Resource Availability Modulates the Cooperative and Competitive Nature of a Microbial Cross-Feeding Mutualism

Abstract

Mutualisms between species play an important role in ecosystem function and stability. However, in some environments, the competitive aspects of an interaction may dominate the mutualistic aspects. Although these transitions could have far-reaching implications, it has been difficult to study the causes and consequences of this mutualistic–competitive transition in experimentally tractable systems. Here, we study a microbial cross-feeding mutualism in which each yeast strain supplies an essential amino acid for its partner strain. We find that, depending upon the amount of freely available amino acid in the environment, this pair of strains can exhibit an obligatory mutualism, facultative mutualism, competition, parasitism, competitive exclusion, or failed mutualism leading to extinction of the population. A simple model capturing the essential features of this interaction explains how resource availability modulates the interaction and predicts that changes in the dynamics of the mutualism in deteriorating environments can provide advance warning that collapse of the mutualism is imminent. We confirm this prediction experimentally by showing that, in the high nutrient competitive regime, the strains rapidly reach a common carrying capacity before slowly reaching the equilibrium ratio between the strains. However, in the low nutrient regime, before collapse of the obligate mutualism, we find that the ratio rapidly reaches its equilibrium and it is the total abundance that is slow to reach equilibrium. Our results provide a general framework for how mutualisms may transition between qualitatively different regimes of interaction in response to changes in nutrient availability in the environment.

Byproduct Cross Feeding and Community Stability in an In Silico Biofilm Model of the Gut Microbiome

“…Well-mixed suspension cultures have the disadvantage that species with widely differing growth rates cannot be co-cultured without engineering artificial dependencies such as amino acid cross feeding between the species [56]. Natural microbial communities have evolved numerous mechanisms for ensuring species coexistence, most notably the biofilm mode of growth.…”

The social network of microorganisms — how auxotrophies shape complex communities

“…A study using amino-acid-auxotrophic yeast strains demonstrated that changes in amino acid availability can modulate the types of interaction between species. Depending on the resource availability, the interaction of these strains changed from obligatory and facultative mutualism to competition and parasitism 69 . Unravelling these dependencies and the resulting dynamic interactions of members in a community would be of great importance for microbiome research.…”

Resource abundance and the critical transition to cooperation

“…Notably, by adjusting amino acid concentrations, Hoek et al . recently altered the relationship between two yeast strains through several distinct outcomes from obligate mutualism to competitive exclusion (Hoek et al ., ).…”