Abstract
Multi-species microbial communities play a critical role in human health, industry, and waste remediation. Recently, the evolution of synthetic consortia in the laboratory has enabled adaptation to be addressed in the context of interacting species. Using an engineered bacterial consortium, we repeatedly evolved cooperative genotypes and examined both the predictability of evolution and the phenotypes that determine community dynamics. Eight Salmonella enterica serovar Typhimurium strains evolved methionine excretion sufficient to support growth of an Escherichia coli methionine auxotroph, from whom they required excreted growth substrates. Non-synonymous mutations in metA, encoding homoserine trans-succinylase (HTS), were detected in each evolved S. enterica methionine cooperator and were shown to be necessary for cooperative consortia growth. Molecular modeling was used to predict that most of the non-synonymous mutations slightly increase the binding affinity for HTS homodimer formation. Despite this genetic parallelism and trend of increasing protein binding stability, these metA alleles gave rise to a wide range of phenotypic diversity in terms of individual versus group benefit. The cooperators with the highest methionine excretion permitted nearly two-fold faster consortia growth and supported the highest fraction of E. coli, yet also had the slowest individual growth rates compared to less cooperative strains. Thus, although the genetic basis of adaptation was quite similar across independent origins of cooperative phenotypes, quantitative measurements of metabolite production were required to predict either the individual-level growth consequences or how these propagate to community-level behavior.
Highlights
Multi-species microbial communities critical to human health [1,2], industrial production [3], and waste remediation [4,5] are governed by complex social dynamics
We found that methionine excretion correlated negatively with individual growth of S. enterica, but positively with the growth rate of the consortia and with the proportion of E. coli partner that the given strains could maintain
To explore the genetic and physiological range of adaptations underlying the rise of cooperation in our consortium, we repeatedly evolved methionine-producing S. enterica strains by selecting for their ability to support growth of their auxotrophic E. coli partner (Fig 1)
Summary
Multi-species microbial communities critical to human health [1,2], industrial production [3], and waste remediation [4,5] are governed by complex social dynamics. Predicting how these communities might respond to environmental changes requires an understanding of how species interactions change the evolution of new traits. A cooperative species that excretes a beneficial cellular product, or “public good,” may alter the environment and alter the selective pressure on other species [8] When this cooperation is costly to individual growth, but rewarded by cooperative behavior, a complex tension arises in which the relative costs and benefits and the structure of the interactions determine whether the cooperation is driven to fixation, coexists, or is eliminated. From the point of view of adaptation, it is unclear whether evolution in communities should be highly variable between instances, owing to the presence of multiple partners, or highly similar, because there are often few phenotypes that primarily govern the interaction [7,9,10]
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