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Abstract

Bacteriophages are important drivers of microbial ecosystems, but their influence and dynamics in terrestrial biomes remain poorly understood compared to aquatic and host-associated systems. To investigate this, we analyzed shotgun metagenomics datasets from ten compost-derived microbial communities propagated over 48 weeks. We found that the communities clustered into two distinct types consisting of hundreds of microbial genera, and in one community type identified Theomophage, a lytic bacteriophage representing a new Schitoviridae subfamily, which accounted for up to 74.3% of the total community metagenome, indicating massive viral outbreaks. We tracked molecular evolution of Theomophage and found that isolated communities were dominated by a single strain that showed little molecular evolution during outbreaks. However, when experimental manipulation allowed phages to migrate between communities, we observed transient coexistence of strains followed by genomic recombination that underpinned replacement of the ancestral strains. Additionally, when Theomophage colonized mesocosms where it was originally absent, new mutations evolved that fixed and spread to other communities. Our study describes the largest bacteriophage outbreak reported to date and reveals the spatial and temporal scales at which terrestrial bacteriophage microdiversity evolves. It also demonstrates that mixing of viral communities, which may be frequent in natural systems, promotes rapid bacteriophage evolution.

Significance Statement Terrestrial viral ecology and evolution is an active research area, but current knowledge on soil viruses still lags behind that of other biomes, and the terrestrial microbiome harbors untapped viral diversity. This study describes parallel, massive outbreaks of a novel bacteriophage in a 48- week evolution experiment with compost-derived microbial communities. The unprecedented abundance of this bacteriophage highlights the importance of accounting for viral sequences – which may be challenging to identify and annotate – when analyzing community sequence data. Moreover, we show how dispersal accelerates the dynamics of molecular evolution on a timescale of weeks. These results advance understanding of the spatiotemporal scales at which bacteriophage eco-evolutionary dynamics play out in terrestrial biomes.