A passive mutualistic interaction promotes the evolution of spatial structure within microbial populations

Abstract

BackgroundWhile mutualistic interactions between different genotypes are pervasive in nature, their evolutionary origin is not clear. The dilemma is that, for mutualistic interactions to emerge and persist, an investment into the partner genotype must pay off: individuals of a first genotype that invest resources to promote the growth of a second genotype must receive a benefit that is not equally accessible to individuals that do not invest. One way for exclusive benefits to emerge is through spatial structure (i.e., physical barriers to the movement of individuals and resources).ResultsHere we propose that organisms can evolve their own spatial structure based on physical attachment between individuals, and we hypothesize that attachment evolves when spatial proximity to members of another species is advantageous. We tested this hypothesis using experimental evolution with combinations of E. coli strains that depend on each other to grow. We found that attachment between cells repeatedly evolved within 8 weeks of evolution and observed that many different types of mutations potentially contributed to increased attachment.ConclusionsWe postulate a general principle by which passive beneficial interactions between organisms select for attachment, and attachment then provides spatial structure that could be conducive for the evolution of active mutualistic interactions.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-017-0950-y) contains supplementary material, which is available to authorized users.

Evolution on the bright side of life: microorganisms and the evolution of mutualism

“…Their use in evolution experiments has allowed scientists to address fundamental questions about the process of evolution, foraging theory, origins of multicellarity, coevolution in host–parasite interactions, and the evolution of cooperation . However, experimental evolution has only recently been applied to understanding mutualism …”

“…Laboratory experiments with cross‐feeding microorganisms have repeatedly documented selection for cheating within mutualism and characterized the impact of exploiters on pairs of mutualists . However, most of this work has focused on identifying mechanisms for suppressing the effects of cheaters, often focusing on the impact of spatial structure and aggregation . This research has shown that spatial structure and aggregation keep cooperative pairings together for multiple generations, allowing them to flourish through partner‐fidelity feedback .…”

“…27,[42][43][44] However, experimental evolution has only recently been applied to understanding mutualism. 10,11,15…”

“…More recently, scientists have begun experimenting with mutualistic interactions between microorganisms . Diverse mutualisms have been engineered or evolved in the laboratory with the goal of understanding microbial physiology and metabolism and understanding how mutualisms can evolve and be stable .…”

“…More recently, scientists have begun experimenting with mutualistic interactions between microorganisms. [10][11][12][13][14][15][16] Diverse mutualisms have been engineered or evolved in the laboratory with doi: 10.1111/nyas.13515 the goal of understanding microbial physiology and metabolism and understanding how mutualisms can evolve and be stable. 10,12,13,17,18 These systems can be outstanding tools for experimentation, yet they have rarely been used to address some of the most pressing questions about the selection environment in mutualism.…”