Abstract
Bacteria are estimated to constitute ~15% of Earth’s biomass and contribute greatly to global resource turnover1. Predatory bacteria, pervasive throughout terrestrial and aquatic habitats2,3, are likely to strongly influence such ecosystem processes and, given the importance of predators to macro-organismal communities4–6, microbial community evolution as well7–9. Here we show that coevolution of a generalist bacterial predator (Myxococcus xanthus) with one species of bacterial prey (Escherichia coli) greatly alters patterns of fitness and genome evolution for both predators and prey and drives sympatric phenotypic diversification of prey. Following ~165 generations of evolution, coevolved prey outcompeted control-evolved prey in the presence of all predators (ancestral, control evolved and coevolved) but not in their absence. Suggestive of Red Queen dynamics10, coevolved predators were found to be more fit relative to their ancestor during consumption of coevolved prey than ancestral prey. Coevolved populations of both predators and prey exhibited greatly accelerated genome evolution relative to controls, including the rapid appearance of mutator genotypes in three coevolved communities. Both predators and prey underwent strong parallel evolution at selection hotspots specific to the coevolution treatment, with all 12 coevolved predator populations mutating at a locus not previously associated with M. xanthus predation. Reciprocally, predators drove strong parallel adaptations at two virulence-associated traits among prey- mucoidy11 and the outer-membrane protease OmpT12. Mucoid variants appeared in 10/12 coevolved prey populations but in only one control. Further, 11/12 coevolved prey populations, but no controls, mutated at ompT, experimental deletion of which increased prey fitness in the presence of predators but not in their absence. These results with simple two-species communities suggest that generalist predatory bacteria are important determinants of how complex prey communities and their interaction networks evolve and diversify in natural habitats.
Footnotes
↵* co-first authors