Abstract

The frequent interactions of rodents with humans make them a common source of zoonotic infections. To obtain an initial unbiased measure of the viral diversity in the enteric tract of wild rodents we sequenced partially purified, randomly amplified viral RNA and DNA in the feces of 105 wild rodents (mouse, vole, and rat) collected in California and Virginia. We identified in decreasing frequency sequences related to the mammalian viruses families Circoviridae, Picobirnaviridae, Picornaviridae, Astroviridae, Parvoviridae, Papillomaviridae, Adenoviridae, and Coronaviridae. Seventeen small circular DNA genomes containing one or two replicase genes distantly related to the Circoviridae representing several potentially new viral families were characterized. In the Picornaviridae family two new candidate genera as well as a close genetic relative of the human pathogen Aichi virus were characterized. Fragments of the first mouse sapelovirus and picobirnaviruses were identified and the first murine astrovirus genome was characterized. A mouse papillomavirus genome and fragments of a novel adenovirus and adenovirus-associated virus were also sequenced. The next largest fraction of the rodent fecal virome was related to insect viruses of the Densoviridae, Iridoviridae, Polydnaviridae, Dicistroviriade, Bromoviridae, and Virgaviridae families followed by plant virus-related sequences in the Nanoviridae, Geminiviridae, Phycodnaviridae, Secoviridae, Partitiviridae, Tymoviridae, Alphaflexiviridae, and Tombusviridae families reflecting the largely insect and plant rodent diet. Phylogenetic analyses of full and partial viral genomes therefore revealed many previously unreported viral species, genera, and families. The close genetic similarities noted between some rodent and human viruses might reflect past zoonoses. This study increases our understanding of the viral diversity in wild rodents and highlights the large number of still uncharacterized viruses in mammals.

Highlights

  • The order Rodentia is the single largest group of mammalian species accounting for 40% of all mammal species [1]

  • The hantavirus pulmonary syndrome (HPS), an infection with an exceptionally high mortality first identified in the southwestern United States, was recognized as a zoonotic viral infection with Sin Nombre virus (SNV) in the Hantavirus genus in the Bunyaviridae family originating from deer mouse (Peromyscus maniculatus) [13]

  • Other members of the Hantavirus genus transmitted from rodents include Hantaan, Dobrava-Belgrade, Seoul, and Puumala viruses, causing hemorrahagic fever with renal syndrome (HFRS) worldwide [25,26,27,28,29,30,31]

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Summary

Introduction

The order Rodentia is the single largest group of mammalian species accounting for 40% of all mammal species [1]. Other members of the Hantavirus genus transmitted from rodents include Hantaan, Dobrava-Belgrade, Seoul, and Puumala viruses, causing hemorrahagic fever with renal syndrome (HFRS) worldwide [25,26,27,28,29,30,31]. Tick-borne encephalitis virus (TBEV) in the Flavivirus genus of the family Flaviviridae can cause fatal encephalitis in humans [41,42,43]. Several rodent species such as voles (Microtus agrestis and Myodes glareolus), field mice (Apodemus agrarius) are natural hosts of ticks that cause TBE [43,44]. An acute viral hemorrhagic fever first described in Author Summary

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