Spatial dynamics of synthetic microbial mutualists and their parasites

A major force contributing to the emergence of novelty in nature is the presence of cooperative interactions, where two or more components of a system act in synergy, sometimes leading to higher-order, emergent phenomena. Within molecular evolution, the so called hypercycle defines the simplest mode...

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Autores: Amor, Daniel R., Montañez, Raúl, Duran Nebreda, Salvador, 1987-, Solé Vicente, Ricard, 1962-
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2017
País:España
Institución:Universitat Pompeu Fabra
Repositorio:Repositorio Digital de la UPF
OAI Identifier:oai:repositori.upf.edu:10230/33733
Acceso en línea:http://hdl.handle.net/10230/33733
http://dx.doi.org/10.1371/journal.pcbi.1005689
Access Level:acceso abierto
Palabra clave:Microbial ecology
Microbial evolution
Parasite evolution
Soil ecology
Gut metagenome
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spelling Spatial dynamics of synthetic microbial mutualists and their parasitesAmor, Daniel R.Montañez, RaúlDuran Nebreda, Salvador, 1987-Solé Vicente, Ricard, 1962-Microbial ecologyMicrobial evolutionParasite evolutionSoil ecologyGut metagenomeA major force contributing to the emergence of novelty in nature is the presence of cooperative interactions, where two or more components of a system act in synergy, sometimes leading to higher-order, emergent phenomena. Within molecular evolution, the so called hypercycle defines the simplest model of an autocatalytic cycle, providing major theoretical insights on the evolution of cooperation in the early biosphere. These closed cooperative loops have also inspired our understanding of how catalytic loops appear in ecological systems. In both cases, hypercycle and ecological cooperative loops, the role played by space seems to be crucial for their stability and resilience against parasites. However, it is difficult to test these ideas in natural ecosystems, where time and spatial scales introduce considerable limitations. Here, we use engineered bacteria as a model system to a variety of environmental scenarios identifying trends that transcend the specific model system, such an enhanced genetic diversity in environments requiring mutualistic interactions. Interestingly, we show that improved environments can slow down mutualistic range expansions as a result of genetic drift effects preceding local resource depletion. Moreover, we show that a parasitic strain is excluded from the population during range expansions (which acknowledges a classical prediction). Nevertheless, environmental deterioration can reshape population interactions, this same strain becoming part of a three-species mutualistic web in scenarios in which the two-strain mutualism becomes non functional. The evolutionary and ecological implications for the design of synthetic ecosystems are outlined.This study was supported by an European Research Council Advanced Grant (SYNCOM, grant number 294294), a MINECO grant FIS2015-67616-P, by Banco Santander through its Santander Universities Global Division, the Secretaria d'Universitats i Recerca del Departament d'Economia i Coneixement de la Generalitat de Catalunya and by the Santa Fe Institute.Public Library of Science (PLoS)201820182017info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/33733http://dx.doi.org/10.1371/journal.pcbi.1005689reponame:Repositorio Digital de la UPFinstname:Universitat Pompeu FabraInglésPLOS Computational Biology. 2017 Aug 21;13(8):e1005689info:eu-repo/grantAgreement/EC/FP7/294294info:eu-repo/grantAgreement/ES/1PE/FIS2015-67616-P© 2017 Amor 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/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.http://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:repositori.upf.edu:10230/337332026-06-12T07:21:37Z
dc.title.none.fl_str_mv Spatial dynamics of synthetic microbial mutualists and their parasites
title Spatial dynamics of synthetic microbial mutualists and their parasites
spellingShingle Spatial dynamics of synthetic microbial mutualists and their parasites
Amor, Daniel R.
Microbial ecology
Microbial evolution
Parasite evolution
Soil ecology
Gut metagenome
title_short Spatial dynamics of synthetic microbial mutualists and their parasites
title_full Spatial dynamics of synthetic microbial mutualists and their parasites
title_fullStr Spatial dynamics of synthetic microbial mutualists and their parasites
title_full_unstemmed Spatial dynamics of synthetic microbial mutualists and their parasites
title_sort Spatial dynamics of synthetic microbial mutualists and their parasites
dc.creator.none.fl_str_mv Amor, Daniel R.
Montañez, Raúl
Duran Nebreda, Salvador, 1987-
Solé Vicente, Ricard, 1962-
author Amor, Daniel R.
author_facet Amor, Daniel R.
Montañez, Raúl
Duran Nebreda, Salvador, 1987-
Solé Vicente, Ricard, 1962-
author_role author
author2 Montañez, Raúl
Duran Nebreda, Salvador, 1987-
Solé Vicente, Ricard, 1962-
author2_role author
author
author
dc.subject.none.fl_str_mv Microbial ecology
Microbial evolution
Parasite evolution
Soil ecology
Gut metagenome
topic Microbial ecology
Microbial evolution
Parasite evolution
Soil ecology
Gut metagenome
description A major force contributing to the emergence of novelty in nature is the presence of cooperative interactions, where two or more components of a system act in synergy, sometimes leading to higher-order, emergent phenomena. Within molecular evolution, the so called hypercycle defines the simplest model of an autocatalytic cycle, providing major theoretical insights on the evolution of cooperation in the early biosphere. These closed cooperative loops have also inspired our understanding of how catalytic loops appear in ecological systems. In both cases, hypercycle and ecological cooperative loops, the role played by space seems to be crucial for their stability and resilience against parasites. However, it is difficult to test these ideas in natural ecosystems, where time and spatial scales introduce considerable limitations. Here, we use engineered bacteria as a model system to a variety of environmental scenarios identifying trends that transcend the specific model system, such an enhanced genetic diversity in environments requiring mutualistic interactions. Interestingly, we show that improved environments can slow down mutualistic range expansions as a result of genetic drift effects preceding local resource depletion. Moreover, we show that a parasitic strain is excluded from the population during range expansions (which acknowledges a classical prediction). Nevertheless, environmental deterioration can reshape population interactions, this same strain becoming part of a three-species mutualistic web in scenarios in which the two-strain mutualism becomes non functional. The evolutionary and ecological implications for the design of synthetic ecosystems are outlined.
publishDate 2017
dc.date.none.fl_str_mv 2017
2018
2018
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10230/33733
http://dx.doi.org/10.1371/journal.pcbi.1005689
url http://hdl.handle.net/10230/33733
http://dx.doi.org/10.1371/journal.pcbi.1005689
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv PLOS Computational Biology. 2017 Aug 21;13(8):e1005689
info:eu-repo/grantAgreement/EC/FP7/294294
info:eu-repo/grantAgreement/ES/1PE/FIS2015-67616-P
dc.rights.none.fl_str_mv http://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Public Library of Science (PLoS)
publisher.none.fl_str_mv Public Library of Science (PLoS)
dc.source.none.fl_str_mv reponame:Repositorio Digital de la UPF
instname:Universitat Pompeu Fabra
instname_str Universitat Pompeu Fabra
reponame_str Repositorio Digital de la UPF
collection Repositorio Digital de la UPF
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