Multiple reassortment and interspecies transmission events contribute to the diversity of feline, canine and feline/canine-like human group A rotavirus strains.

Jelle Matthijnssens1 Simona De Grazia Jan Piessens Elisabeth Heylen Mark Zeller Giovanni M Giammanco Krisztián Bányai Canio Buonavoglia Max Ciarlet Vito Martella Marc Van Ranst
Affiliations 1 institutions
  1. Laboratory of Clinical and Epidemiological Virology, Department of Microbiology and Immunology, Rega Institute for Medical Research, University of Leuven, Minderbroedersstraat 10, B-3000 Leuven, Belgium. [email protected]

Abstract

RNA-RNA hybridization assays and complete genome sequence analyses have shown that feline rotavirus (FRV) and canine rotavirus (CRV) strains display at least two distinct genotype constellations (genogroups), represented by the FRV strain RVA/Cat-tc/AUS/Cat97/1984/G3P[3] and the human rotavirus (HRV) strain RVA/Human-tc/JPN/AU-1/1982/G3P3[9], respectively. G3P[3] and G3P[9] strains have been detected sporadically in humans. The complete genomes of two CRV strains (RVA/Dog-tc/ITA/RV198-95/1995/G3P[3] and RVA/Dog-tc/ITA/RV52-96/1996/G3P[3]) and an unusual HRV strain (RVA/Human-tc/ITA/PA260-97/1997/G3P[3]) were determined to further elucidate the complex relationships among FRV, CRV and HRV strains. The CRV strains RV198-95 and RV52-96 were shown to possess a Cat97-like genotype constellation. However, 3 and 5 genes of RV198-95 and RV52-96, respectively, were found in distinct subclusters of the same genotypes, suggesting the occurrence of reassortment events among strains belonging to this FRV/CRV/HRV genogroup. Detailed phylogenetic analyses of the HRV strain PA260-97 showed that (i) 8 genome segments (VP3, VP4, VP6, VP7 and NSP2-5) clustered closely with RV198-95 and/or RV52-96; (ii) 2 genome segments (VP1 and VP2) were more closely related to HRV AU-1; and (iii) 1 genome segment (NSP1) was distantly related to any other established NSP1 genotypes and was ratified as a new NSP1 genotype, A15. These findings suggest that the human strain PA260-97 has a history of zoonotic transmission and is likely a reassortant among FRV/CRV strains from the Cat97 and AU-1-like genogroups. In addition, a potential third BA222-05-like genogroup of FRV and HRV strains should be recognized, consisting of rotavirus strains with a stable genetic genotype constellation of genes also partially related to bovine rotavirus (BRV) and bovine-like rotaviruses. The detailed phylogenetic analysis indicated that three major genotype constellations exist among FRV, CRV and feline/canine-like HRV strains, and that reassortment and interspecies transmission events contribute significantly to their wide genetic diversity.

Supporting text Virus Host Location
Genetic Variation 127 Reassortant Viruses 103 Animals 1948 Cat Diseases 67 Cats 120 Child, Preschool 37 Dog Diseases 65 Dogs 176 Genes, Viral 37 Genotype 137 Humans 1440 Phylogeny 805 Rotavirus 65 Rotavirus Infections 61 Sequence Analysis, DNA 113 Zoonoses 397

Evidence records

4 total
Genomic Evolution
4 records · 2 evidence types
Evidence type
3 records
OVE983
Key finding

Reassortment occurred among FRV, CRV, and HRV genogroup strains, as indicated by mixed genome segments and distinct subclusters in genes of RV198-95 and RV52-96.

Virus
Host
Not specified
Location
Not specified
Supporting text

3 and 5 genes of RV198-95 and RV52-96, respectively, were found in distinct subclusters of the same genotypes, suggesting the occurrence of reassortment events among strains belonging to this FRV/CRV/HRV genogroup.

Event type
reassortment
Genes or segments
3 genes of RV198-95 | 5 genes of RV52-96
OVE986
Key finding

Phylogenetic analyses indicate cross-species transmission of group A rotaviruses between feline and canine hosts contributing to their genetic diversity.

Virus
Host
Location
Not specified
Supporting text

The detailed phylogenetic analysis indicated that three major genotype constellations exist among FRV, CRV and feline/canine-like HRV strains, and that reassortment and interspecies transmission events contribute significantly to their wide genetic diversity.

Event type
reassortment
OVE985
Key finding

Genomic analysis indicates that the human rotavirus strain PA260-97 originated through zoonotic transmission and reassortment with feline and canine rotavirus strains in Italy.

Virus
Host
Location
Supporting text

The complete genomes of two CRV strains (RVA/Dog-tc/ITA/RV198-95/1995/G3P[3] and RVA/Dog-tc/ITA/RV52-96/1996/G3P[3]) and an unusual HRV strain (RVA/Human-tc/ITA/PA260-97/1997/G3P[3]) were determined to further elucidate the complex relationships among FRV, CRV and HRV strains. These findings suggest that the human strain PA260-97 has a history of zoonotic transmission and is likely a reassortant among FRV/CRV strains from the Cat97 and AU-1-like genogroups.

Event type
reassortment
Evidence type
1 records
OVE984
Key finding

Phylogenetic analysis showed that the human rotavirus strain PA260-97 clustered with canine and feline-like strains RV198-95 and RV52-96 for most genome segments, but grouped with the human AU-1 strain for two segments, indicating mixed evolutionary origins.

Virus
Host
Location
Not specified
Supporting text

Detailed phylogenetic analyses of the HRV strain PA260-97 showed that (i) 8 genome segments (VP3, VP4, VP6, VP7 and NSP2-5) clustered closely with RV198-95 and/or RV52-96; (ii) 2 genome segments (VP1 and VP2) were more closely related to HRV AU-1; and (iii) 1 genome segment (NSP1) was distantly related to any other established NSP1 genotypes and was ratified as a new NSP1 genotype, A15. These findings suggest that the human strain PA260-97 has a history of zoonotic transmission and is likely a reassortant among FRV/CRV strains from the Cat97 and AU-1-like genogroups.

Genes or proteins
VP1 | VP2 | VP3 | VP4 | VP6 | VP7 | NSP1 | NSP2 | NSP3 | NSP4 | NSP5
Analysis methods
phylogenetic analysis | complete genome sequence analysis