Bacteria-phage (co)evolution is constrained in a synthetic community across multiple bacteria-phage pairs

Abstract

Bacteriophages can be important drivers of bacterial densities, and therefore microbial community composition and function. These ecological interactions are likely to be greatly affected by evolutionary dynamics, because bacteria can rapidly evolve resistance to phage while phage can reciprocally evolve to increase infectivity. Most studies to date have explored eco-evolutionary dynamics using isolated pairs of bacteria-phage but in nature, multiple bacteria and phages coexist and (co)evolve simultaneously. How coevolution plays out in this context is poorly understood. Here, we examine how three coexisting soil bacteria (Ochrobactrum sp., Pseudomonas sp., and Variovorax sp.) interact and evolve with three species-specific bacteriophages over eight weeks of experimental evolution, both as host-parasite pairs in isolation and as a mixed community. Across all species phage resistance evolution was inhibited in polyculture, with the most pronounced effect on Ochrobactrum. Between bacteria-phage pairs there were also substantial differences in the effect of phage on host densities, and evolutionary dynamics including whether pairs coevolved. These contrasts emphasise the difficulty in generalising from monoculture to polyculture, and between bacteria-phage pairs to wider systems. Future studies should consider how multiple bacteria and phage pairs interact simultaneously to better understand how coevolutionary dynamics happen in natural communities. ImportanceThis project is unique in examining evolutionary dynamics among coexisting bacteria and their phages, rather than focus on single focal species - this makes our work more applicable to natural contexts while still working with controlled synthetic communities. While it is commonly assumed that bacteria will evolve phage resistance and coevolve with phage, this may be uncommon in more complex communities due to reduced contact rates and/or reduced mutation rates. Furthermore, the contrast in population dynamics and ability to coevolve between bacteria-phage pairs highlights the need for more pairs to be studied. Over-reliance on model systems that are known to coevolve means we lack an understanding of how wider bacteria-phage pairs interact, and to what extent results can be generalised beyond these pairs.