An off-lattice discrete model to characterise filamentous yeast colony morphology
We combine an off-lattice agent-based mathematical model and experimentation to explore filamentous growth of a yeast colony. Under environmental stress, Saccharomyces cerevisiae yeast cells can transition from a bipolar (sated) to unipolar (pseudohyphal) budding mechanism, where cells elongate and...
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creator | Li, Kai Green, J Edward F Tronnolone, Hayden Tam, Alexander K Y Black, Andrew J Gardner, Jennifer M Sundstrom, Joanna F Jiranek, Vladimir Binder, Benjamin J |
description | We combine an off-lattice agent-based mathematical model and experimentation to explore filamentous growth of a yeast colony. Under environmental stress, Saccharomyces cerevisiae yeast cells can transition from a bipolar (sated) to unipolar (pseudohyphal) budding mechanism, where cells elongate and bud end-to-end. This budding asymmetry yields spatially non-uniform growth, where filaments extend away from the colony centre, foraging for food. We use approximate Bayesian computation to quantify how individual cell budding mechanisms give rise to spatial patterns observed in experiments. We apply this method of parameter inference to experimental images of colonies of two strains of S. cerevisiae, in low and high nutrient environments. The colony size at the transition from sated to pseudohyphal growth, and a forking mechanism for pseudohyphal cell proliferation are the key features driving colony morphology. Simulations run with the most likely inferred parameters produce colony morphologies that closely resemble experimental results. |
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Under environmental stress, Saccharomyces cerevisiae yeast cells can transition from a bipolar (sated) to unipolar (pseudohyphal) budding mechanism, where cells elongate and bud end-to-end. This budding asymmetry yields spatially non-uniform growth, where filaments extend away from the colony centre, foraging for food. We use approximate Bayesian computation to quantify how individual cell budding mechanisms give rise to spatial patterns observed in experiments. We apply this method of parameter inference to experimental images of colonies of two strains of S. cerevisiae, in low and high nutrient environments. The colony size at the transition from sated to pseudohyphal growth, and a forking mechanism for pseudohyphal cell proliferation are the key features driving colony morphology. Simulations run with the most likely inferred parameters produce colony morphologies that closely resemble experimental results.</description><identifier>ISSN: 1553-7358</identifier><identifier>ISSN: 1553-734X</identifier><identifier>EISSN: 1553-7358</identifier><identifier>DOI: 10.1371/journal.pcbi.1012605</identifier><identifier>PMID: 39570980</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Bayes Theorem ; Biology and Life Sciences ; Computational Biology ; Computer Simulation ; Mathematical models ; Medicine and Health Sciences ; Microbial colonies ; Models, Biological ; Physical Sciences ; Research and Analysis Methods ; Saccharomyces cerevisiae - cytology ; Saccharomyces cerevisiae - growth & development ; Simulation methods ; Yeast fungi</subject><ispartof>PLoS computational biology, 2024-11, Vol.20 (11), p.e1012605</ispartof><rights>Copyright: © 2024 Li et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2024 Public Library of Science</rights><rights>2024 Li et al 2024 Li et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c461t-3079b1917d3028acf52a895f0b6fb96a727d9a68ce97631b927dc13b2abbd7543</cites><orcidid>0000-0001-5061-9563 ; 0000-0002-9775-8963 ; 0000-0002-4898-3101</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11620580/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11620580/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39570980$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Csikász-Nagy, Attila</contributor><creatorcontrib>Li, Kai</creatorcontrib><creatorcontrib>Green, J