Abstract
ABSTRACTMany 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.
Highlights
Many mutualistic microbial relationships are based on nutrient cross-feeding
We previously developed a bacterial coculture that features cross-feeding of waste products from Escherichia coli and a communally valuable nutrient (NH4ϩ) from Rhodopseudomonas palustris Nx (Fig. 1A) [28]
Within our coculture (Fig. 1A), E. coli ferments sugars into waste organic acids, providing essential carbon and electrons to R. palustris Nx
Summary
Many mutualistic microbial relationships are based on nutrient cross-feeding. Traditionally, cross-feeding is viewed as being unidirectional, from the producer to the recipient. While most mutualism cross-feeding studies only consider unidirectional metabolite transfer from producer to recipient, we hypothesized that partially privatized cross-fed resources could be subject to competition between partner populations. Such competition from partial privatization mechanisms seems likely, considering that competition for exogenous limiting resources is known to affect mutualism stability [9, 17,18,19,20]. At neutral pH, NH4ϩ is the predominant form, but small amounts of NH3 can potentially leave the cell by passive diffusion across the membrane; this passive diffusion is referred to here as NH4ϩ excretion [23] (Fig. 1B) This inherent “leakiness” for NH3 likely fosters NH4ϩ cross-feeding, as extracellular NH3 is available to neighboring microbes. During NH4ϩ cross-feeding, AmtB likely facilitates both NH4ϩ acquisition by a recipient partner and recapture of NH4ϩ by the N2 fixer
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