High-order interactions distort the functional landscape of microbial consortia

Understanding the link between community composition and function is a major challenge in microbial population biology, with implications for the management of natural microbiomes and the design of synthetic consortia. Specifically, it is poorly understood whether community functions can be quantita...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:PLoS biology 2019-12, Vol.17 (12), p.e3000550-e3000550
Hauptverfasser: Sanchez-Gorostiaga, Alicia, Bajić, Djordje, Osborne, Melisa L, Poyatos, Juan F, Sanchez, Alvaro
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page e3000550
container_issue 12
container_start_page e3000550
container_title PLoS biology
container_volume 17
creator Sanchez-Gorostiaga, Alicia
Bajić, Djordje
Osborne, Melisa L
Poyatos, Juan F
Sanchez, Alvaro
description Understanding the link between community composition and function is a major challenge in microbial population biology, with implications for the management of natural microbiomes and the design of synthetic consortia. Specifically, it is poorly understood whether community functions can be quantitatively predicted from traits of species in monoculture. Inspired by the study of complex genetic interactions, we have examined how the amylolytic rate of combinatorial assemblages of six starch-degrading soil bacteria depend on the separate functional contributions from each species and their interactions. Filtering our results through the theory of biochemical kinetics, we show that this simple function is additive in the absence of interactions among community members. For about half of the combinatorially assembled consortia, the amylolytic function is dominated by pairwise and higher-order interactions. For the other half, the function is additive despite the presence of strong competitive interactions. We explain the mechanistic basis of these findings and propose a quantitative framework that allows us to separate the effect of behavioral and population dynamics interactions. Our results suggest that the functional robustness of a consortium to pairwise and higher-order interactions critically affects our ability to predict and bottom-up engineer ecosystem function in complex communities.
doi_str_mv 10.1371/journal.pbio.3000550
format Article
fullrecord <record><control><sourceid>proquest_plos_</sourceid><recordid>TN_cdi_plos_journals_2339845704</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><doaj_id>oai_doaj_org_article_04bacd10c4f04f0daafa671cf25c4645</doaj_id><sourcerecordid>2339845704</sourcerecordid><originalsourceid>FETCH-LOGICAL-c592t-6fe377b1be8a710a331eb84db56026786545729782cda1ac90432cc295ac07713</originalsourceid><addsrcrecordid>eNptUk1r3DAUFCWlSbf9B6Ux5JKLt_qwLPkSKCFpAoFc2rN4fpJ3tXitjWQX-u-r3XVCUgoCiaeZ0bynIeQLo0smFPu2CVMcoF_uWh-WglIqJX1HzpisZKm0lievzqfkY0obSjlvuP5ATgXTmcH1GXm886t1GaJ1sfDD6CLg6MOQCuvTGOJYjGtXdNNwqEJf9DDYhLBzReiKrccYWp_LmCkZ7eETed9Bn9zneV-QX7c3P6_vyofHH_fX3x9KlA0fy7pzQqmWtU6DYhSEYK7VlW1lTXmtdJ2dK94ozdECA2xoJTgibyQgVYqJBTk_6u76kMw8i2S4EI3O1AxfkPsjwgbYmF30W4h_TABvDoUQVwayY-ydoVULaBnFqqN5WYAOasWw4xKrupJZ62p-bWq3zqIbxgj9G9G3N4Nfm1X4bepGcM15FricBWJ4mlwazdYndH0epwvTwTfjstFyD734B_r_7qojKv9AStF1L2YYNft8PLPMPh9mzkemfX3dyAvpORDiL3TFuWc</addsrcrecordid><sourcetype>Open Website</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2339845704</pqid></control><display><type>article</type><title>High-order interactions distort the functional landscape of microbial consortia</title><source>MEDLINE</source><source>DOAJ Directory of Open Access Journals</source><source>Public Library of Science (PLoS) Journals Open Access</source><source>EZB-FREE-00999 freely available EZB journals</source><source>PubMed Central</source><creator>Sanchez-Gorostiaga, Alicia ; Bajić, Djordje ; Osborne, Melisa L ; Poyatos, Juan F ; Sanchez, Alvaro</creator><contributor>Shou, Wenying</contributor><creatorcontrib>Sanchez-Gorostiaga, Alicia ; Bajić, Djordje ; Osborne, Melisa L ; Poyatos, Juan F ; Sanchez, Alvaro ; Shou, Wenying</creatorcontrib><description>Understanding the link between community composition and function is a major challenge in microbial population biology, with implications for the management of natural microbiomes and the design of synthetic consortia. Specifically, it is poorly understood whether community functions