Snowdrift game dynamics and facultative cheating in yeast

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Abstract
Yeast secrete invertase to break down sucrose into monosaccharides that they can metabolize. Gore et al. show that 99% of the monosaccharides diffuse away to where they can be used by other yeast cells, making this a cooperative behaviour susceptible to cheating by cells that do not secrete invertase. But that remaining 1% is sufficient to give the cooperators an advantage under certain circumstances. They can invade populations of cheaters, and the equilibrium frequencies of cheaters and cooperators that results depends on the concentration of glucose. Using both this experimental work and theoretical modelling, the authors show that this is not a prisoner's dilemma situation, but rather a snowdrift game, in which cheating can be profitable, but is not necessarily the best strategy if others are cheating too. Yeast secrete invertase to break down sucrose into monosaccharides that they can metabolize. However, 99% of the monosaccharides diffuse away where they can be used by other yeast cells, making this a cooperative behaviour that is susceptible to cheating by cells that do not secrete invertase. Here this is shown to be a snowdrift game, in which cheating can be profitable, but is not necessarily the best strategy if others are cheating too. The origin of cooperation is a central challenge to our understanding of evolution1,2,3. The fact that microbial interactions can be manipulated in ways that animal interactions cannot has led to a growing interest in microbial models of cooperation4,5,6,7,8,9,10 and competition11,12. For the budding yeast Saccharomyces cerevisiae to grow on sucrose, the disaccharide must first be hydrolysed by the enzyme invertase13,14. This hydrolysis reaction is performed outside the cytoplasm in the periplasmic space between the plasma membrane and the cell wall. Here we demonstrate that the vast majority (∼99 per cent) of the monosaccharides created by sucrose hydrolysis diffuse away before they can be imported into the cell, serving to make invertase production and secretion a cooperative behaviour15,16. A mutant cheater strain that does not produce invertase is able to take advantage of and invade a population of wild-type cooperator cells. However, over a wide range of conditions, the wild-type cooperator can also invade a population of cheater cells. Therefore, we observe steady-state coexistence between the two strains in well-mixed culture resulting from the fact that rare strategies outperform common strategies—the defining features of what game theorists call the snowdrift game17. A model of the cooperative interaction incorporating nonlinear benefits explains the origin of this coexistence. We are able to alter the outcome of the competition by varying either the cost of cooperation or the glucose concentration in the media. Finally, we note that glucose repression of invertase expression in wild-type cells produces a strategy that is optimal for the snowdrift game—wild-type cells cooperate only when competing against cheater cells.