Adaptation of metabolite leakiness leads to symbiotic chemical exchange and to a resilient microbial ecosystem.

Microbial communities display remarkable diversity, facilitated by the secretion of chemicals that can create new niches. However, it is unclear why cells often secrete even essential metabolites after evolution. Based on theoretical results indicating that cells can enhance their own growth rate by...

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Autores principales:	Jumpei F Yamagishi, Nen Saito, Kunihiko Kaneko
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2021
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/a4714773773844a88cfbd6fbbfbc709e
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spelling	oai:doaj.org-article:a4714773773844a88cfbd6fbbfbc709e2021-11-25T05:40:35ZAdaptation of metabolite leakiness leads to symbiotic chemical exchange and to a resilient microbial ecosystem.1553-734X1553-735810.1371/journal.pcbi.1009143https://doaj.org/article/a4714773773844a88cfbd6fbbfbc709e2021-06-01T00:00:00Zhttps://doi.org/10.1371/journal.pcbi.1009143https://doaj.org/toc/1553-734Xhttps://doaj.org/toc/1553-7358Microbial communities display remarkable diversity, facilitated by the secretion of chemicals that can create new niches. However, it is unclear why cells often secrete even essential metabolites after evolution. Based on theoretical results indicating that cells can enhance their own growth rate by leaking even essential metabolites, we show that such "leaker" cells can establish an asymmetric form of mutualism with "consumer" cells that consume the leaked chemicals: the consumer cells benefit from the uptake of the secreted metabolites, while the leaker cells also benefit from such consumption, as it reduces the metabolite accumulation in the environment and thereby enables further secretion, resulting in frequency-dependent coexistence of multiple microbial species. As supported by extensive simulations, such symbiotic relationships generally evolve when each species has a complex reaction network and adapts its leakiness to optimize its own growth rate under crowded conditions and nutrient limitations. Accordingly, symbiotic ecosystems with diverse cell species that leak and exchange many metabolites with each other are shaped by cell-level adaptation of leakiness of metabolites. Moreover, the resultant ecosystems with entangled metabolite exchange are resilient against structural and environmental perturbations. Thus, we present a theory for the origin of resilient ecosystems with diverse microbes mediated by secretion and exchange of essential chemicals.Jumpei F YamagishiNen SaitoKunihiko KanekoPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Computational Biology, Vol 17, Iss 6, p e1009143 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Jumpei F Yamagishi Nen Saito Kunihiko Kaneko Adaptation of metabolite leakiness leads to symbiotic chemical exchange and to a resilient microbial ecosystem.
description	Microbial communities display remarkable diversity, facilitated by the secretion of chemicals that can create new niches. However, it is unclear why cells often secrete even essential metabolites after evolution. Based on theoretical results indicating that cells can enhance their own growth rate by leaking even essential metabolites, we show that such "leaker" cells can establish an asymmetric form of mutualism with "consumer" cells that consume the leaked chemicals: the consumer cells benefit from the uptake of the secreted metabolites, while the leaker cells also benefit from such consumption, as it reduces the metabolite accumulation in the environment and thereby enables further secretion, resulting in frequency-dependent coexistence of multiple microbial species. As supported by extensive simulations, such symbiotic relationships generally evolve when each species has a complex reaction network and adapts its leakiness to optimize its own growth rate under crowded conditions and nutrient limitations. Accordingly, symbiotic ecosystems with diverse cell species that leak and exchange many metabolites with each other are shaped by cell-level adaptation of leakiness of metabolites. Moreover, the resultant ecosystems with entangled metabolite exchange are resilient against structural and environmental perturbations. Thus, we present a theory for the origin of resilient ecosystems with diverse microbes mediated by secretion and exchange of essential chemicals.
format	article
author	Jumpei F Yamagishi Nen Saito Kunihiko Kaneko
author_facet	Jumpei F Yamagishi Nen Saito Kunihiko Kaneko
author_sort	Jumpei F Yamagishi
title	Adaptation of metabolite leakiness leads to symbiotic chemical exchange and to a resilient microbial ecosystem.
title_short	Adaptation of metabolite leakiness leads to symbiotic chemical exchange and to a resilient microbial ecosystem.
title_full	Adaptation of metabolite leakiness leads to symbiotic chemical exchange and to a resilient microbial ecosystem.
title_fullStr	Adaptation of metabolite leakiness leads to symbiotic chemical exchange and to a resilient microbial ecosystem.
title_full_unstemmed	Adaptation of metabolite leakiness leads to symbiotic chemical exchange and to a resilient microbial ecosystem.
title_sort	adaptation of metabolite leakiness leads to symbiotic chemical exchange and to a resilient microbial ecosystem.
publisher	Public Library of Science (PLoS)
publishDate	2021
url	https://doaj.org/article/a4714773773844a88cfbd6fbbfbc709e
work_keys_str_mv	AT jumpeifyamagishi adaptationofmetaboliteleakinessleadstosymbioticchemicalexchangeandtoaresilientmicrobialecosystem AT nensaito adaptationofmetaboliteleakinessleadstosymbioticchemicalexchangeandtoaresilientmicrobialecosystem AT kunihikokaneko adaptationofmetaboliteleakinessleadstosymbioticchemicalexchangeandtoaresilientmicrobialecosystem
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Adaptation of metabolite leakiness leads to symbiotic chemical exchange and to a resilient microbial ecosystem.

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