Complete Genome Sequencing Reveals Unusual Equine Rotavirus A of Bat Origin from India

Rotaviruses are the most common viral agents associated with foal diarrhea. Between 2014 and 2017, the annual prevalence of rotavirus in diarrheic foals ranged between 18 and 28% in Haryana (India). Whole-genome sequencing of two equine rotavirus A (ERVA) isolates (RVA/Horse-wt/IND/ERV4/2017 and RVA/Horse-wt/IND/ERV6/2017) was carried out to determine the genotypic constellations (GCs) of ERVAs. The GCs of both the isolates were G3-P[3]-I8-R3-C3-M3-A9-N3-T3-E3-H6, a unique combination reported for ERVAs so far. Both the isolates carried VP6 of genotype I8, previously unreported from equines. Upon comparison with RVAs of other species, the GC of both isolates was identical to that of a bat rotavirus strain, MSLH14, isolated from China in 2012. The nucleotide sequences of the genes encoding VP3, NSP2, and NSP3 shared >95.81% identity with bat RVA strains isolated from Africa (Gabon). The genes encoding VP1, VP2, VP7, NSP1, and NSP4 shared 94.82% to 97.12% nucleotide identities with the human strains which have zoonotic links to bats (RCH272 and MS2015-1-0001). The VP6 genes of both strains were distinct and had the highest similarity of only 87.08% with that of CMH222, a human strain of bat origin. The phylogenetic analysis and lineage studies revealed that VP7 of both isolates clustered in a new lineage (lineage X) of the G3 genotype with bat, human, and alpaca strains. Similarly, VP4 clustered in a distinct P[3] lineage. These unusual findings highlight the terra incognita of the genomic diversity of equine rotaviruses and support the need for the surveillance of RVAs in animals and humans with a "one health" approach. IMPORTANCE Rotaviruses are globally prevalent diarrheal pathogens in young animals including foals, piglets, calves, goats, sheep, cats, and dogs along with humans. The genome of rotaviruses consists of 11 segments, which enables them to undergo reshuffling by reassortment of segments from multiple species during mixed infections. In this study, the prevalence of equine rotaviruses was 32.11% in organized equine farms of North India. The complete genome analysis of two ERVA isolates revealed an unusual genomic constellation, which was previously reported only in a bat RVA strain. A segment-wise phylogenetic analysis revealed that most segments of both isolates were highly similar either to bat or to bat-like human rotaviruses. The occurrence of unusual bat-like rotaviruses in equines emphasizes the need of extensive surveillance of complete genomes of both animal and human rotaviruses with a "one health" approach.