Spatial heterogeneity of viral communities across the gastrointestinal tracts of ruminants

Abstract Background: The gastrointestinal tract (GIT) microbiome of ruminants significantly influences their nutrition metabolism and health. Current understanding is extensive for bacterial and archaeal communities, but limited for viral communities within the GIT. Results: We created the Ruminant Gastrointestinal Virome Catalogue (RGVC), which includes 43,981 non-redundant viral Operational Taxonomic Units (vOTUs), with 89.3% newly identified, derived from 370 samples across 10 GIT regions in seven ruminant species. The composition of viral communities is mainly influenced by the GIT regions rather than by the ruminant species. We identified 4,603 putative prokaryotic hosts across 31 bacterial and three archaeal classes for 5,954 viruses, along with significant variations across GIT regions and a strong correlation between hosts and their associated viruses. Lysogeny, constituting 45.6% of survival strategies, was more prevalent than the lytic cycle (4.08%), and the abundances of these viruses varied regionally. The lysogenic viruses encoded 1,805 auxiliary metabolic genes (AMGs) that play key roles in carbohydrates, amino acids, and other metabolisms in their hosts. The variation in AMG abundance across regions highlights the distinct viral communities and the varied virus-host interactions within the GIT. Conclusion: This study offers a comprehensive view of the spatial heterogeneity of viral communities in the ruminant GIT and indicates that this diversity is driven by the interaction of lysogenic viruses with their prokaryotic hosts through AMGs. These findings set the stage for future research into the ecological and nutritional impacts of the ruminant virome, with the potential to uncover novel roles and mechanisms in various GIT regions.