RT Journal Article
SR Electronic
T1 Recipient-biased competition for a cross-fed nutrient is required for coexistence of microbial mutualists
JF bioRxiv
FD Cold Spring Harbor Laboratory
SP 144220
DO 10.1101/144220
A1 Alexandra L. McCully
A1 Breah LaSarre
A1 James B. McKinlay
YR 2017
UL http://biorxiv.org/content/early/2017/05/31/144220.abstract
AB Many mutualistic microbial relationships are based on the exchange of nutrients, or cross-feeding. Traditionally, cross-feeding interactions are viewed as being unidirectional from the producer to the recipient. This is likely true when a cross-fed nutrient is a waste-product of the producer’s metabolism. However, in some cases the nutrient holds value for both the producer and the recipient. In such cases, there is potential for reacquisition of a valuable cross-fed nutrient by producers in a population, essentially leading to competition against the recipients. The consequences of inter-partner competition for cross-fed nutrients on mutualism dynamics have not been considered. We investigated the effects of such competition on a mutualism using a synthetic anaerobic coculture pairing fermentative Escherichia coli and phototrophic Rhodopseudomonas palustris. In this coculture, E. coli excretes waste organic acids that serve as a carbon source for R. palustris. In return, R. palustris cross-feeds E. coli ammonium (NH4+), a valuable nitrogen source that both species in the mutualism prefer. To interrogate the impact of inter-partner competition, we varied the relative affinities for NH4+ in each species in coculture, both theoretically using kinetic model simulations and experimentally using mutants lacking NH4+ transporters. We demonstrated that the recipient partner must have a competitive advantage in acquiring a valuable cross-fed nutrient in order for the mutualism to persist. Our results reveal that interpartner competition shaping mutualism dynamics is not limited to environmental resources but rather can apply to the very metabolites that form the basis of the cooperative relationship.Significance Mutualistic relationships, particularly those based on nutrient cross-feeding, play crucial roles in the stability of diverse ecosystems and drive global biogeochemical cycles. Cross-fed nutrients within these systems can be either waste products valued only by one partner or nutrients that both partners value. Here, we explore how inter-partner competition for a valuable cross-fed nutrient impacts mutualism dynamics. We discovered that mutualism stability necessitates that the recipient must be competitive in obtaining the cross-fed nutrient. We propose that the requirement for recipient-biased competition is a general rule for mutualistic coexistence based on the transfer of mutually valuable resources, microbial or otherwise.