Loading…

From Genes to Ecosystems in Microbiology: Modeling Approaches and the Importance of Individuality

Models are important tools in microbial ecology. They can be used to advance understanding by helping to interpret observations and test hypotheses, and to predict the effects of ecosystem management actions or a different climate. Over the past decades, biological knowledge and ecosystem observatio...

Full description

Saved in:
Bibliographic Details
Published in:Frontiers in microbiology 2017-11, Vol.8, p.2299-2299
Main Authors: Kreft, Jan-Ulrich, Plugge, Caroline M, Prats, Clara, Leveau, Johan H J, Zhang, Weiwen, Hellweger, Ferdi L
Format: Article
Language:English
Subjects:
Citations: Items that this one cites
Items that cite this one
Online Access:Get full text
Tags: Add Tag
No Tags, Be the first to tag this record!
cited_by cdi_FETCH-LOGICAL-c555t-ac89d19418ec367cfb97d7e587b0dd5a189af099abe6b4da3624acf5e09d7a393
cites cdi_FETCH-LOGICAL-c555t-ac89d19418ec367cfb97d7e587b0dd5a189af099abe6b4da3624acf5e09d7a393
container_end_page 2299
container_issue
container_start_page 2299
container_title Frontiers in microbiology
container_volume 8
creator Kreft, Jan-Ulrich
Plugge, Caroline M
Prats, Clara
Leveau, Johan H J
Zhang, Weiwen
Hellweger, Ferdi L
description Models are important tools in microbial ecology. They can be used to advance understanding by helping to interpret observations and test hypotheses, and to predict the effects of ecosystem management actions or a different climate. Over the past decades, biological knowledge and ecosystem observations have advanced to the molecular and in particular gene level. However, microbial ecology models have changed less and a current challenge is to make them utilize the knowledge and observations at the genetic level. We review published models that explicitly consider genes and make predictions at the population or ecosystem level. The models can be grouped into three general approaches, i.e., metabolic flux, gene-centric and agent-based. We describe and contrast these approaches by applying them to a hypothetical ecosystem and discuss their strengths and weaknesses. An important distinguishing feature is how variation between individual cells (individuality) is handled. In microbial ecosystems, individual heterogeneity is generated by a number of mechanisms including stochastic interactions of molecules (e.g., gene expression), stochastic and deterministic cell division asymmetry, small-scale environmental heterogeneity, and differential transport in a heterogeneous environment. This heterogeneity can then be amplified and transferred to other cell properties by several mechanisms, including nutrient uptake, metabolism and growth, cell cycle asynchronicity and the effects of age and damage. For example, stochastic gene expression may lead to heterogeneity in nutrient uptake enzyme levels, which in turn results in heterogeneity in intracellular nutrient levels. Individuality can have important ecological consequences, including division of labor, bet hedging, aging and sub-optimality. Understanding the importance of individuality and the mechanism(s) underlying it for the specific microbial system and question investigated is essential for selecting the optimal modeling strategy.
doi_str_mv 10.3389/fmicb.2017.02299
format article
fullrecord <record><control><sourceid>proquest_doaj_</sourceid><recordid>TN_cdi_doaj_primary_oai_doaj_org_article_c85f8318f8af45a8ae96935ae0210926</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><doaj_id>oai_doaj_org_article_c85f8318f8af45a8ae96935ae0210926</doaj_id><sourcerecordid>1975998152</sourcerecordid><originalsourceid>FETCH-LOGICAL-c555t-ac89d19418ec367cfb97d7e587b0dd5a189af099abe6b4da3624acf5e09d7a393</originalsourceid><addsrcrecordid>eNpVkk1r3DAQhk1paUKae0_Fx152qw_LlnIohJCkCwm9tNCbGEvjXQVb2kp2wv77yrvbJRFIM_p4nxnBWxSfKVlyLtW3bnCmXTJCmyVhTKl3xTmt62rBCfvz_lV-Vlym9ETyqAjL68fijCnG5_y8gLsYhvIePaZyDOWtCWmXRhxS6Xz56EwMrQt9WO-uysdgsXd-XV5vtzGA2WQJeFuOGyxXwzbEEbzBMnTlylv37OwEvRt3n4oPHfQJL4_xovh9d_vr5sfi4ef96ub6YWGEEOMCjFSWqopKNLxuTNeqxjYoZNMSawVQqaAjSkGLdVtZ4DWrwHQCibINcMUvitWBawM86W10A8SdDuD0_iDEtYY4OtOjNlJ0klPZSegqARJQ1YoLQMIoUazOrKsD6wXW6POf0WsP0bi0B_aujTP8ZYra93PYTm3SgpOq4ln8_SDOhwNag36M0L_p6O2Ndxu9Ds9aNJRKLjKAHgAmTUZHNBgNjHvhaTNPRhqmc01Vz0W_HovG8HfCNOrBJYN9Dx7DlDRVjVBKUsHyU3LEx5BSxO7UGiV6dpbeO0vPztJ7Z2XJl9dfOgn--4j_AzcZzaI</addsrcrecordid><sourcetype>Open Website</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1975998152</pqid></control><display><type>article</type><title>From Genes to Ecosystems in Microbiology: Modeling Approaches and