Edward F</creatorcontrib><creatorcontrib>Tronnolone, Hayden</creatorcontrib><creatorcontrib>Tam, Alexander K Y</creatorcontrib><creatorcontrib>Black, Andrew J</creatorcontrib><creatorcontrib>Gardner, Jennifer M</creatorcontrib><creatorcontrib>Sundstrom, Joanna F</creatorcontrib><creatorcontrib>Jiranek, Vladimir</creatorcontrib><creatorcontrib>Binder, Benjamin J</creatorcontrib><title>An off-lattice discrete model to characterise filamentous yeast colony morphology</title><title>PLoS computational biology</title><addtitle>PLoS Comput Biol</addtitle><description>We combine an off-lattice agent-based mathematical model and experimentation to explore filamentous growth of a yeast colony. Under environmental stress, Saccharomyces cerevisiae yeast cells can transition from a bipolar (sated) to unipolar (pseudohyphal) budding mechanism, where cells elongate and bud end-to-end. This budding asymmetry yields spatially non-uniform growth, where filaments extend away from the colony centre, foraging for food. We use approximate Bayesian computation to quantify how individual cell budding mechanisms give rise to spatial patterns observed in experiments. We apply this method of parameter inference to experimental images of colonies of two strains of S. cerevisiae, in low and high nutrient environments. The colony size at the transition from sated to pseudohyphal growth, and a forking mechanism for pseudohyphal cell proliferation are the key features driving colony morphology. Simulations run with the most likely inferred parameters produce colony morphologies that closely resemble experimental results.</description><subject>Bayes Theorem</subject><subject>Biology and Life Sciences</subject><subject>Computational Biology</subject><subject>Computer Simulation</subject><subject>Mathematical models</subject><subject>Medicine and Health Sciences</subject><subject>Microbial colonies</subject><subject>Models, Biological</subject><subject>Physical Sciences</subject><subject>Research and Analysis Methods</subject><subject>Saccharomyces cerevisiae - cytology</subject><subject>Saccharomyces cerevisiae - growth & development</subject><subject>Simulation methods</subject><subject>Yeast fungi</subject><issn>1553-7358</issn><issn>1553-734X</issn><issn>1553-7358</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>DOA</sourceid><recordid>eNqVkk-P0zAQxSMEYpeFb4BQjnBIseM4tk-oWsFSaQXi39kaO5M2lRMX21nRb78uLavtEfngsf3eT57RK4rXlCwoE_T91s9hArfYWTMsKKF1S_iT4pJyzirBuHz6qL4oXsS4JSSXqn1eXDDFBVGSXBbfllPp-75ykNJgseyGaAMmLEffoSuTL-0GAtiEYYhY9oODEafk51juEWIqrXd-2md52G1yud6_LJ714CK-Ou1Xxa9PH39ef65uv96srpe3lW1amipGhDJUUdExUkuwPa9BKt4T0_ZGtSBq0SlopUUlWkaNymdLmanBmE7whl0VqyO387DVuzCMEPbaw6D_Xviw1hByTw41y4CmNgxAmMZ0ygACNwoMCGYYHlgfjqzdbEbsbO4wgDuDnr9Mw0av_Z2mtK0JlyQT3p4Iwf-eMSY95kmiczBhHpZmlFHZyJrTLF0cpWvIfxum3mekzavDcbB-wjxk1EtJpaobJlk2vDszZE3CP2kNc4x69eP7f2i_nGubo9YGH2PA_qFhSvQhY_qUMX3ImD5lLNvePB7Wg-lfqNg9yLfQwA</recordid><startdate>20241121</startdate><enddate>20241121</enddate><creator>Li, Kai</creator><creator>Green, J Edward F</creator><creator>Tronnolone, Hayden</creator><creator>Tam, Alexander K Y</creator><creator>Black, Andrew J</creator><creator>Gardner, Jennifer M</creator><creator>Sundstrom, Joanna F</creator><creator>Jiranek, Vladimir</creator><creator>Binder, Benjamin J</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>ISN</scope><scope>ISR</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-5061-9563</orcidid><orcidid>https://orcid.org/0000-0002-9775-8963</orcidid><orcidid>https://orcid.org/0000-0002-4898-3101</orcidid></search><sort><creationdate>20241121</creationdate><title>An off-lattice discrete model to characterise filamentous yeast colony morphology</title><author>Li, Kai ; Green, J Edward F ; Tronnolone, Hayden ; Tam, Alexander K Y ; Black, Andrew