Rapid evolution of stability and productivity at the origin of a microbial mutualism

Abstract

Mutualistic interactions are taxonomically and functionally diverse. Despite their ubiquity, however, the basic ecological and evolutionary processes underlying their origin and maintenance are poorly understood. A major reason for this is the lack of an experimentally tractable model system. We examine the evolution of an experimentally imposed obligate mutualism between sulfatereducing and methanogenic microorganisms that have no known history of previous interaction. Twenty-four independent pairings (cocultures) of the bacterium Desulfovibrio vulgaris and the archaeon Methanococcus maripaludis were established and followed for 300 community doublings in two environments, one allowing for the development of a heterogeneous distribution of resources and the other not. Evolved cocultures grew up to 80% faster and were up to 30% more productive (biomass yield per mole of substrate) than the ancestors. The evolutionary process was marked by periods of significant instability leading to extinction of two of the cocultures, but it resulted in more stable, efficient, and productive mutualisms for most replicated pairings. Comparisons of evolved cocultures with those assembled from one evolved mutualist and one ancestral mutualist showed that evolution of both species contributed to improved productivity. Surprisingly, however, overall improvements in growth rate and yield were less than the sum of the individual contributions, suggesting antagonistic interactions between mutations from the coevolved populations. Physical constraints on the transfer of metabolites in the evolution environment affected the evolution of M. maripaludis, but not of D. vulgaris. Together, these results demonstrate that challenges can imperil nascent obligate mutualisms and demonstrate the evolutionary responses that enable their persistence and future evolution.adaptation | experimental evolution | environmental heterogeneity | syntrophy | methanogenesis

How sulphate-reducing microorganisms cope with stress: lessons from systems biology

“…This situation could lead to unstable growth, especially if one species is inhibited [83][84][85] . A recent experiment with 24 independently evolving co-cultures confirmed these predictions 86 . Initially, growth was unstable and two cocultures almost went extinct.…”

Dynamics in the mixed microbial concourse

“…The partnership between D. vulgaris and M. maripaludis, discussed above, can be broken and reinitiated under controlled conditions (Hillesland and Stahl 2010). Although these strains derive from syntrophic lineages, they have been isolated from different environments and propagated separately.…”

Microbial mutualism dynamics governed by dose-dependent toxicity of cross-fed nutrients

“…As an alternative, synthetic microbial communities (cocultures) have been developed in which two or more species are cultivated together under laboratory conditions. Cocultures preserve core aspects of natural systems while offering greater practical experimental control (Shou et al, 2007;Hillesland and Stahl, 2010;Summers et al, 2010;Harcombe, 2010;Momeni et al, 2011;Hom and Murray, 2014;Mee et al, 2014). They are also more amenable to modeling than are natural systems and facilitate the development, experimental testing and refining of models for predicting community behavior (Zomorrodi and Segrè, 2015;Johns et al, 2016;Lindemann et al, 2016;Widder et al, 2016).…”