the Importance of Individuality</title><source>PubMed Central</source><creator>Kreft, Jan-Ulrich ; Plugge, Caroline M ; Prats, Clara ; Leveau, Johan H J ; Zhang, Weiwen ; Hellweger, Ferdi L</creator><creatorcontrib>Kreft, Jan-Ulrich ; Plugge, Caroline M ; Prats, Clara ; Leveau, Johan H J ; Zhang, Weiwen ; Hellweger, Ferdi L</creatorcontrib><description>Models are important tools in microbial ecology. They can be used to advance understanding by helping to interpret observations and test hypotheses, and to predict the effects of ecosystem management actions or a different climate. Over the past decades, biological knowledge and ecosystem observations have advanced to the molecular and in particular gene level. However, microbial ecology models have changed less and a current challenge is to make them utilize the knowledge and observations at the genetic level. We review published models that explicitly consider genes and make predictions at the population or ecosystem level. The models can be grouped into three general approaches, i.e., metabolic flux, gene-centric and agent-based. We describe and contrast these approaches by applying them to a hypothetical ecosystem and discuss their strengths and weaknesses. An important distinguishing feature is how variation between individual cells (individuality) is handled. In microbial ecosystems, individual heterogeneity is generated by a number of mechanisms including stochastic interactions of molecules (e.g., gene expression), stochastic and deterministic cell division asymmetry, small-scale environmental heterogeneity, and differential transport in a heterogeneous environment. This heterogeneity can then be amplified and transferred to other cell properties by several mechanisms, including nutrient uptake, metabolism and growth, cell cycle asynchronicity and the effects of age and damage. For example, stochastic gene expression may lead to heterogeneity in nutrient uptake enzyme levels, which in turn results in heterogeneity in intracellular nutrient levels. Individuality can have important ecological consequences, including division of labor, bet hedging, aging and sub-optimality. Understanding the importance of individuality and the mechanism(s) underlying it for the specific microbial system and question investigated is essential for selecting the optimal modeling strategy.</description><identifier>ISSN: 1664-302X</identifier><identifier>EISSN: 1664-302X</identifier><identifier>DOI: 10.3389/fmicb.2017.02299</identifier><identifier>PMID: 29230200</identifier><language>eng</language><publisher>Switzerland: Frontiers Media S.A</publisher><subject>Agent-based modeling ; Ciències de la terra i de la vida ; Enginyeria agroalimentària ; Gene-centric modeling ; Genètica microbiana ; Heterogeneity ; Individuality ; Metabolic flux modeling ; Microbial ecology ; Microbial genetics ; Microbiologia ; Microbiology ; Single cell ; Àrees temàtiques de la UPC</subject><ispartof>Frontiers in microbiology, 2017-11, Vol.8, p.2299-2299</ispartof><rights>Attribution-NonCommercial 3.0 Spain info:eu-repo/semantics/openAccess &lt;a href="http://creativecommons.org/licenses/by-nc/3.0/es/"&gt;http://creativecommons.org/licenses/by-nc/3.0/es/&lt;/a&gt;</rights><rights>Copyright © 2017 Kreft, Plugge, Prats, Leveau, Zhang and Hellweger. 2017 Kreft, Plugge, Prats, Leveau, Zhang and Hellweger</rights><rights>Wageningen University &amp; Research</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c555t-ac89d19418ec367cfb97d7e587b0dd5a189af099abe6b4da3624acf5e09d7a393</citedby><cites>FETCH-LOGICAL-c555t-ac89d19418ec367cfb97d7e587b0dd5a189af099abe6b4da3624acf5e09d7a393</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5711835/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5711835/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,27903,27904,53769,53771</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29230200$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kreft, Jan-Ulrich</creatorcontrib><creatorcontrib>Plugge, Caroline M</creatorcontrib><creatorcontrib>Prats, Clara</creatorcontrib><creatorcontrib>Leveau, Johan H J</creatorcontrib><creatorcontrib>Zhang, Weiwen</creatorcontrib><creatorcontrib>Hellweger, Ferdi L</creatorcontrib><title>From Genes to Ecosystems in Microbiology: Modeling Approaches and the Importance of Individuality</title><title>Frontiers in microbiology</title><addtitle>Front Microbiol</addtitle><description>Models are important tools in microbial ecology. They can be used to advance understanding by helping to interpret observations and test hypotheses, and to predict the