Virome profiling of long-tailed marmots reveals tissue tropism and cross-species transmission of a diversity of uncharacterized mammalian viruses

Background Anthropogenic land conversion and population encroachment into wildlife habitats are amplifying zoonotic risks through intensified human-livestock-wildlife contacts. As ecologically resilient rodents exhibiting dynamic population fluxes, long-tailed marmots ( Marmota caudata ) are crucial viral reservoirs in Central Asian ecosystems. Their sympatric coexistence with domestic herds creates sustained spillover risks, yet comprehensive virome characterization remains fragmented. This study pioneers a whole-virome profiling strategy to comprehensively characterize the viral diversity of 101 wild M. caudata across five habitats in Xinjiang, addressing critical knowledge gaps in rodent-borne zoonoses under anthropogenic pressures. Results Our study identified 3,314 viral contigs spanning 21 families, with intestinal and lung samples exhibiting the highest viral diversity. Organ-specific tropism was characterized by preferential niches, notably adenoviral predominance in intestinal ecosystems and herpesviral selectivity for lymph node microenvironments. Phylogenetic reconstruction revealed cross-species transmission of rotavirus and ephemerovirus from bovines to marmots, along with identification of 72 novel viruses expanding taxonomic diversity across 17 species and 2 genera. Particularly, two novel coronaviruses showing lung tropism are sufficiently divergent to be new subgenus candidates within the genus Betacoronavirus . Conclusions This comprehensive virome profiling delineates the ecological niches of marmot-associated viruses and identifies a diversity of uncharacterized mammalian viruses, including taxonomically novel lineages and multiple potential zoonotic pathogens requiring prioritized attention. These findings expand our understanding of the circulation dynamics and diverse background of marmot viruses, providing important reference data for developing surveillance frameworks and prevention strategies targeting zoonotic risks associated with this ecologically pivotal species.