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

, , , , , и .
PLOS Biology, 14 (8): e1002540+ (24.08.2016)
DOI: 10.1371/journal.pbio.1002540

Аннотация

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. Species often engage in mutualistic interactions that are beneficial for both partners. However, there is also a cost associated with cooperation, for example, in the form of energy required to make nutrients for a partner. When environments change, the costs and benefits of cooperating can change as well, and this can cause the mutualistic interaction to break down into other interaction types, such as parasitism. In this study, we varied nutrient availability to examine how changing environments can affect the interaction between two cross-feeding yeast strains. Lower nutrient concentrations made each strain more dependent on the nutrients provided by its partner strain and thus favored cooperation. Using both experiments and mathematic models, we found that in different environments, these yeast strains can interact in at least seven different qualitatively different ways, including obligate mutualism, facultative mutualism, parasitism, and competition. We also found that the dynamics of how the two strains influence each other change drastically in different nutrient concentrations. Examining the population dynamics could therefore potentially be used to predict the stability or collapse of a community.

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