Whole-genome characterization of a Peruvian alpaca rotavirus isolate expressing a novel VP4 genotype
Introduction
Among the South American camelids (SACs), alpacas (Vicugna pacu) and llamas (Llama glama) are domesticated species, whereas vicuñas (Vicugna vicugna) and guanacos (Llama guanicoe) are wild species. A cornerstone of the Andean highland economy is raising alpacas for meat and fiber. Peru has the largest alpaca herd in the world (4–4.5 million alpacas) (Tuckwell, 1994), producing an average of approximately 3.5 million kilograms of alpaca fiber annually (∼90% of the total worldwide production) (Rosadio et al., 2012). Infections, particularly diarrheal infections, caused by various pathogens are a major cause of neonatal death for SACs (Cebra et al., 2003, Whitehead, 2009, Lopez et al., 2011). Previous studies have demonstrated the importance of rotavirus infections among these animals (Parreño et al., 2001, Parreño et al., 2004, Lopez et al., 2011, Papp et al., 2012, Rosadio et al., 2012, Badaracco et al., 2013, Garmendia et al., 2015).
Whole-genome rotavirus sequences in SACs are available for only two strains isolated from a guanaco (Matthijnssens et al., 2009). Partial genome characterization is available for one strain from a vicuña and two strains from alpacas; however, only one or two of the 11 genome segments have been sequenced for the alpaca Rotavirus A (RVA) isolates (Badaracco et al., 2013, Garmendia et al., 2015). Here, we report the complete genome sequence of rotavirus strain RVA/Alpaca-tc/PER/SA44/2014/G3P[40] and describe a novel VP4 genotype.
Rotaviruses are members of the Rotavirus genus of the Reoviridae family, and are classified into eight species (A-H) (Matthijnssens et al., 2012a). RVA is a major cause of dehydrating diarrhea in humans and animals worldwide (Santos and Hoshino, 2005). The RVA genome consists of 11 segments of double-stranded RNA (dsRNA) encoding six structural proteins (VP1-4, VP6, and VP7) and six nonstructural proteins (NSP1-6) (Estes and Greenberg, 2013). The RVA genomic classification nomenclature is based on all 11 segments of dsRNA. The notation Gx-P[x]-Ix-Rx-Cx-Mx-Ax-Nx-Tx-Ex-Hx is used to represent genotypes of the VP7-VP4-VP6-VP1-VP2-VP3-NSP1-NSP2-NSP3-NSP4-NSP5/6–encoding gene segments, respectively, with x indicating the number of the genotype (Matthijnssens et al., 2008, Matthijnssens et al., 2011a). Currently, there are 28 G, 39 P, 21 I, 14 R, 14C, 13 M, 24 A, 14 N, 16 T, 21 E, and 16 H genotypes (https://rega.kuleuven.be/cev/viralmetagenomics/virus-classification/minutes-of-the-7th-rcwg-meeting).
Section snippets
Stool samples and RT-PCR detection of RV
The RVA strain described in this study (SA44) was isolated from a stool sample collected in February 2014 from a neonatal diarrheic alpaca belonging to the herd of Silli. This community is located in the southern highlands of Peru (14°24′45.3′′s, 71°11′32.6′′ W; ∼4000 m ASL) in the province of Canchis in the state of Cusco. The importation of alpacas stool samples was approved by the Brazilian Institute of Environment (IBAMA; Brasília, DF, Brazil) license in 14BR012948/DF 02/20/2014.
The stool
Virus isolation
The RVA strain was successfully propagated in MA-104 cells, as confirmed by the presence of RV particles by TEM (Fig. 1). PAGE analysis of the genome demonstrated a typical (4:2:3:2) RVA electropherotype (data not shown).
Phylogenetic analyses
Sequences generated for all 11 genome segments of alpaca strain SA44 were deposited into GenBank under accession numbers KT935476-KT935485 and KU168341. Comparison of the SA44 sequence with sequences of known RVA strains suggested that the genomic makeup of the newly identified
Discussion
Genome sequence comparison analyses have determined that most human RVA strains belong to three defined genotype constellations of the non-G, non-P genes: namely, I1-R1-C1-M1-A1-N1-T1-E1-H1 (Wa-like), I2-R2-C2-M2-A2-N2-T2-E2-H2 (DS-1-like), and I3-R3-C3-M3-A3-N3-T3-E3-H3 (AU-1-like) (Matthijnssens and Van Ranst, 2012). The AU-1-like constellation presumably originated from canine or feline strains and has been occasionally detected in humans and bats (Matthijnssens et al., 2011a, He et al., 2013
Conflicts of interest
No conflicts of interest are declared.
Acknowledgements
This study was supported, in part, by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; Nos. 471063/2012-6 and 303864/2014-1), the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), and the Fundação Carlos Chagas de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ; Nos. E-26/103.113/2011 and E-26/201.374/2014), Brazil. The funders had no role in study design, data collection, data interpretation, or the decision to submit the work for publication.
References (35)
- et al.
Discovery and molecular characterization of a group A rotavirus strain detected in an Argentinean vicuña (Vicugna vicugna)
Vet. Microbiol.
(2013) - et al.
Molecular characterization of rotavirus isolated from alpaca (Vicugna pacos) crias with diarrhea in the Andean Region of Cusco
Peru. Vet. Microbiol.
(2015) - et al.
Novel NSP1 genotype characterised in an African camel G8P[11] rotavirus strain
Infect. Genet. Evol.
(2014) - et al.
Full-length genomic analysis of porcine G9P[23] and G9P[7] rotavirus strains isolated from pigs with diarrhea in South Korea
Infect. Genet. Evol.
(2012) - et al.
Genotype constellation and evolution of group A rotaviruses infecting humans
Curr. Opin. Virol.
(2012) - et al.
Multiple reassortment and interspecies transmission events contribute to the diversity of feline, canine and feline/canine-like human group A rotavirus strains
Infect. Genet. Evol.
(2011) - et al.
Multiple reassortment and interspecies transmission events contribute to the diversity of feline, canine and feline/canine-like human group A rotavirus strains
Infect. Genet. Evol.
(2011) - et al.
Whole-genomic analysis of 12 porcine group A rotaviruses isolated from symptomatic piglets in Brazil during the years of 2012-2013
Infect. Genet. Evol.
(2015) - et al.
Whole genome sequence and phylogenetic analyses reveal human rotavirus G3P[3] strains Ro1845 and HCR3A are examples of direct virion transmission of canine/feline rotaviruses to humans
Virology
(2008) Neonatal diseases in llamas and alpacas
Vet. Clin. Food Anim.
(2009)
The complete genome sequence of a G3P[10] Chinese bat rotavirus suggests multiple bat rotavirus inter-host species transmission events
Infect. Genet. Evol.
Potential pathogens in feces from unweaned llamas and alpacas with diarrhea
J. Am. Vet. Med. Assoc.
Unusual assortment of segments in 2 rare human rotavirus genomes
Emerg. Infect. Dis.
Rotaviruses
Characterization of a novel G3P[3] rotavirus isolated from a lesser horseshoe bat: a distant relative of feline/canine rotaviruses
J. Virol.
Rapid diagnosis of rotavirus infection by direct detection of viral nucleic acid in silver-stained polyacrylamide gels
J. Clin. Microbiol.
Molecular characterization of VP6 genes of human rotavirus isolates: correlation of genogroups with subgroups and evidence of independent segregation
J. Virol.
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