Active Temperate Phages Linked to Core Bacterial Taxa Dominate the Wheat Phyllosphere Virome

Abstract

The wheat phyllosphere supports diverse microbial communities, yet the viral life-history strategies that enable persistence in this dynamic habitat remain largely unknown. Accordingly, 36 non-amplified double-stranded DNA viromes were analyzed across tissues, years, and continents to test whether temperate phages are the dominant component of the wheat phyllosphere virome. A total of 7,958 viral operational taxonomic units were identified, including 1,211 high-quality or complete genomes, revealing extensive viral novelty. Among 726 active viral operational taxonomic units, the virome was structured around a persistent Danish core comprising 290 core members detected in at least half of the samples, including 13 detected in all Danish samples. Temperate phages disproportionately contributed to this active virome, exhibiting significantly higher prevalence than virulent phages and dominating both relative abundance and per-sample representation. Seven ubiquitous members predicted to infect Erwinia corresponded to previously characterized inducible prophages, consistent with in planta prophage induction as a source of extracellular viral particles. Two of the ubiquitous members also belonged to the genus Sendosyvirus, including one detected in both Danish and United States samples, consistent with stable phage-host associations across environments. More broadly, viral presence-absence structure closely tracked bacterial community composition, and active phages were more frequently predicted to infect prevalent bacterial genera. Together, these findings indicate that the wheat phyllosphere virome is organized around a recurrent set of active temperate phages linked to core bacterial taxa. This pattern supports the hypothesis that lysogeny and recurrent prophage induction contribute to viral persistence and host coupling in the wheat phyllosphere.