Jeroen Meijer, Paulien Hogeweg, Paul Rainey, Bas Dutilh.
Bacteriophages are important players in shaping microbial communities, yet their abundance and dynamics in highly diverse, natural environments remain poorly understood. In particular, many different genotypes of a single phage can be present, but their relevance for viral dynamics and ecological interactions is not currently known. Here, we explore this question by analyzing shotgun metagenomes from 10 compost-derived microbial communities that were tracked in parallel over a period of 1 year, where size-filtered viral fractions were periodically collected, pooled and redistributed between different mesocosms to allow viral migration between communities. By comparing viromes and full community metagenomes we recovered thousands of viral sequences, which revealed both parallel and divergent viral dynamics between the 10 communities. In a subset of communities and time points a single, previously undescribed Schitoviridae bacteriophage accounted for up to 74% of the total community metagenome (i.e. combined cellular and viral sequences), indicating massive viral outbreaks of a single bacteriophage. Tracking polymorphisms of the bacteriophage and taxonomic profiling of the full microbial communities showed that different mesocosms were initially dominated by a single bacteriophage strain which transferred and settled in other communities through the experimental protocol, and that massive outbreaks only occurred in a specific community type. In summary, we here describe viral outbreaks of (to the best of our knowledge) unparalleled magnitude of a single bacteriophage strain, further uncovering the relevant scales of bacteriophage dynamics in complex communities.