effects of ecosystem management actions or a different climate. Over the past decades, biological knowledge and ecosystem observations have advanced to the molecular and in particular gene level. However, microbial ecology models have changed less and a current challenge is to make them utilize the knowledge and observations at the genetic level. We review published models that explicitly consider genes and make predictions at the population or ecosystem level. The models can be grouped into three general approaches, i.e., metabolic flux, gene-centric and agent-based. We describe and contrast these approaches by applying them to a hypothetical ecosystem and discuss their strengths and weaknesses. An important distinguishing feature is how variation between individual cells (individuality) is handled. In microbial ecosystems, individual heterogeneity is generated by a number of mechanisms including stochastic interactions of molecules (e.g., gene expression), stochastic and deterministic cell division asymmetry, small-scale environmental heterogeneity, and differential transport in a heterogeneous environment. This heterogeneity can then be amplified and transferred to other cell properties by several mechanisms, including nutrient uptake, metabolism and growth, cell cycle asynchronicity and the effects of age and damage. For example, stochastic gene expression may lead to heterogeneity in nutrient uptake enzyme levels, which in turn results in heterogeneity in intracellular nutrient levels. Individuality can have important ecological consequences, including division of labor, bet hedging, aging and sub-optimality. Understanding the importance of individuality and the mechanism(s) underlying it for the specific microbial system and question investigated is essential for selecting the optimal modeling strategy.</description><subject>Agent-based modeling</subject><subject>Ciències de la terra i de la vida</subject><subject>Enginyeria agroalimentària</subject><subject>Gene-centric modeling</subject><subject>Genètica microbiana</subject><subject>Heterogeneity</subject><subject>Individuality</subject><subject>Metabolic flux modeling</subject><subject>Microbial ecology</subject><subject>Microbial genetics</subject><subject>Microbiologia</subject><subject>Microbiology</subject><subject>Single cell</subject><subject>Àrees temàtiques de la UPC</subject><issn>1664-302X</issn><issn>1664-302X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>DOA</sourceid><recordid>eNpVkk1r3DAQhk1paUKae0_Fx152qw_LlnIohJCkCwm9tNCbGEvjXQVb2kp2wv77yrvbJRFIM_p4nxnBWxSfKVlyLtW3bnCmXTJCmyVhTKl3xTmt62rBCfvz_lV-Vlym9ETyqAjL68fijCnG5_y8gLsYhvIePaZyDOWtCWmXRhxS6Xz56EwMrQt9WO-uysdgsXd-XV5vtzGA2WQJeFuOGyxXwzbEEbzBMnTlylv37OwEvRt3n4oPHfQJL4_xovh9d_vr5sfi4ef96ub6YWGEEOMCjFSWqopKNLxuTNeqxjYoZNMSawVQqaAjSkGLdVtZ4DWrwHQCibINcMUvitWBawM86W10A8SdDuD0_iDEtYY4OtOjNlJ0klPZSegqARJQ1YoLQMIoUazOrKsD6wXW6POf0WsP0bi0B_aujTP8ZYra93PYTm3SgpOq4ln8_SDOhwNag36M0L_p6O2Ndxu9Ds9aNJRKLjKAHgAmTUZHNBgNjHvhaTNPRhqmc01Vz0W_HovG8HfCNOrBJYN9Dx7DlDRVjVBKUsHyU3LEx5BSxO7UGiV6dpbeO0vPztJ7Z2XJl9dfOgn--4j_AzcZzaI</recordid><startdate>20171127</startdate><enddate>20171127</enddate><creator>Kreft, Jan-Ulrich</creator><creator>Plugge, Caroline M</creator><creator>Prats, Clara</creator><creator>Leveau, Johan H J</creator><creator>Zhang, Weiwen</creator><creator>Hellweger, Ferdi L</creator><general>Frontiers Media S.A</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>XX2</scope><scope>5PM</scope><scope>QVL</scope><scope>DOA</scope></search><sort><creationdate>20171127</creationdate><title>From Genes to Ecosystems in Microbiology: Modeling Approaches and the Importance of Individuality</title><author>Kreft, Jan-Ulrich ; Plugge, Caroline M ; Prats, Clara ; Leveau, Johan H J ; Zhang, Weiwen ; Hellweger, Ferdi L</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c555t-ac89d19418ec367cfb97d7e587b0dd5a189af099abe6b4da3624acf5e09d7a393</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Agent-based modeling</topic><topic>Ciències de la terra i de la vida</topic><topic>Enginyeria agroalimentària</topic><topic>Gene-centric modeling</topic><topic>Genètica microbiana</topic><topic>Heterogeneity</topic><topic>Individuality</topic><topic>Metabolic flux modeling</topic><topic>Microbial ecology</topic><topic>Microbial genetics</topic><topic>Microbiologia</topic><topic>Microbiology</topic><topic>Single cell</topic><topic>Àrees temàtiques de la UPC</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kreft, Jan-Ulrich</creatorcontrib><creatorcontrib>Plugge, Caroline M</creatorcontrib><creatorcontrib>Prats, Clara</creatorcontrib><creatorcontrib>Leveau, Johan