Simian Rotaviruses Possess Divergent Gene Constellations That Originated from Interspecies Transmission and Reassortment

Abstract

Group A rotaviruses (RVs) are a major cause of acute dehydrating diarrhea in infants and children under the age of 5 years worldwide. These infections lead to approximately 527,000 deaths each year, the vast majority occurring in developing countries (33). RVs are also responsible for gastroenteritis in many other animal species, notably mammals and birds (16,38). RVs are members of the family Reoviridae and possess a genome consisting of 11 segments of double-stranded RNA (dsRNA). The prototypic genome of a group A RV encodes six structural proteins (VP) and six nonstructural proteins (NSP) (5). The mature RV virion is a nonenveloped triple-layered icosahedral particle. The inner most protein layer is formed by the core lattice protein VP2.Attached to the interior surface of the VP2 layer near the fivefold axes are complexes of the viral RNA-dependent RNA polymerase VP1 and the RNA capping enzyme VP3. Collectively, VP1, VP2, VP3, and the dsRNA genome form the core of the virion (5, 11). The core is surrounded by VP6, the sole constituent of the intermediate protein layer of the virion. The antigenic properties of VP6 are used in classifying RV isolates into groups. The outer protein layer of the virion is composed of trimers of the VP7 glycoprotein penetrated by spikes of the VP4 attachment protein (50). The properties of VP7 and VP4 form the basis of a dual classification system defining RV G types (glycosylated) and P types (protease sensitive), respectively. At present, 23 G genotypes and 31 P genotypes have been recognized in the literature based on sequence analyses (17,39,42,45,47). Recently, a comprehensive sequence-based classification system was established for the RVs which, together with a uniform nomenclature, allows each genome segment of the virus to be assigned to a particular genotype. In the comprehensive classification system, the acronym Gx-P[x]-Ix-Rx-Cx-Mx-AxNx-Tx-Ex-Hx defines the genotypes of VP7-VP4-VP6-VP1-VP2-VP3-NSP1-NSP2-NSP3-NSP4-NSP5 encoding genome segments (17, 18).

Full genome characterization of the first G3P[24] rotavirus strain detected in humans provides evidence of interspecies reassortment and mutational saturation in the VP7 gene

“…Worldwide, the majority of human RVA strains possess either the Wa-like genogroup 1 constellation (I1-R1-C1-M1-A1-N1-T1-E1-H1) or the DS-1-like genogroup 2 constellation (I2-R2-C2-M2-A2-N2-T2-E2-H2) that are believed to have a common origin with the porcine and the bovine RVAs, respectively (Matthijnssens et al , 2008). A smaller group of RVA strains have the AU-1-like genogroup 3 constellation (I3-R3-C3-M3-A3-N3-T3-E3-H3) that is believed to have originated from feline RVAs (Matthijnssens et al , 2008, 2010). Currently, genotypes are assigned based on percentage nucleotide identity of at least 50 % length of the ORF.…”

The complete genome sequence of a G3P[10] Chinese bat rotavirus suggests multiple bat rotavirus inter-host species transmission events

“…A uniform classification system exists for each of the 11 RVA gene segments (VP7, VP4, VP6, VP1-VP3, NSP1-NSP5) defining G-, P-, I-R-, C-, M-, A-, N-, T-, E-and H-genotypes, respectively (Matthijnssens et al, 2008). Despite this seemingly close host range restriction, RVA strains are known to frequently cross the host species barrier, resulting in the detection of RVA strains unusual to that host species (Matthijnssens et al, 2010;Mino et al, 2013;Khamrin et al, 2009). Often, but not always, such inter-host species transmissions are dead-end infections.…”

Whole genome characterization of new bovine rotavirus G21P[29] and G24P[33] strains provides evidence for interspecies transmission

“…For example, Matthijnssens et al (2008a) demonstrated that Wa-like human rotaviruses and porcine rotaviruses have a common origin and that DS-1-like human rotaviruses and bovine rotaviruses have a common origin. More recently, determination of the complete genome sequences of simian rotaviruses indicated that simian rotaviruses are of diverse ancestry that originated largely by interspecies transmission and reassortment with non-human animal rotaviruses (Matthijnssens et al, 2010b). Furthermore, several studies have provided evidence for naturally occurring reassortants between humans and animals by analysis of whole genomes of rotavirus strains (Bányai et al, 2009;Esona et al, 2009;Ghosh et al, 2010;Matthijnssens et al, 2008cMatthijnssens et al, , 2009Matthijnssens et al, , 2010aMukherjee et al, 2009;Tsugawa & Hoshino, 2008).…”