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

Bacteriophages are important drivers of microbial ecosystems, yet their dynamics in complex natural communities remain poorly understood compared to simplified laboratory systems. To address this gap, we analyzed viral dynamics across 20 compost-derived microbial communities propagated for one year in mesocosms. Communities clustered into two distinct types, each dominated by different cellulose-degraders and comprising hundreds of genera. In one type, we observed massive, parallel outbreaks of Theomophage, a previously undescribed bacteriophage, reaching 74% of metagenomic sequencing reads, the largest bacteriophage outbreak documented to date. Theomophage populations in isolated communities were composed of a single genotype that showed striking evolutionary stability throughout the experiment. In contrast, following experimental viral migration between mesocosms, all Theomophage populations showed rapid evolution via recombination between preexisting genotypes, replacement of ancestral lineages, and, upon successful migration to mesocosms of the alternate community type where Theomophage was initially absent, rapid acquisition of novel mutations that swept local populations and then spread to other mesocosms. Our study reveals the spatial and temporal scales at which bacteriophage microdiversity evolves in complex communities. It further shows that mixing of viral communities -- likely common in natural systems -- can rapidly accelerate bacteriophage evolution.