H J</creatorcontrib><creatorcontrib>Zhang, Weiwen</creatorcontrib><creatorcontrib>Hellweger, Ferdi L</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Recercat</collection><collection>PubMed Central (Full Participant titles)</collection><collection>NARCIS:Publications</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>Frontiers in microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kreft, Jan-Ulrich</au><au>Plugge, Caroline M</au><au>Prats, Clara</au><au>Leveau, Johan H J</au><au>Zhang, Weiwen</au><au>Hellweger, Ferdi L</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>From Genes to Ecosystems in Microbiology: Modeling Approaches and the Importance of Individuality</atitle><jtitle>Frontiers in microbiology</jtitle><addtitle>Front Microbiol</addtitle><date>2017-11-27</date><risdate>2017</risdate><volume>8</volume><spage>2299</spage><epage>2299</epage><pages>2299-2299</pages><issn>1664-302X</issn><eissn>1664-302X</eissn><abstract>Models are important tools in microbial ecology. They can be used to advance understanding by helping to interpret observations and test hypotheses, and to predict the effects of ecosystem management actions or a different climate. Over the past decades, biological knowledge and ecosystem observations have advanced to the molecular and in particular gene level. However, microbial ecology models have changed less and a current challenge is to make them utilize the knowledge and observations at the genetic level. We review published models that explicitly consider genes and make predictions at the population or ecosystem level. The models can be grouped into three general approaches, i.e., metabolic flux, gene-centric and agent-based. We describe and contrast these approaches by applying them to a hypothetical ecosystem and discuss their strengths and weaknesses. An important distinguishing feature is how variation between individual cells (individuality) is handled. In microbial ecosystems, individual heterogeneity is generated by a number of mechanisms including stochastic interactions of molecules (e.g., gene expression), stochastic and deterministic cell division asymmetry, small-scale environmental heterogeneity, and differential transport in a heterogeneous environment. This heterogeneity can then be amplified and transferred to other cell properties by several mechanisms, including nutrient uptake, metabolism and growth, cell cycle asynchronicity and the effects of age and damage. For example, stochastic gene expression may lead to heterogeneity in nutrient uptake enzyme levels, which in turn results in heterogeneity in intracellular nutrient levels. Individuality can have important ecological consequences, including division of labor, bet hedging, aging and sub-optimality. Understanding the importance of individuality and the mechanism(s) underlying it for the specific microbial system and question investigated is essential for selecting the optimal modeling strategy.</abstract><cop>Switzerland</cop><pub>Frontiers Media S.A</pub><pmid>29230200</pmid><doi>10.3389/fmicb.2017.02299</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 1664-302X
ispartof Frontiers in microbiology, 2017-11, Vol.8, p.2299-2299
issn 1664-302X
1664-302X
language eng
recordid cdi_doaj_primary_oai_doaj_org_article_c85f8318f8af45a8ae96935ae0210926
source PubMed Central
subjects Agent-based modeling
Ciències de la terra i de la vida
Enginyeria agroalimentària
Gene-centric modeling
Genètica microbiana
Heterogeneity
Individuality
Metabolic flux modeling
Microbial ecology
Microbial genetics
Microbiologia
Microbiology
Single cell
Àrees temàtiques de la UPC
title From Genes to Ecosystems in Microbiology: Modeling Approaches and the Importance of Individuality
url http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-24T10%3A19%3A03IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_doaj_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=From%20Genes%20to%20Ecosystems%20in%20Microbiology:%20Modeling%20Approaches%20and%20the%20Importance%20of%20Individuality&rft.jtitle=Frontiers%20in%20microbiology&rft.au=Kreft,%20Jan-Ulrich&rft.date=2017-11-27&rft.volume=8&rft.spage=2299&rft.epage=2299&rft.pages=2299-2299&rft.issn=1664-302X&rft.eissn=1664-302X&rft_id=info:doi/10.3389/fmicb.2017.02299&rft_dat=%3Cproquest_doaj_%3E1975998152%3C/proquest_doaj_%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c555t-ac89d19418ec367cfb97d7e587b0dd5a189af099abe6b4da3624acf5e09d7a393%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=1975998152&rft_id=info:pmid/29230200&rfr_iscdi=true