Literature covered: early 2000s to late 2017Bacteria frequently exchange metabolites with other micro- and macro-organisms. In these often obligate cross-feeding interactions, primary metabolites such as vitamins, amino acids, nucleotides, or growth factors are exchanged. The widespread distribution of this type of metabolic interactions, however, is at odds with evolutionary theory: why should an organism invest costly resources to benefit other individuals rather than using these metabolites to maximize its own fitness? Recent empirical work has shown that bacterial genotypes can significantly benefit from trading metabolites with other bacteria relative to cells not engaging in such interactions. Here, we will provide a comprehensive overview over the ecological factors and evolutionary mechanisms that have been identified to explain the evolution and maintenance of metabolic mutualisms among microorganisms. Furthermore, we will highlight general principles that underlie the adaptive evolution of interconnected microbial metabolic networks as well as the evolutionary consequences that result for cells living in such communities.

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Bacteria frequently lose biosynthetic genes, thus making them dependent on an environmental uptake of the corresponding metabolite. Despite the ubiquity of this ‘genome streamlining’, it is generally unclear whether the concomitant loss of biosynthetic functions is favored by natural selection or rather caused by random genetic drift. Here we demonstrate experimentally that a loss of metabolic functions is strongly selected for when the corresponding metabolites can be derived from the environment. Serially propagating replicate populations of the bacterium Escherichia coli in amino acid-containing environments revealed that auxotrophic genotypes rapidly evolved in less than 2,000 generations in almost all replicate populations. Moreover, auxotrophs also evolved in environments lacking amino acids–yet to a much lesser extent. Loss of these biosynthetic functions was due to mutations in both structural and regulatory genes. In competition experiments performed in the presence of amino acids, auxotrophic mutants gained a significant fitness advantage over the evolutionary ancestor, suggesting their emergence was selectively favored. Interestingly, auxotrophic mutants derived amino acids not only via an environmental uptake, but also by cross-feeding from coexisting strains. Our results show that adaptive fitness benefits can favor biosynthetic loss-of-function mutants and drive the establishment of intricate metabolic interactions within microbial communities.

In bacterial communities, cells often communicate by the release and detection of small diffusible molecules, a process termed quorum-sensing. Signal molecules are thought to broadly diffuse in space; however, they often regulate traits such as conjugative transfer that strictly depend on the local community composition. This raises the question how nearby cells within the community can be detected. Here, we compare the range of communication of different quorum-sensing systems. While some systems support long-range communication, we show that others support a form of highly localized communication. In these systems, signal molecules propagate no more than a few microns away from signaling cells, due to the irreversible uptake of the signal molecules from the environment. This enables cells to accurately detect micron scale changes in the community composition. Several mobile genetic elements, including conjugative elements and phages, employ short-range communication to assess the fraction of susceptible host cells in their vicinity and adaptively trigger horizontal gene transfer in response. Our results underscore the complex spatial biology of bacteria, which can communicate and interact at widely different spatial scales.