Disentangling strictly self-serving mutations from win-win mutations in a mutualistic microbial community

Mutualisms can be promoted by pleiotropic win-win mutations which directly benefit self (self-serving) and partner (partner-serving). Intuitively, partner-serving phenotype could be quantified as an individual’s benefit supply rate to partners. Here, we demonstrate the inadequacy of this thinking, and propose an alternative. Specifically, we evolved well-mixed mutualistic communities where two engineered yeast strains exchanged essential metabolites lysine and hypoxanthine. Among cells that consumed lysine and released hypoxanthine, a chromosome duplication mutation seemed win-win: it improved cell’s affinity for lysine (self-serving), and increased hypoxanthine release rate per cell (partner-serving). However, increased release rate was due to increased cell size accompanied by increased lysine utilization per birth. Consequently, total hypoxanthine release rate per lysine utilization (defined as ‘exchange ratio’) remained unchanged. Indeed, this mutation did not increase the steady state growth rate of partner, and is thus solely self-serving during long-term growth. By extension, reduced benefit production rate by an individual may not imply cheating.
eLife digest Many organisms – including microbes – have mutually beneficially relationships. Often, the exchanged goods, such as nutrients, are costly to make. But what happens when individuals evolve to help themselves more? Can they also evolve to be more helpful to others? Hart, Pineda et al. studied a community of two genetically modified yeast strains that had to exchange essential nutrients to survive. One strain overproduced the molecule hypoxanthine, but depended on the second strain to provide the nutrient lysine, and vice versa. The communities were then allowed to evolve. The lysine-requiring strain frequently ended up with a mutation that initially seemed to be win-win: helping self to grow faster and at the same time, releasing more hypoxanthine to the partner. However, closer examination showed that the mutation also made these cells bigger, and bigger cells had to consume more lysine. Consequently, releasing more hypoxanthine was accompanied by consuming more lysine. Since the 'give' to 'take' ratio stayed the same, the partner strain did not benefit more from the mutant than from the ancestor. This suggests that an individual should not be considered helpful solely based on how much it gives to a partner, but also, on how much it takes. In the case of the mutant yeast strain, it produced 30 percent more nutrients, but also consumed 30 percent more, and was therefore not more helpful to the partner than the ancestor. Similarly, releasing less may not imply cheating. Beneficial interactions are very common in natural communities, such as among microbes living in the mouth cavity and the gut. Therefore, a better understanding of how they benefit from and affect each other may provide scientists with more insight into diseases linked to problems with microbial communities, such as tooth decay, inflammation of the gut, or obesity.