Spatial structure is a well-known universal mechanism to promote cooperation 17, which frequently emerges in bacterial populations, for instance, due to the restricted range of microbial interactions 18, 19. We considered specifically a scenario where a bacterial community is organized as a dynamical metapopulation (i.e., the community is transiently separated into groups, adding to other implementations of spatial structure such as groups connected via migration, and range expansions) 14, 15, 16, and a public good is essential for its survival. This is linked to the synergistic effects of spatial structure and eco-evolutionary feedbacks, that impact in a nonintuitive manner on the dilemma 12, 13. Here, we show how cheating can instead induce the continuance of cooperation, a prospect that has yet remained largely unexplored 6.
Much previous work focused therefore on identifying mechanisms that prevent the invasion of cheaters 7. With their particular relevance to humans in matters of health (microbiome) 10, and industry (bioremediation, biofuels, etc) 11, the necessity of recognizing the consequences of social dilemmas in microorganisms becomes even more significant. The threat of cheaters represents at a microbial scale a well-known public-good dilemma, known as the tragedy of the commons 9, and can fundamentally interfere with the sustainability of these communities. Notably, the functions of these, and equivalent, public goods are constantly at the risk of being disabled by the invasion of cheaters in the population, individuals that do not contribute and only reap the advantages of the common resource 5, 6, 7, 8. Classical examples comprise molecules that can specify the precise density reached by a population (quorum-sensing autoinducers) 1, support the assemblage of collective multicellular structures (biofilms extracellular polymeric substances) 2, or process basic nutrients that would be unavailable otherwise (iron-scavenging siderophores, exoenzymes catalyzing the decomposition of complex sugars, etc.) 3, 4. These resources generally entail compounds secreted into the environment, which in effect work as public goods. In many bacterial populations, resources produced by an individual may benefit other members of the population. Our work explains the unanticipated dynamics that eco-evolutionary feedbacks can generate in microbial communities, feedbacks that reveal fundamental for the adaptive change of ecosystems at all scales. The characterization of the experimental system identifies additional factors that can matter, like the impact of the lag phase on the tolerance to stress, or the appearance of spontaneous mutants.
We validate this result by carefully combining theory and experiments, with the engineering of a synthetic bacterial community in which the public compound allows survival to a lethal stress. The effect is made possible by the interplay between spatial constraints and the essentiality of the shared resource. Here, we show that the demographic collapse induced by cheaters in the population can actually contribute to the rescue of cooperation, in a clear illustration of how ecology and evolution can influence each other. However, that invasions result instead in the persistence of cooperation is a prospect that has yet remained largely unexplored. Minimizing cheater invasions appears then as a necessary mechanism to maintain these populations. Bacterial populations whose growth depends on the cooperative production of public goods are usually threatened by the rise of cheaters that do not contribute but just consume the common resource.
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