Recipient-Biased Competition for an Intracellularly Generated Cross-Fed Nutrient Is Required for Coexistence of Microbial Mutualists

ABSTRACT Many mutualistic microbial relationships are based on nutrient cross-feeding. Traditionally, cross-feeding is viewed as being unidirectional, from the producer to the recipient. This is likely true when a producer’s waste, such as a fermentation product, has value only for a recipient. Howe...

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Autores principales:	Alexandra L. McCully, Breah LaSarre, James B. McKinlay
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	cross-feeding coculture fermentation hydrogen microbial communities mutualism Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/b9c7583a02e0434799c115eeb974a210
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spelling	oai:doaj.org-article:b9c7583a02e0434799c115eeb974a2102021-11-15T15:51:56ZRecipient-Biased Competition for an Intracellularly Generated Cross-Fed Nutrient Is Required for Coexistence of Microbial Mutualists10.1128/mBio.01620-172150-7511https://doaj.org/article/b9c7583a02e0434799c115eeb974a2102017-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01620-17https://doaj.org/toc/2150-7511ABSTRACT Many mutualistic microbial relationships are based on nutrient cross-feeding. Traditionally, cross-feeding is viewed as being unidirectional, from the producer to the recipient. This is likely true when a producer’s waste, such as a fermentation product, has value only for a recipient. However, in some cases the cross-fed nutrient holds value for both the producer and the recipient. In such cases, there is potential for nutrient reacquisition by producer cells in a population, leading to competition against recipients. Here, we investigated the consequences of interpartner competition for cross-fed nutrients on mutualism dynamics by using an anaerobic coculture pairing fermentative Escherichia coli and phototrophic Rhodopseudomonas palustris. In this coculture, E. coli excretes waste organic acids that provide a carbon source for R. palustris. In return, R. palustris cross-feeds E. coli ammonium (NH4+), a compound that both species value. To explore the potential for interpartner competition, we first used a kinetic model to simulate cocultures with varied affinities for NH4+ in each species. The model predicted that interpartner competition for NH4+ could profoundly impact population dynamics. We then experimentally tested the predictions by culturing mutants lacking NH4+ transporters in both NH4+ competition assays and mutualistic cocultures. Both theoretical and experimental results indicated that the recipient must have a competitive advantage in acquiring cross-fed NH4+ to sustain the mutualism. This recipient-biased competitive advantage is predicted to be crucial, particularly when the communally valuable nutrient is generated intracellularly. Thus, the very metabolites that form the basis for mutualistic cross-feeding can also be subject to competition between mutualistic partners. IMPORTANCE Mutualistic relationships, particularly those based on nutrient cross-feeding, promote stability of diverse ecosystems and drive global biogeochemical cycles. Cross-fed nutrients within these systems can be either waste products valued by only one partner or nutrients valued by both partners. Here, we explored how interpartner competition for a communally valuable cross-fed nutrient impacts mutualism dynamics. We discovered that mutualism stability necessitates that the recipient have a competitive advantage against the producer in obtaining the cross-fed nutrient, provided that the nutrient is generated intracellularly. We propose that the requirement for recipient-biased competition is a general rule for mutualistic coexistence based on the transfer of intracellularly generated, communally valuable resources.Alexandra L. McCullyBreah LaSarreJames B. McKinlayAmerican Society for Microbiologyarticlecross-feedingcoculturefermentationhydrogenmicrobial communitiesmutualismMicrobiologyQR1-502ENmBio, Vol 8, Iss 6 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	cross-feeding coculture fermentation hydrogen microbial communities mutualism Microbiology QR1-502
spellingShingle	cross-feeding coculture fermentation hydrogen microbial communities mutualism Microbiology QR1-502 Alexandra L. McCully Breah LaSarre James B. McKinlay Recipient-Biased Competition for an Intracellularly Generated Cross-Fed Nutrient Is Required for Coexistence of Microbial Mutualists
