Comparative analysis of rodent and small mammal viromes to better understand the wildlife origin of emerging infectious diseases

Abstract

Background: Rodents represent around 43% of all mammalian species, are widely distributed, and are the natural reservoirs of a diverse group of zoonotic viruses, including hantaviruses, Lassa viruses, and tick-borne encephalitis viruses. Thus, analyzing the viral diversity harbored by rodents could assist efforts to predict and reduce the risk of future emergence of zoonotic viral diseases.

Results: We used next-generation sequencing metagenomic analysis to survey for a range of mammalian viral families in rodents and other small animals of the orders Rodentia, Lagomorpha, and Soricomorpha in China. We sampled 3,055 small animals from 20 provinces and then outlined the spectra of mammalian viruses within these individuals and the basic ecological and genetic characteristics of novel rodent and shrew viruses among the viral spectra. Further analysis revealed that host taxonomy plays a primary role and geographical location plays a secondary role in determining viral diversity. Many viruses were reported for the first time with distinct evolutionary lineages, and viruses related to known human or animal pathogens were identified. Phylogram comparison between viruses and hosts indicated that host shifts commonly happened in many different species during viral evolutionary history.

Conclusions: These results expand our understanding of the viromes of rodents and insectivores in China and suggest that there is high diversity of viruses awaiting discovery in these species in Asia. These findings, combined with our previous bat virome data, greatly increase our knowledge of the viral community in wildlife in a densely populated country in an emerging disease hotspot.

Keywords: Emerging infectious diseases; Rodents; Small mammals; Viral evolution; Virome.

Fig. 1

a Numbers of animal samples from various provinces. The numbers of the 3,055 samples belonging to the 55 species of eight families identified are indicated by a pie chart for each province. The numbers of samples from the 55 species and the provinces and dates of collection are detailed in Additional file 1: Table S1. b The prevalence diagram of each viral family related to province, animal species, and reads number. The X axis represents how many provinces certain viral family presents; the Y axis represents how many animal species certain viral family presents; and the sizes of these circles represent the sizes of reads numbers of viral families. c Heatmap based on the normalized sequence reads of 23 families of mammalian viruses in each pooled sample. The species are listed in the right text column. Location information is provided in the life text column. The names of the mammalian viral families are presented in the top text row. The boxes colored from green to red represent the viral reads, which were normalized by average viral genome size and total sequencing reads in each pool

Fig. 2

a Overview of the diversity and abundance of the identified RNA and DNA viruses classified by viral family and host genus. b Overview of the diversity and abundance of the identified RNA and DNA viruses classified by viral family and geographical distribution. The number of viruses obtained by sample-by-sample PCR screening was normalized by sample size of each host genus (a) or province (b)

Fig. 3

a Phylogenetic tree based on the partial L protein sequences of HVs. b Phylogenetic tree based on the complete L proteins of AreVs. The viruses found in this study are labeled in red font. The evolutionary lineages of involved hosts on the right were drawn based on mt-cyt b from genus to family according to previous reports [, , –70]. The relationships between viruses and their hosts were linked by red lines

Fig. 4

a Phylogenetic tree based on the complete aa sequences of ORF1b of ArteVs. b Phylogenetic tree based on the polyproteins of hepacivirus and PestVs. c Phylogenetic tree based on the complete ORF1 sequences of HEVs. The viruses found in this study are labeled in red font. The evolutionary lineages of involved hosts on the right were drawn based on mt-cyt b from genus to family according to previous reports [, , –70]. The relationships between viruses and their hosts were linked by red lines

Fig. 5

a Phylogenetic tree based on the partial RdRp (NSP12) proteins of CoVs. b Phylogenetic tree based on the complete RNA-dependent RNA polymerase proteins of PicoVs. c Phylogenetic tree based on 387 nucleotides of the partial RdRp gene of AstVs. The viruses found in this study are labeled in red font. The relationships between viruses and their hosts were shown in Additional file 3: Figures S10, S11, and S12

Fig. 6

a Phylogenetic tree based on the complete replicase (Rep) proteins of CVs. b Phylogenetic tree based on the VP1 proteins of members of the subfamily Parvovirinae. The viruses found in this study are labeled in red font. The relationships between viruses and their hosts were shown in Additional file 3: Figures S13 and S14