Rumen DNA virome and its relationship with feed efficiency in dairy cows

Background There are numerous viruses in the rumen that interact with other microorganisms, which play crucial roles in regulating rumen environmental metabolism. However, the knowledge of rumen viruses is limited, and their relationship with production traits (e.g., feed efficiency) has not been reported. In this study, we combined next-generation sequencing (NGS) and HiFi sequencing to investigate the rumen DNA virome and reveal the potential mechanisms of how viruses influence feed efficiency in dairy cows. Results Compared with NGS, HiFi sequencing improved the length, completeness, and resolution of viral operational taxonomic units (vOTUs) obviously. A total of 6,922 vOTUs were recruited, including 4,716 lytic and 1,961 temperate vOTUs. At family level, lytic viruses were mainly composed of Siphoviridae (30.35%) and Schitoviridae (23.93%), while temperate viruses were predominantly Siphoviridae (67.21%). A total of 2,382 auxiliary metabolic genes (AMGs) were annotated, which involved in the pathways of carbon metabolism, nitrogen metabolism, energy metabolism, etc. A total of 2,232 vOTU-hMAG (host metagenome-assembled genome) linkages were predicted, with Firmicutes_A (33.60%) and Bacteroidota (33.24%) being the most common host at phylum level. Differential viruses were detected between high and low feed efficiency groups at the family, genus and species levels ( P  < 0.05). By integrating differential viruses, vOTU-hMAG linkages and AMGs, two pathways have been proposed for how rumen viruses affect feed efficiency in dairy cows: 1) lytic viruses lyse host related to cattle phenotypes, such as vOTU1836 can lyse Ruminococcaceae that have a positive effect on organic acids, and 2) AMG-mediated modulation of host metabolism, for example, GT2 carried by vOTU0897 may enhance the fermentation capacity of Lachnosopraceae to produce more organic acids. Conclusions Overall, we constructed a rumen DNA virome profile of Holstein dairy cows, showing the structural and functional composition of rumen viruses, the roles of AMGs carried by vOTUs and the linkages between vOTUs and their hosts. By integrating the above information, we proposed potential mechanisms through which rumen viruses influence feed efficiency in dairy cows, providing new insights into the regulation of feed digestion and nutrient utilization in dairy cows.