Resource Availability Modulates the Cooperative and Competitive Nature of a Microbial Cross-Feeding Mutualism - PubMed (original) (raw)

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

Tim A Hoek et al. PLoS Biol. 2016.

Erratum in

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.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1

Fig 1. Two auxotrophic yeast strains can form a stable cross-feeding mutualism in a range of nutrient concentrations.

(A) The YFP-tagged strain is unable to produce the amino acid tryptophan but overproduces the amino acid leucine, whereas the RFP-tagged strain is unable to produce leucine but overproduces tryptophan. (B) The mutualism is probed by co-culturing the two auxotrophic yeast strains in batch culture with 10x dilution daily. Flow cytometry and spectrophotometry report on the relative fraction and total abundance of the two yeast strains at the end of each day of growth. (C) Optical density after 8 d of daily dilution and growth. The co-culture is able to survive in low amino acid concentrations where the monocultures cannot survive (solid lines indicate the concentrations below which each auxotrophic strain goes extinct). (D) Abundance of the co-culture (solid line) and monocultures (dashed line) for the Trp- (green) and Leu- (red) strains. In low amino acid concentrations (1 and 8 μM), the strains form an obligate mutualism; in medium amino acid concentrations (8 and 64 μM), the strains form a facultative mutualism; and in high amino acid concentrations (32 and 256 μM), the strains form an amensalism, as the Leu- strain is relatively unaffected and the Trp- strain is harmed by the interaction.

Fig 2

Fig 2. A simple phenomenological model predicts that a cross-feeding mutualism can shift between many qualitative outcomes.

Plot shows equilibrium density of co-cultures (solid lines) or monocultures (dashed lines) as a function of amino acids. The colorbar above the plot shows the qualitative regimes of interaction and indicates the effect of growth in co-culture for both strains in comparison with their growth in monoculture. Effects of growing in co-culture can be beneficial (+), harmful (-), neutral (0), or leading to extinction (X).

Fig 3

Fig 3. Our experimental cross-feeding mutualism shifts between the predicted eight different qualitative outcomes.

Co-cultures were grown at amino acid concentrations ranging from 0 to 200 μM Tryptophan and 0 to 1,600 μM Leucine. Leucine concentrations were 8 times higher than tryptophan concentrations in all conditions. Cultures were started at 6 different fractions and run for 7 d with a 10x dilution each day. In cultures that reached equilibrium (small dots), data shows mean density (+- standard error of the mean [s.e.m]), whereas in cultures that did not reach equilibrium (larger triangles), mean equilibrium density is estimated based on growth (+- s.e.m. S2 and S3 Figs, S1 Information). Colorbar above the plot shows the qualitative regimes of interaction as in Fig 2.

Fig 4

Fig 4. Eigenvector orientation predicts characteristic behaviors prior to population collapse.

Main plot shows the two eigenvalues as a function of supplemented amino acids (black and magenta solid lines). Population collapse occurs when the slower eigenvalue (magenta solid line) reaches zero. Insets I–V show simulated population trajectories (solid, arrowed black lines) for different amino acid concentrations and starting from different initial population densities (small black dots). The eigenvector (magenta arrow) of the stable equilibrium point (blue dot) corresponds to the slower eigenvalue. Insets show that trajectories align to the eigenvector when the system is close to collapse. This indicates that the ratio of the densities of each strain within the population (i.e., f = X/Y) relaxes faster than the total population size (i.e., n = X+Y) when the system is close to extinction (inset I), whereas the opposite scenario occurs before the competitive exclusion regime (inset V).

Fig 5

Fig 5. Relaxation dynamics is observed before population collapse.

In each figure, we started co-cultures at 48 different population sizes (n = X+Y) and relative abundances (f = X/Y). Six co-cultures per figure are highlighted (colored arrows), with day 0 density represented by a colored dot and each arrow signifying the change over a single day. Black dots on the axes indicate monoculture equilibria, whereas the blue dot shows the co-culture equilibrium. (A) In obligatory mutualistic conditions, close to extinction, populations approach equilibrium from the direction corresponding to constant ratio, f. (B) In medium amino acid concentrations, there is no privileged direction for approaching equilibrium. (C) At high concentrations, when the two strains compete against each other, the population approaches equilibrium from the constant n manifold. Axes are linear at densities of 0 to 104 cells/well and logarithmic for higher densities.

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