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

• Published in: mBio Vol. 8; no. 6
• Main Authors: McCully, Alexandra L, LaSarre, Breah, McKinlay, James B
• Format: Journal Article
• Language: English
• Published: United States American Society for Microbiology 28.11.2017
• Subjects: Ammonium Compounds - metabolism; Anaerobiosis; BASIC BIOLOGICAL SCIENCES; Carbon - metabolism; Carboxylic Acids - metabolism; coculture; Computer Simulation; cross-feeding; Escherichia coli - growth & development; Escherichia coli - metabolism; Fermentation; hydrogen; microbial communities; mutualism; nitrogen fixation; Population Dynamics; purple bacteria; Rhodopseudomonas - growth & development; Rhodopseudomonas - metabolism; Symbiosis; synthetic ecology; synthetic ecology; coculture; cross-feeding; purple bacteria; fermentation; hydrogen; microbial communities; nitrogen fixation; mutualism
• ISSN: 2161-2129; 2150-7511
• DOI: 10.1128/mBio.01620-17

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 and phototrophic In this coculture, excretes waste organic acids that provide a carbon source for In return, cross-feeds ammonium (NH ), 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 in each species. The model predicted that interpartner competition for NH could profoundly impact population dynamics. We then experimentally tested the predictions by culturing mutants lacking NH transporters in both NH competition assays and mutualistic cocultures. Both theoretical and experimental results indicated that the recipient must have a competitive advantage in acquiring cross-fed NH 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. 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.