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

Abstract

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 (NH 4 + ), 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 NH 4 + in each species. The model predicted that interpartner competition for NH 4 + could profoundly impact population dynamics. We then experimentally tested the predictions by culturing mutants lacking NH 4 + transporters in both NH 4 + competition assaysmore » and mutualistic cocultures. Both theoretical and experimental results indicated that the recipient must have a competitive advantage in acquiring cross-fed NH 4 + 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.« less

Authors:
 [1];  [1];  [1];  [1];  [2]
  1. Univ. of Indiana, Bloomington, IN (United States)
  2. Univ. of Rhode Island, Kingston, RI (United States)
Publication Date:
Research Org.:
Univ. of Indiana, Bloomington, IN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1437774
Alternate Identifier(s):
OSTI ID: 1510521
Grant/Contract Number:  
SC0008131
Resource Type:
Journal Article: Published Article
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Volume: 8; Journal Issue: 6; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; cross-feeding; coculture; fermentation; hydrogen; microbial communities; mutualism; nitrogen fixation; purple bacteria; synthetic ecology

Citation Formats

McCully, Alexandra L., LaSarre, Breah, McKinlay, James B., Whiteley, Marvin, and Ramsey, Matthew Mark. Recipient-Biased Competition for an Intracellularly Generated Cross-Fed Nutrient Is Required for Coexistence of Microbial Mutualists. United States: N. p., 2017. Web. doi:10.1128/mbio.01620-17.
McCully, Alexandra L., LaSarre, Breah, McKinlay, James B., Whiteley, Marvin, & Ramsey, Matthew Mark. Recipient-Biased Competition for an Intracellularly Generated Cross-Fed Nutrient Is Required for Coexistence of Microbial Mutualists. United States. doi:10.1128/mbio.01620-17.
McCully, Alexandra L., LaSarre, Breah, McKinlay, James B., Whiteley, Marvin, and Ramsey, Matthew Mark. Tue . "Recipient-Biased Competition for an Intracellularly Generated Cross-Fed Nutrient Is Required for Coexistence of Microbial Mutualists". United States. doi:10.1128/mbio.01620-17.
@article{osti_1437774,
title = {Recipient-Biased Competition for an Intracellularly Generated Cross-Fed Nutrient Is Required for Coexistence of Microbial Mutualists},
author = {McCully, Alexandra L. and LaSarre, Breah and McKinlay, James B. and Whiteley, Marvin and Ramsey, Matthew Mark},
abstractNote = {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 (NH 4 + ), 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 NH 4 + in each species. The model predicted that interpartner competition for NH 4 + could profoundly impact population dynamics. We then experimentally tested the predictions by culturing mutants lacking NH 4 + transporters in both NH 4 + competition assays and mutualistic cocultures. Both theoretical and experimental results indicated that the recipient must have a competitive advantage in acquiring cross-fed NH 4 + 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.},
doi = {10.1128/mbio.01620-17},
journal = {mBio (Online)},
issn = {2150-7511},
number = 6,
volume = 8,
place = {United States},
year = {2017},
month = {11}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at 10.1128/mbio.01620-17

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Cited by: 3 works
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Works referenced in this record:

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