Discovery of a Highly Divergent Coronavirus in the Asian House Shrew from China Illuminates the Origin of the Alphacoronaviruses

Abstract

Although shrews are one of the largest groups of mammals little is known about their role in the evolution and transmission of viral pathogens including coronaviruses. We captured 266 Asian house shrews () in Jiangxi and Zhejiang provinces, China, during 2013-2015. Coronavirus (CoV) RNA was detected in 24 Asian house shrews, with an overall prevalence of 9.02%. Complete viral genome sequences were successfully recovered from the RNA positive samples. The newly discovered shrew CoV fell into four lineages reflecting their geographic origins, indicative of largely allopatric evolution. Notably, these viruses were most closely related to alphacoronaviruses, but sufficiently divergent that they should be considered a novel member of the genus , which we denote Wénchéng shrew virus (WESV). Phylogenetic analysis revealed that WESV was a highly divergent member of the alphacoronaviruses and, more dramatically, that the S gene of WESV fell in a cluster that was genetically distinct from that of known coronaviruses. The divergent position of WESV suggests that coronaviruses have a long association with Asian house shrews. In addition, the genome of WESV contains a distinct NS7 gene that exhibits no sequence similarity to any known viruses. Together, these data suggest that shrews are natural reservoirs for coronaviruses and may have played an important and long-term role in CoV evolution. The subfamily contains several notorious human and animal pathogens, including severe acute respiratory syndrome coronavirus, Middle East respiratory syndrome coronavirus, and porcine epidemic diarrhea virus. Because of their genetic diversity and phylogenetic relationships it has been proposed that the alphacoronaviruses likely have their ultimate ancestry in those viruses residing in bats. Here, we described a novel alphacoronavirus (Wénchéng shrew virus, WESV) that was sampled from Asian house shrews in China. Notably, WESV is a highly divergent member of the alphacoronaviruses and possesses an S gene that is genetically distinct from that of all known coronaviruses. In addition, the genome of WESV contains a distinct NS7 gene that exhibits no sequence similarity to any known viruses. Together, these data suggest that shrews are important and long-standing hosts for coronaviruses that merit additional research and surveillance.

Extensive diversity and evolution of hepadnaviruses in bats in China

“…We surveyed 462 rodents from 8 species and 148 Asian house shrews from Zhejiang province. Although our previous studies have demonstrated the extensive diversity of a broad range of viruses (arenaviruses, coronaviruses, hantaviruses, rotaviruses) in rodents and shrews from Longquan and Wenzhou in Zhejiang province (Li et al, , 2016Wang et al, 2015, 2017bLin et al, 2012, no hepadnavirus was identified in these small mammals, even though these viruses are presentin the bats sampled from the same location (i.e. Longquan).…”

Hosts and Sources of Endemic Human Coronaviruses

“…The 450 species in the order suggest a smaller genetic diversity as compared to the orders Rodentia and Chiroptera with 2269 and 1241 species, respectively. Nevertheless, surprisingly diverse alpha-and betacoronaviruses were detected in Eulipotyphla, including viruses clustering with important CoV clades such as MERS-CoV (Corman et al, 2014c;Tsoleridis et al, 2016;Wang et al, 2017). Other CoVs in shrews and hedgehogs are genetically equidistant and represent relatively deep lineages in the phylogenetic tree.…”

Characterization of a novel bat-HKU2-like swine enteric alphacoronavirus (SeACoV) infection in cultured cells and development of a SeACoV infectious clone

“…SeACoV shared 95% nucleotide (nt) sequence identity with the bat CoV HKU2 strains and 96-98% nt identity with the HKU2-derived bat SADSrelated coronavirus (SADSr-CoV) strains at the complete genome level Zhou et al, 2018). Interestingly, SeACoV and other HKU2-related α-CoVs possess the unique S genes closely related to the betacoronavirus (β-CoV), in a manner similar to those by rodent and Asian house shrew α-CoVs (Tsoleridis et al, 2019;Wang et al, 2015Wang et al, , 2017b, suggesting the occurrence of ancient recombination events https://doi.org/10.1016/j.virol.2019.08.006 Received 30 May 2019; Received in revised form 8 August 2019; Accepted 8 August 2019 between α-CoV and β-CoV (Lau et al, 2007;Pan et al, 2017).…”