can be quantitatively predicted from traits of species in monoculture. Inspired by the study of complex genetic interactions, we have examined how the amylolytic rate of combinatorial assemblages of six starch-degrading soil bacteria depend on the separate functional contributions from each species and their interactions. Filtering our results through the theory of biochemical kinetics, we show that this simple function is additive in the absence of interactions among community members. For about half of the combinatorially assembled consortia, the amylolytic function is dominated by pairwise and higher-order interactions. For the other half, the function is additive despite the presence of strong competitive interactions. We explain the mechanistic basis of these findings and propose a quantitative framework that allows us to separate the effect of behavioral and population dynamics interactions. Our results suggest that the functional robustness of a consortium to pairwise and higher-order interactions critically affects our ability to predict and bottom-up engineer ecosystem function in complex communities.</description><identifier>ISSN: 1545-7885</identifier><identifier>ISSN: 1544-9173</identifier><identifier>EISSN: 1545-7885</identifier><identifier>DOI: 10.1371/journal.pbio.3000550</identifier><identifier>PMID: 31830028</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Bacteria ; Bacteria - genetics ; Biology and Life Sciences ; Biotechnology ; Combinatorial analysis ; Community composition ; Consortia ; Ecology ; Enzymes ; Evolutionary biology ; Medicine and Health Sciences ; Microbial Consortia - physiology ; Microbial Interactions - physiology ; Microbiomes ; Microbiota - genetics ; Microbiota - physiology ; Microorganisms ; Monoculture ; Mutation ; Physical Sciences ; Population biology ; Population dynamics ; Research and Analysis Methods ; Social Sciences ; Soil - chemistry ; Soil bacteria ; Soil degradation ; Soil Microbiology ; Soil microorganisms ; Starch</subject><ispartof>PLoS biology, 2019-12, Vol.17 (12), p.e3000550-e3000550</ispartof><rights>2019 Sanchez-Gorostiaga et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2019 Sanchez-Gorostiaga et al 2019 Sanchez-Gorostiaga et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c592t-6fe377b1be8a710a331eb84db56026786545729782cda1ac90432cc295ac07713</citedby><cites>FETCH-LOGICAL-c592t-6fe377b1be8a710a331eb84db56026786545729782cda1ac90432cc295ac07713</cites><orcidid>0000-0002-2719-5659 ; 0000-0002-2292-5608 ; 0000-0002-6716-7898 ; 0000-0002-3945-7134</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/PMC6932822/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6932822/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31830028$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Shou, Wenying</contributor><creatorcontrib>Sanchez-Gorostiaga, Alicia</creatorcontrib><creatorcontrib>Bajić, Djordje</creatorcontrib><creatorcontrib>Osborne, Melisa L</creatorcontrib><creatorcontrib>Poyatos, Juan F</creatorcontrib><creatorcontrib>Sanchez, Alvaro</creatorcontrib><title>High-order interactions distort the functional landscape of microbial consortia</title><title>PLoS biology</title><addtitle>PLoS Biol</addtitle><description>Understanding the link between community composition and function is a major challenge in microbial population biology, with implications for the management of natural microbiomes and the design of synthetic consortia. Specifically, it is poorly understood whether community functions can be quantitatively predicted from traits of species in monoculture. Inspired by the study of complex genetic interactions, we have examined how the amylolytic rate of combinatorial assemblages of six starch-degrading soil bacteria depend on the separate functional contributions from each species and their interactions. Filtering our results through the theory of biochemical kinetics, we show that this simple function is additive in the absence of interactions among community members. For about half of the combinatorially assembled consortia, the amylolytic function is dominated by pairwise and higher-order interactions. For the other half, the function is additive despite the presence of strong competitive interactions. We explain the mechanistic basis of these findings and propose a quantitative framework that allows us to separate the effect of behavioral and population dynamics interactions. Our results suggest that the functional robustness of a consortium to pairwise and higher-order interactions critically affects our ability to predict and bottom-up engineer ecosystem function in complex communities.