Localized coevolution between microbial predator and prey alters community-wide gene expression and ecosystem function

In dynamic and spatially heterogeneous microbial communities, pairs of locally coevolved species interact between themselves and other species across multiple spatial and temporal scales. We currently do not understand how local pairwise coevolutionary processes scale to influence whole microbial communities and how local coevolutionary processes affect wider species interaction networks. Here we investigate the community-wide functional response to a coevolutionary mismatch between a focal bacterial prey species and its ciliate predator in a synthetic 30 species microbial community over two months. We observed that the coevolved prey had little influence on community structure or carrying capacity in the presence or absence of the coevolved predator. However, community metabolic potential (represented by per-cell ATP concentration) was significantly higher in the presence of both coevolved focal species. This ecosystem-level response was mirrored by community-wide transcriptional shifts that resulted in the differential regulation of nutrient acquisition and surface colonization pathways across multiple species. Our findings suggest that the disruption of localized pairwise coevolution can alter community-wide transcriptional networks, even when the overall ecological response is muted. We propose that these altered expression patterns may be an important signal of future diversification and ecological change. SignificanceClosely interacting microbial species pairs (e.g., predator and prey) can become coadapted via reciprocal natural selection. A fundamental challenge in evolutionary ecology is to untangle how coevolution in small species groups affects and is affected by biotic interactions in diverse communities. We conducted an experiment with an idealized 30 species microbial community where we experimentally manipulated the coevolutionary history of a predator and a single prey species. Altering the coevolutionary history of the prey had little effect on the ecology of the system but induced large functional changes in community transcription and metabolic potential. Our results illustrate that localized coevolutionary processes between species pairs can reverberate through ecosystem-scale transcriptional networks with important consequences for broader ecosystem function.