Eco-evolutionary modelling of microbial syntrophy indicates the robustness of cross-feeding over cross-facilitation

Abstract Syntrophic cooperation among prokaryotes is ubiquitous and diverse. It relies on unilateral or mutual aid that may be both catalytic and metabolic in nature. Hypotheses of eukaryotic origins claim that mitochondrial endosymbiosis emerged from mutually beneficial syntrophy of archaeal and bacterial partners. However, there are no other examples of prokaryotic syntrophy leading to endosymbiosis. One potential reason is that when externalized products become public goods, they incite social conflict due to selfish mutants that may undermine any mutualistic interactions. To rigorously evaluate these arguments, here we construct a general mathematical framework of the ecology and evolution of different types of syntrophic partnerships. We do so both in a general microbial and in a eukaryogenetic context. Studying the case where partners cross-feed on each other’s self-inhibiting waste, we show that cooperative partnerships will eventually dominate over selfish mutants. By contrast, systems where producers actively secrete enzymes that cross-facilitate their partners’ resource consumption are not robust against cheaters over evolutionary time. We conclude that cross-facilitation is unlikely to provide an adequate syntrophic origin for endosymbiosis, but that cross-feeding mutualisms may indeed have played that role.