Synergistic epistasis enhances the co-operativity of mutualistic interspecies interactions

Abstract

Early evolution of mutualism is characterized by big and predictable adaptive changes, including the specialization of interacting partners, such as through deleterious mutations in genes not required for metabolic cross-feeding. We sought to investigate whether these early mutations improve cooperativity by manifesting in synergistic epistasis between genomes of the mutually interacting species. Specifically, we have characterized evolutionary trajectories of syntrophic interactions of Desulfovibrio vulgaris (Dv) with Methanococcus maripaludis (Mm) by longitudinally monitoring mutations accumulated over 1000 generations of nine independently evolved communities with analysis of the genotypic structure of one community down to the single-cell level. We discovered extensive parallelism across communities despite considerable variance in their evolutionary trajectories and the perseverance within many evolution lines of a rare lineage of Dv that retained sulfate-respiration (SR+) capability, which is not required for metabolic cross-feeding. An in-depth investigation revealed that synergistic epistasis across pairings of Dv and Mm genotypes had enhanced cooperativity within SR− and SR+ assemblages, enabling their coexistence within the same community. Thus, our findings demonstrate that cooperativity of a mutualism can improve through synergistic epistasis between genomes of the interacting species, enabling the coexistence of mutualistic assemblages of generalists and their specialized variants.

The evolution of reduced facilitation in a four-species bacterial community

“…2C, D). As in other such experiments 10,20,26 , we also observed some parallelism in genomic evolution, where several mutations and deletions occurred in parallel lines of the same experimental condition, at least in Ct . While it is tempting to speculate on the effects these mutations might have, we prefer to leave mechanistic analyses to future work where we would build the appropriate mutants.…”

“…In contrast, studies that have experimentally evolved communities beginning with positive or facilitative interactions mostly contain only two species or two strains of the same species, often with strong dependencies on one another 10,[20][21][22][23][24][25][26] . This may be because microbial isolates tend to compete with one another when co-cultured in the lab 27 , meaning that a synthetic community assembled in the lab is unlikely to spontaneously display several positive inter-species interactions.…”

Evolutionary repeatability of emergent properties of ecological communities

“…Laboratory evolution studies have been carried out in various antagonistic (usually, bacteria-phage [24,26,), mutualistic and commensal [141][142][143][144][145][146][147][148][149][150][151][152][153][154][155][156] systems with two or more [22,[157][158][159][160][161][162][163][164][165] species and in adaptive diversifications [61,106,107,[166][167][168][169][170][171][172]. While most of these studies do not focus on evolutionary repeatability per se, the data they collect show that various community-level properties, such as absolute and relative abundances of community members [111,145,146,173], species interactions [24,174,175], community growth rate [142,…”

Evolutionary repeatability of emergent properties of ecological communities

“…Laboratory evolution studies have been carried out in various antagonistic (usually, bacteriaphage [18,20,), mutualistic and commensal [135][136][137][138][139][140][141][142][143][144][145][146][147][148][149][150] systems with two-or more [151][152][153][154][155][156][157][158][159][160] species and in adaptive diversifications [55,100,101,[161][162][163][164][165][166][167]. While most of these studies do not focus on evolutionary repeatability per se, the data they collect show that various community-level properties, such as absolute and relative abundances of community members [105,139,140,168], species interactions [18,169,170], community growth rate [136,…”