J ; Gardner, Jennifer M ; Sundstrom, Joanna F ; Jiranek, Vladimir ; Binder, Benjamin J</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c461t-3079b1917d3028acf52a895f0b6fb96a727d9a68ce97631b927dc13b2abbd7543</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Bayes Theorem</topic><topic>Biology and Life Sciences</topic><topic>Computational Biology</topic><topic>Computer Simulation</topic><topic>Mathematical models</topic><topic>Medicine and Health Sciences</topic><topic>Microbial colonies</topic><topic>Models, Biological</topic><topic>Physical Sciences</topic><topic>Research and Analysis Methods</topic><topic>Saccharomyces cerevisiae - cytology</topic><topic>Saccharomyces cerevisiae - growth & development</topic><topic>Simulation methods</topic><topic>Yeast fungi</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Li, Kai</creatorcontrib><creatorcontrib>Green, J Edward F</creatorcontrib><creatorcontrib>Tronnolone, Hayden</creatorcontrib><creatorcontrib>Tam, Alexander K Y</creatorcontrib><creatorcontrib>Black, Andrew J</creatorcontrib><creatorcontrib>Gardner, Jennifer M</creatorcontrib><creatorcontrib>Sundstrom, Joanna F</creatorcontrib><creatorcontrib>Jiranek, Vladimir</creatorcontrib><creatorcontrib>Binder, Benjamin J</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS computational biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Li, Kai</au><au>Green, J Edward F</au><au>Tronnolone, Hayden</au><au>Tam, Alexander K Y</au><au>Black, Andrew J</au><au>Gardner, Jennifer M</au><au>Sundstrom, Joanna F</au><au>Jiranek, Vladimir</au><au>Binder, Benjamin J</au><au>Csikász-Nagy, Attila</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>An off-lattice discrete model to characterise filamentous yeast colony morphology</atitle><jtitle>PLoS computational biology</jtitle><addtitle>PLoS Comput Biol</addtitle><date>2024-11-21</date><risdate>2024</risdate><volume>20</volume><issue>11</issue><spage>e1012605</spage><pages>e1012605-</pages><issn>1553-7358</issn><issn>1553-734X</issn><eissn>1553-7358</eissn><abstract>We combine an off-lattice agent-based mathematical model and experimentation to explore filamentous growth of a yeast colony. Under environmental stress, Saccharomyces cerevisiae yeast cells can transition from a bipolar (sated) to unipolar (pseudohyphal) budding mechanism, where cells elongate and bud end-to-end. This budding asymmetry yields spatially non-uniform growth, where filaments extend away from the colony centre, foraging for food. We use approximate Bayesian computation to quantify how individual cell budding mechanisms give rise to spatial patterns observed in experiments. We apply this method of parameter inference to experimental images of colonies of two strains of S. cerevisiae, in low and high nutrient environments. The colony size at the transition from sated to pseudohyphal growth, and a forking mechanism for pseudohyphal cell proliferation are the key features driving colony morphology. Simulations run with the most likely inferred parameters produce colony morphologies that closely resemble experimental results.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>39570980</pmid><doi>10.1371/journal.pcbi.1012605</doi><tpages>e1012605</tpages><orcidid>https://orcid.org/0000-0001-5061-9563</orcidid><orcidid>https://orcid.org/0000-0002-9775-8963</orcidid><orcidid>https://orcid.org/0000-0002-4898-3101</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Bayes Theorem Biology and Life Sciences Computational Biology Computer Simulation Mathematical models Medicine and Health Sciences Microbial colonies Models, Biological Physical Sciences Research and Analysis Methods Saccharomyces cerevisiae - cytology Saccharomyces cerevisiae - growth & development Simulation methods Yeast fungi |
title | An off-lattice discrete model to characterise filamentous yeast colony morphology |
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