description	ABSTRACT Many mutualistic microbial relationships are based on nutrient cross-feeding. Traditionally, cross-feeding is viewed as being unidirectional, from the producer to the recipient. This is likely true when a producer’s waste, such as a fermentation product, has value only for a recipient. However, in some cases the cross-fed nutrient holds value for both the producer and the recipient. In such cases, there is potential for nutrient reacquisition by producer cells in a population, leading to competition against recipients. Here, we investigated the consequences of interpartner competition for cross-fed nutrients on mutualism dynamics by using an anaerobic coculture pairing fermentative Escherichia coli and phototrophic Rhodopseudomonas palustris. In this coculture, E. coli excretes waste organic acids that provide a carbon source for R. palustris. In return, R. palustris cross-feeds E. coli ammonium (NH4+), a compound that both species value. To explore the potential for interpartner competition, we first used a kinetic model to simulate cocultures with varied affinities for NH4+ in each species. The model predicted that interpartner competition for NH4+ could profoundly impact population dynamics. We then experimentally tested the predictions by culturing mutants lacking NH4+ transporters in both NH4+ competition assays and mutualistic cocultures. Both theoretical and experimental results indicated that the recipient must have a competitive advantage in acquiring cross-fed NH4+ to sustain the mutualism. This recipient-biased competitive advantage is predicted to be crucial, particularly when the communally valuable nutrient is generated intracellularly. Thus, the very metabolites that form the basis for mutualistic cross-feeding can also be subject to competition between mutualistic partners. IMPORTANCE Mutualistic relationships, particularly those based on nutrient cross-feeding, promote stability of diverse ecosystems and drive global biogeochemical cycles. Cross-fed nutrients within these systems can be either waste products valued by only one partner or nutrients valued by both partners. Here, we explored how interpartner competition for a communally valuable cross-fed nutrient impacts mutualism dynamics. We discovered that mutualism stability necessitates that the recipient have a competitive advantage against the producer in obtaining the cross-fed nutrient, provided that the nutrient is generated intracellularly. We propose that the requirement for recipient-biased competition is a general rule for mutualistic coexistence based on the transfer of intracellularly generated, communally valuable resources.
format	article
author	Alexandra L. McCully Breah LaSarre James B. McKinlay
author_facet	Alexandra L. McCully Breah LaSarre James B. McKinlay
author_sort	Alexandra L. McCully
title	Recipient-Biased Competition for an Intracellularly Generated Cross-Fed Nutrient Is Required for Coexistence of Microbial Mutualists
title_short	Recipient-Biased Competition for an Intracellularly Generated Cross-Fed Nutrient Is Required for Coexistence of Microbial Mutualists
title_full	Recipient-Biased Competition for an Intracellularly Generated Cross-Fed Nutrient Is Required for Coexistence of Microbial Mutualists
title_fullStr	Recipient-Biased Competition for an Intracellularly Generated Cross-Fed Nutrient Is Required for Coexistence of Microbial Mutualists
title_full_unstemmed	Recipient-Biased Competition for an Intracellularly Generated Cross-Fed Nutrient Is Required for Coexistence of Microbial Mutualists
title_sort	recipient-biased competition for an intracellularly generated cross-fed nutrient is required for coexistence of microbial mutualists
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/b9c7583a02e0434799c115eeb974a210
work_keys_str_mv	AT alexandralmccully recipientbiasedcompetitionforanintracellularlygeneratedcrossfednutrientisrequiredforcoexistenceofmicrobialmutualists AT breahlasarre recipientbiasedcompetitionforanintracellularlygeneratedcrossfednutrientisrequiredforcoexistenceofmicrobialmutualists AT jamesbmckinlay recipientbiasedcompetitionforanintracellularlygeneratedcrossfednutrientisrequiredforcoexistenceofmicrobialmutualists
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Recipient-Biased Competition for an Intracellularly Generated Cross-Fed Nutrient Is Required for Coexistence of Microbial Mutualists

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