWhm8UFcrlR1MKbr28QIMaslSLVmqpyzzxod___vI_w0vA-9X4JimEJ_mgskagNE_Z7ykfw</recordid><startdate>20170117</startdate><enddate>20170117</enddate><creator>Smith, William P. J.</creator><creator>Davit, Yohan</creator><creator>Osborne, James M.</creator><creator>Kim, Wook</creator><creator>Foster, Kevin R.</creator><creator>Pitt-Francis, Joe M.</creator><general>National Academy of Sciences</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-4687-6633</orcidid></search><sort><creationdate>20170117</creationdate><title>Cell morphology drives spatial patterning in microbial communities</title><author>Smith, William P. J. ; Davit, Yohan ; Osborne, James M. ; Kim, Wook ; Foster, Kevin R. ; Pitt-Francis, Joe M.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c477t-2f07664b4d3ebb6b41bc2fc4bc1dc8adf7880c7c5680b27615df233018bc0fa93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Bioengineering</topic><topic>Biofilms</topic><topic>Biological Sciences</topic><topic>Biophysical Phenomena</topic><topic>Cells</topic><topic>Computer Simulation</topic><topic>Engineering Sciences</topic><topic>Escherichia coli - cytology</topic><topic>Escherichia coli - genetics</topic><topic>Escherichia coli - growth & development</topic><topic>Escherichia coli Proteins - genetics</topic><topic>Fluids mechanics</topic><topic>Mechanics</topic><topic>Microbial Consortia - genetics</topic><topic>Microbial Consortia - physiology</topic><topic>Microorganisms</topic><topic>Models, Biological</topic><topic>Morphology</topic><topic>Mutation</topic><topic>Phenotype</topic><topic>Physical Sciences</topic><topic>PNAS Plus</topic><topic>Synthetic Biology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Smith, William P. J.</creatorcontrib><creatorcontrib>Davit, Yohan</creatorcontrib><creatorcontrib>Osborne, James M.</creatorcontrib><creatorcontrib>Kim, Wook</creatorcontrib><creatorcontrib>Foster, Kevin R.</creatorcontrib><creatorcontrib>Pitt-Francis, Joe M.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Smith, William P. J.</au><au>Davit, Yohan</au><au>Osborne, James M.</au><au>Kim, Wook</au><au>Foster, Kevin R.</au><au>Pitt-Francis, Joe M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cell morphology drives spatial patterning in microbial communities</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2017-01-17</date><risdate>2017</risdate><volume>114</volume><issue>3</issue><spage>E280</spage><epage>E286</epage><pages>E280-E286</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><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.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>28039436</pmid><doi>10.1073/pnas.1613007114</doi><orcidid>https://orcid.org/0000-0003-4687-6633</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0027-8424 |
| ispartof | Proceedings of the National Academy of Sciences - PNAS, 2017-01, Vol.114 (3), p.E280-E286 |
| issn | 0027-8424 1091-6490 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_5255625 |
| source | MEDLINE; JSTOR Archive Collection A-Z Listing; PubMed Central; Alma/SFX Local Collection; Free Full-Text Journals in Chemistry |
| subjects | Bioengineering Biofilms Biological Sciences Biophysical Phenomena Cells Computer Simulation Engineering Sciences Escherichia coli - cytology Escherichia coli - genetics Escherichia coli - growth & development Escherichia coli Proteins - genetics Fluids mechanics Mechanics Microbial Consortia - genetics Microbial Consortia - physiology Microorganisms Models, Biological Morphology Mutation Phenotype Physical Sciences PNAS Plus Synthetic Biology |
| title | Cell morphology drives spatial patterning in microbial communities |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-03T11%3A38%3A36IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-jstor_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Cell%20morphology%20drives%20spatial%20patterning%20in%20microbial%20communities&rft.jtitle=Proceedings%20of%20the%20National%20Academy%20of%20Sciences%20-%20PNAS&rft.au=Smith,%20William%20P.%20J.&rft.date=2017-01-17&rft.volume=114&rft.issue=3&rft.spage=E280&rft.epage=E286&rft.pages=E280-E286&rft.issn=0027-8424&rft.eissn=1091-6490&rft_id=info:doi/10.1073/pnas.1613007114&rft_dat=%3Cjstor_pubme%3E26479004%3C/jstor_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1861336414&rft_id=info:pmid/28039436&rft_jstor_id=26479004&rfr_iscdi=true |