Genetic characterization of the marmot gut virome in high-altitude Qinghai Province and identification of novel viruses with zoonotic potential.

Abstract

The high-altitude ecosystems of Qinghai Province, China, harbor unique viral communities shaped by extreme environmental conditions and host adaptations. This study presents a comprehensive genetic characterization of the marmot gut virome, revealing novel viral strains with zoonotic potential. Using viral metagenomics, we analyzed intestinal contents from 70 marmots collected from Chengduo and Maqin counties. Sequencing on the Illumina NovaSeq 6000 platform identified 19 viral genomes belonging to four major families: Adenoviridae, Astroviridae, Parvoviridae, and Picornaviridae, along with four novel circular Rep-encoding single-stranded DNA (CRESS DNA) viruses. Phylogenetic analyses demonstrated close relationships between marmot-derived strains and viruses from humans, bats, and other mammals, highlighting potential cross-species transmission risks. Notably, bat-associated adenoviruses showed closer phylogenetic proximity to human strains, while novel parvoviruses formed a distinct clade within the Dependoparvovirus genus. The discovery of a novel astrovirus with low sequence similarity to known genera underscores the need for taxonomic reclassification. Additionally, a novel picornavirus related to Sapelovirus and four divergent CRESS DNA viruses were identified, expanding our understanding of viral diversity in high-altitude rodents. These findings emphasize the role of marmots as viral reservoirs and highlight the importance of high-altitude ecosystems as hotspots for zoonotic pathogen emergence. This study provides critical insights into viral evolution, host adaptation, and zoonotic risks, advocating for integrated surveillance strategies to mitigate future spillover events.IMPORTANCEViruses are the most abundant and diverse biological entities on Earth, yet their presence in wildlife from extreme environments remains poorly understood. High-altitude ecosystems, shaped by harsh conditions like intense UV radiation and low oxygen levels, create unique settings for virus evolution. This study is the first to comprehensively profile the gut virome of marmots in Qinghai Province, uncovering novel viral strains and highlighting how extreme environments drive viral diversity. Marmots, as key species in these regions, can act as bridges for virus transmission among wildlife, livestock, and humans, posing zoonotic risks. Understanding these viral communities is essential for predicting and preventing future outbreaks. Our findings emphasize the urgent need for integrated, One Health-based surveillance strategies to safeguard both public health and biodiversity in fragile high-altitude ecosystems.