Eco-evolutionary dynamics of massive, parallel bacteriophage outbreaks in compost communities

Bacteriophages play critical roles in microbial ecosystems, yet their dynamics in complex natural communities remain poorly understood compared to simplified laboratory systems. Here, we tracked viral dynamics in 20 compost-derived microbial communities over 1 year. Communities formed two alternative stable types, each dominated by distinct cellulose degraders and comprising hundreds of genera. In one community type, we observed massive, parallel outbreaks of Theomophage, a previously uncharacterized member of the Schitoviridae, reaching up to 74% of metagenomic reads—the largest bacteriophage outbreak documented to date. Despite extensive replication, Theomophage displayed notable genetic stability during outbreaks and over time. In contrast, the experimental migration of viral communities triggered rapid evolution driven by recombination and the accumulation of newly arising mutations, particularly after colonization of communities of the alternative type in which the phage was initially absent. These results reveal the spatial and temporal scales at which bacteriophage microdiversity evolves in complex ecosystems and show that viral mixing, likely common in nature, can rapidly accelerate phage evolution.