Full Genomic Analysis of Human Rotavirus Strain B4106 and Lapine Rotavirus Strain 30/96 Provides Evidence for Interspecies Transmission

Abstract

The Belgian rotavirus strain B4106, isolated from a child with gastroenteritis, was previously found to have VP7 (G3), VP4 (P[14]), and NSP4 (A genotype) genes closely related to those of lapine rotaviruses, suggesting a possible lapine origin or natural reassortment of strain B4106. To investigate the origin of this unusual strain, the gene sequences encoding VP1, VP2, VP3, VP6, NSP1, NSP2, NSP3, and NSP5/6 were also determined. To allow comparison to a lapine strain, the 11 double-stranded RNA segments of a European G3P[14] rabbit rotavirus strain 30/96 were also determined. The complete genome similarity between strains B4106 and 30/96 was 93.4% at the nucleotide level and 96.9% at the amino acid level. All 11 genome segments of strain B4106 were closely related to those of lapine rotaviruses and clustered with the lapine strains in phylogenetic analyses. In addition, sequence analyses of the NSP5 gene of strain B4106 revealed that the altered electrophoretic mobility of NSP5, resulting in a super-short pattern, was due to a gene rearrangement (head-to-tail partial duplication, combined with two short insertions and a deletion). Altogether, these findings confirm that a rotavirus strain with an entirely lapine genome complement was able to infect and cause severe disease in a human child.Group A rotaviruses (family Reoviridae) are important enteropathogens of humans and of a large variety of mammals and birds (11, 37). The rotavirus genome consists of 11 segments of double-stranded RNA (dsRNA) encoding six structural viral proteins (VP) and six nonstructural proteins (NSP) (37). A mature infectious rotavirus particle is composed of three concentric layers, consisting of a protein core, an inner protein capsid, and an outer protein capsid (84). The outer protein layer consists of VP4 and VP7, the two independent neutralization antigens of the virus, defining 26 P (proteasesensitive) and 15 G (glycoprotein) types, respectively (37,55,68,69,85). The G and P types are peculiarly distributed across the various animal species (88), suggesting host species barriers and restriction, although a number of unusual G and P types, regarded as animal-like strains, have been identified in humans in different parts of the world (85, 88).Although rotaviruses infect particular species preferentially for which they have been defined as the homologous strains, heterologous rotavirus infections occur in both natural and experimental circumstances. Studies in the rabbit and mouse models have demonstrated that only homologous virus strains replicate efficiently and spread horizontally (21,38,44). Based on a Jennerian approach, animal strains that are naturally attenuated in humans have been exploited for the construction of candidate rotavirus vaccines for humans. In a number of field trials with such candidate rotavirus vaccines, the rhesus rotavirus (RRV) strain MMU18006 and the bovine strains NCDV, UK, and WC3 were shown to replicate to a lower extent in humans than in their homologous hosts but to induce immune responses (24, 2...

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

“…Recently, a number of new genotypes have been found in humans and animals (Collins et al, 2010; Lamhoujeb et al, 2010;Martella et al, 2006Martella et al, , 2007Matthijnssens et al, 2009Matthijnssens et al, , 2010aMcNeal et al, 2005;Parra et al, 2007;Rahman et al, 2005; Schumann et al, 2009; Solberg et al, 2009;Ursu et al, 2009). However, the genetic background of most strains has remained to be identified.…”

“…Excluding the VP4 and VP7 genotypes, I2-R2-C2-A3/A13-N2-T6/T7-E2-H3, corresponding to VP6, VP1-VP3 and NSP1-NSP5 genotypes, are commonly found in bovine rotaviruses (Matthijnssens et al, 2006. Since most of the gene segments of bovine rotavirus strains are clustered together within the same corresponding genotypes regardless of the geographical origin or time of isolation, it is thought that these are typical gene segments of bovine rotaviruses.…”

“…They elicit neutralizing antibodies independently. In a dual classification system, rotaviruses are classified into 24 G genotypes and 32 P genotypes based on the nucleotide sequences of VP7 and VP4 genes, respectively (Collins et al, 2010; Esona et al, 2010;Matthijnssens et al, 2006Matthijnssens et al, , 2008a Schumann et al, 2009; Solberg et al, 2009;Ursu et al, 2009). Recently, a new classification system has been established using nucleotide sequences of all of the 11 genomic RNA segments by the Rotavirus Classification Working Group (RCWG) (Matthijnssens et al, 2008b).…”

“…In this study, we determined the complete ORF sequences of AzuK-1 and Dai-10 strains and investigated the evolutionary relationships among the two strains and other rotaviruses. (Table 1), the possibility of involvement of some gene segments other than VP4 and VP7 in efficiency of transmission cannot be excluded.Excluding the VP4 and VP7 genotypes, I2-R2-C2-A3/A13-N2-T6/T7-E2-H3, corresponding to VP6, VP1-VP3 and NSP1-NSP5 genotypes, are commonly found in bovine rotaviruses (Matthijnssens et al, 2006. Since most of the gene segments of bovine rotavirus strains are clustered together within the same corresponding genotypes regardless of the geographical origin or time of isolation, it is thought that these are typical gene segments of bovine rotaviruses.…”

Human, porcine and bovine rotaviruses in Slovenia: evidence of interspecies transmission and genome reassortment

“…Evidence exists to show that zoonotic transmission and reassortment of animal rotaviruses occurs. Zoonotic rotavirus strains are capable of causing not only asymptomatic infection but also mild to severe diarrhoea in humans (Gentsch et al, 2005;Ghosh et al, 2007;Khamrin et al, 2006;Mascarenhas et al, 2007;Matthijnssens et al, 2006b;Palombo, 2002;Varghese et al, 2004).…”