</description><subject>Bacteria</subject><subject>Bacteria - genetics</subject><subject>Biology and Life Sciences</subject><subject>Biotechnology</subject><subject>Combinatorial analysis</subject><subject>Community composition</subject><subject>Consortia</subject><subject>Ecology</subject><subject>Enzymes</subject><subject>Evolutionary biology</subject><subject>Medicine and Health Sciences</subject><subject>Microbial Consortia - physiology</subject><subject>Microbial Interactions - physiology</subject><subject>Microbiomes</subject><subject>Microbiota - genetics</subject><subject>Microbiota - physiology</subject><subject>Microorganisms</subject><subject>Monoculture</subject><subject>Mutation</subject><subject>Physical Sciences</subject><subject>Population biology</subject><subject>Population dynamics</subject><subject>Research and Analysis Methods</subject><subject>Social Sciences</subject><subject>Soil - chemistry</subject><subject>Soil bacteria</subject><subject>Soil degradation</subject><subject>Soil Microbiology</subject><subject>Soil microorganisms</subject><subject>Starch</subject><issn>1545-7885</issn><issn>1544-9173</issn><issn>1545-7885</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNptUk1r3DAUFCWlSbf9B6Ux5JKLt_qwLPkSKCFpAoFc2rN4fpJ3tXitjWQX-u-r3XVCUgoCiaeZ0bynIeQLo0smFPu2CVMcoF_uWh-WglIqJX1HzpisZKm0lievzqfkY0obSjlvuP5ATgXTmcH1GXm886t1GaJ1sfDD6CLg6MOQCuvTGOJYjGtXdNNwqEJf9DDYhLBzReiKrccYWp_LmCkZ7eETed9Bn9zneV-QX7c3P6_vyofHH_fX3x9KlA0fy7pzQqmWtU6DYhSEYK7VlW1lTXmtdJ2dK94ozdECA2xoJTgibyQgVYqJBTk_6u76kMw8i2S4EI3O1AxfkPsjwgbYmF30W4h_TABvDoUQVwayY-ydoVULaBnFqqN5WYAOasWw4xKrupJZ62p-bWq3zqIbxgj9G9G3N4Nfm1X4bepGcM15FricBWJ4mlwazdYndH0epwvTwTfjstFyD734B_r_7qojKv9AStF1L2YYNft8PLPMPh9mzkemfX3dyAvpORDiL3TFuWc</recordid><startdate>20191201</startdate><enddate>20191201</enddate><creator>Sanchez-Gorostiaga, Alicia</creator><creator>Bajić, Djordje</creator><creator>Osborne, Melisa L</creator><creator>Poyatos, Juan F</creator><creator>Sanchez, Alvaro</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>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PATMY</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><scope>CZG</scope><orcidid>https://orcid.org/0000-0002-2719-5659</orcidid><orcidid>https://orcid.org/0000-0002-2292-5608</orcidid><orcidid>https://orcid.org/0000-0002-6716-7898</orcidid><orcidid>https://orcid.org/0000-0002-3945-7134</orcidid></search><sort><creationdate>20191201</creationdate><title>High-order interactions distort the functional landscape of microbial consortia</title><author>Sanchez-Gorostiaga, Alicia ; Bajić, Djordje ; Osborne, Melisa L ; Poyatos, Juan F ; Sanchez, Alvaro</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c592t-6fe377b1be8a710a331eb84db56026786545729782cda1ac90432cc295ac07713</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Bacteria</topic><topic>Bacteria - genetics</topic><topic>Biology and Life Sciences</topic><topic>Biotechnology</topic><topic>Combinatorial analysis</topic><topic>Community composition</topic><topic>Consortia</topic><topic>Ecology</topic><topic>Enzymes</topic><topic>Evolutionary biology</topic><topic>Medicine and Health Sciences</topic><topic>Microbial Consortia - physiology</topic><topic>Microbial Interactions - physiology</topic><topic>Microbiomes</topic><topic>Microbiota - genetics</topic><topic>Microbiota - physiology</topic><topic>Microorganisms</topic><topic>Monoculture</topic><topic>Mutation</topic><topic>Physical Sciences</topic><topic>Population biology</topic><topic>Population dynamics</topic><topic>Research and Analysis Methods</topic><topic>Social Sciences</topic><topic>Soil - chemistry</topic><topic>Soil bacteria</topic><topic>Soil degradation</topic><topic>Soil Microbiology</topic><topic>Soil microorganisms</topic><topic>Starch</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sanchez-Gorostiaga, Alicia</creatorcontrib><creatorcontrib>Bajić, Djordje</creatorcontrib><creatorcontrib>Osborne, Melisa L</creatorcontrib><creatorcontrib>Poyatos, Juan F</creatorcontrib><creatorcontrib>Sanchez, Alvaro</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</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>Health &amp; Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>Agricultural &amp; Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Access via ProQuest (Open Access)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><collection>PLoS Biology</collection><jtitle>PLoS biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sanchez-Gorostiaga, Alicia</au><au>Bajić, Djordje</au><au>Osborne, Melisa L</au><au>Poyatos, Juan F</au><au>Sanchez, Alvaro</au><au>Shou, Wenying</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>High-order interactions distort the functional landscape of microbial consortia</atitle><jtitle>PLoS biology</jtitle><addtitle>PLoS Biol</addtitle><date>2019-12-01</date><risdate>2019</risdate><volume>17</volume><issue>12</issue><spage>e3000550</spage><epage>e3000550</epage><pages>e3000550-e3000550</pages><issn>1545-7885</issn><issn>1544-9173</issn><eissn>1545-7885</eissn><abstract>Understanding the link between community composition and function is a major challenge in microbial population biology, with implications for the management of natural microbiomes and the design of synthetic consortia. Specifically, it is poorly understood whether community functions can be quantitatively predicted from traits of species in monoculture. Inspired by the study of complex genetic interactions, we have examined how the amylolytic rate of combinatorial assemblages of six starch-degrading soil bacteria depend on the separate functional contributions from each species and their interactions. Filtering our results through the theory of biochemical kinetics, we show that this simple function is additive in the absence of interactions among community members. For about half of the combinatorially assembled consortia, the amylolytic function is dominated by pairwise and higher-order interactions. For the other half, the function is additive despite the presence of strong competitive interactions. We explain the mechanistic basis of these findings and propose a quantitative framework that allows us to separate the effect of behavioral and population dynamics interactions. Our results suggest that the functional robustness of a consortium to pairwise and higher-order interactions critically affects our ability to predict and bottom-up engineer ecosystem function in complex communities.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>31830028</pmid><doi>10.1371/journal.pbio.3000550</doi><orcidid>https://orcid.org/0000-0002-2719-5659</orcidid><orcidid>https://orcid.org/0000-0002-2292-5608</orcidid><orcidid>https://orcid.org/0000-0002-6716-7898</orcidid><orcidid>https://orcid.org/0000-0002-3945-7134</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 1545-7885
ispartof PLoS biology, 2019-12, Vol.17 (12), p.e3000550-e3000550
issn 1545-7885
1544-9173
1545-7885
language eng
recordid cdi_plos_journals_2339845704
source MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; PubMed Central
subjects Bacteria
Bacteria - genetics
Biology and Life Sciences
Biotechnology
Combinatorial analysis
Community composition
Consortia
Ecology
Enzymes
Evolutionary biology
Medicine and Health Sciences
Microbial Consortia - physiology
Microbial Interactions - physiology
Microbiomes
Microbiota - genetics
Microbiota - physiology
Microorganisms
Monoculture
Mutation
Physical Sciences
Population biology
Population dynamics
Research and Analysis Methods
Social Sciences
Soil - chemistry
Soil bacteria
Soil degradation
Soil Microbiology
Soil microorganisms
Starch
title High-order interactions distort the functional landscape of microbial consortia
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-26T23%3A52%3A56IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=High-order%20interactions%20distort%20the%20functional%20landscape%20of%20microbial%20consortia&rft.jtitle=PLoS%20biology&rft.au=Sanchez-Gorostiaga,%20Alicia&rft.date=2019-12-01&rft.volume=17&rft.issue=12&rft.spage=e3000550&rft.epage=e3000550&rft.pages=e3000550-e3000550&rft.issn=1545-7885&rft.eissn=1545-7885&rft_id=info:doi/10.1371/journal.pbio.3000550&rft_dat=%3Cproquest_plos_%3E2339845704%3C/proquest_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2339845704&rft_id=info:pmid/31830028&rft_doaj_id=oai_doaj_org_article_04bacd10c4f04f0daafa671cf25c4645&rfr_iscdi=true