Genomic Characterization and Phylogenetic Classification of Bovine Coronaviruses Through Whole Genome Sequence Analysis
<p>Phylogenetic tree constructed using whole genomes of 67 recent bovine coronavirus (BCoV) isolates from Japan and 16 reference BCoV strains from other countries. The tree was constructed using the maximum-likelihood method with the general time reversible nucleotide substitution model implemented in the MEGA X program. Numbers at each branch represent groups with >70% bootstrap support using 1000 replicates. Strain name, host (green): in case of wild ruminant, source: fecal sample (F), nasal swab (N), and unknown (U), year of collection, country, and the GenBank accession number are indicated. Bold text represents the Japanese BCoV isolates used in this study. The scale bar indicates nucleotide substitutions per site.</p> "> Figure 2
<p>Phylogenetic tree constructed using complete sequences of spike glycoproteins from 67 recent BCoV isolates collected from Japan, previously reported BCoV strains collected in the United States, Canada, Sweden, Denmark, Italy, Germany, France, and Korea, and human enteric coronavirus (HCoV-4408). The tree was constructed using the maximum-likelihood method with the general time reversible nucleotide substitution model implemented in the MEGA X program. Numbers at each branch represent groups with >70% bootstrap support using 1000 replicates. Strain name, host (green): in case of wild ruminant, source: fecal sample (F), nasal swab (N), and unknown (U), year of collection, country, and the GenBank accession number are indicated. Bold text represents the Japanese BCoV isolates used in this study. Box represents human enteric coronavirus. The scale bar indicates nucleotide substitutions per site.</p> ">
Abstract
:1. Introduction
2. Materials and Methods
2.1. Samples and Ethics Statement
2.2. RNA Extraction and Sequence Analysis
2.3. Phylogenetic Analysis
3. Results
3.1. Sequence Analysis
3.2. Whole Genome Phylogenetic Analysis
3.3. Phylogenetic Analysis for S Genes
4. Discussion
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Alenius, S.; Niskanen, R.; Juntti, N.; Larsson, B. Bovine coronavirus as the causative agent of winter dysentery: serological evidence. Acta Vet. Scand. 1991, 32, 163–170. [Google Scholar] [PubMed]
- Lathrop, S.L.; Wittum, T.E.; Loerch, S.C.; Perino, L.J.; Saif, L.J. Antibody titers against bovine coronavirus and shedding of the virus via the respiratory tract in feedlot cattle. Am. J. Vet. Res. 2000, 61, 1057–1061. [Google Scholar] [CrossRef] [PubMed]
- Mebus, C.A.; Stair, E.L.; Rhodes, M.B.; Twiehaus, M.J. Neonatal calf diarrhea; propagation, attenuation, and characteristics of coronavirus-like agent. Am. J. Vet. Res. 1973, 34, 145–150. [Google Scholar] [PubMed]
- Saif, L.J.; Brock, K.V.; Redman, D.R.; Kohler, E.M. Winter dysentery in dairy herds: electron microscopic and serological evidence for an association with coronavirus infection. Vet. Rec. 1991, 128, 447–449. [Google Scholar] [CrossRef] [PubMed]
- Storz, J.; Purdy, W.; Lin, X.; Burrell, M.; Truax, R.E.; Briggs, R.E.; Frank, G.H.; Loan, R.W. Isolation of respiratory bovine coronavirus, other cytocidal viruses, and Pasteurella spp. from cattle involved in two natural outbreaks of shipping fever. J. Am. Vet. Med. Assoc. 2000, 216, 1599–1604. [Google Scholar] [CrossRef] [PubMed]
- Clark, M.A. Bovine coronavirus. Br. Vet. J. 1993, 149, 51–70. [Google Scholar] [CrossRef]
- Saif, L.J. Bovine respiratory coronavirus. Vet. Clin. N. Am. Food Anim. Pract. 2010, 26, 349–364. [Google Scholar] [CrossRef]
- Hasoksuz, M.; Lathrop, S.; Al-dubaib, M.A.; Lewis, P.; Saif, L.J. Antigenic variation among bovine coronavirus (BECV) and bovine respiratory coronavirus (BRCV) detected using monoclonal antibodies. Arch. Virol. 1999, 144, 2441–2447. [Google Scholar] [CrossRef]
- Kourtesis, A.B.; Gélinas, A.M.; Dea, S. Genomic and antigenic variation of the HE glycoprotein of bovine coronaviruses associated with neonatal calf diarrhea and winter dysentery. Arch. Virol. 2001, 146, 1219–1230. [Google Scholar] [CrossRef] [Green Version]
- Tsunemitsu, H.; Saif, L.J. Antigenic and biological comparisons of bovine coronaviruses derived from neonatal calf diarrhea and winter dysentery of adult cattle. Arch. Virol. 1995, 140, 1303–1311. [Google Scholar] [CrossRef]
- Cavanagh, D. Nidovirales: A new order copmprising Coronaviridae and Arteriviridae. Arch. Virol. 1997, 142, 629–633. [Google Scholar] [PubMed]
- Abraham, S.; Kienzle, T.E.; Lapps, W.; Brian, D.A. Deduced sequence of the bovine coronavirus spike protein and identification of in the internal proteolytic cleavage site. Virology 1990, 176, 296–301. [Google Scholar] [CrossRef]
- Cavanagh, D.; Davis, P.J.; Pappin, D.J.; Binnis, M.M.; Boursnell, M.E.; Brown, T.D. Coronavirus IBV: partial amino terminal sequencing of spike polypeptide S2 identifies the sequence Arg-Arg-Phe-Arg-Arg at the cleavage site of the spike precursor propoylypeptide of IBV strains Beaudette and M41. Virus Res. 1986, 4, 133–143. [Google Scholar] [CrossRef]
- Godet, M.; Grosclaude, J.; Delemas, B.; Laude, H. Major receptor-binding and neutralization determinants are located within the same domain of the transmissible gastroenteritis virus (coronavirus) spike protein. J. Virol. 1994, 68, 8808–8016. [Google Scholar] [CrossRef] [Green Version]
- Kubo, H.; Yamada, Y.K.; Taguchi, F. Localization of neutralizing epitopes and the receptor-binding site within the amino-terminal 330 amino acids of the murine coronavirus spike protein. J. Virol. 1994, 68, 5403–5410. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schultze, B.; Gross, H.J.; Brossmer, R.; Herrier, G. The S protein of bovine coronavirus is a hemagglutinin recognizing 9-O-acetylated sialic acid as a receptor determinant. J. Virol. 1991, 65, 6232–6237. [Google Scholar] [CrossRef] [Green Version]
- Takase-Yoden, S.; Kikuchi, T.; Siddell, S.G.; Taguchi, F. Localization of major neutralizing epitopes on the S1 polypeptide of the nurine coronavirus peplomer glycoprotein. Virus Res. 1991, 18, 99–107. [Google Scholar]
- Yoo, D.; Deregt, D. A single amino acid change within antigenic domain II of the spike protein of bovine coronavirus confers resistance to virus neutralization. Clin. Diagn. Lab. Immunol. 2001, 8, 297–302. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Luo, Z.; Weiss, S. Roles in cell-to-cell fusion of two conserved hydrophobic regions in the murine coronavirus spike protein. Virology 1998, 244, 483–494. [Google Scholar] [CrossRef] [Green Version]
- Yoo, D.W.; Parker, M.D.; Babiuk, L.A. The S2 subunit of the spike glycoprotein of bovine coronavirus mediates membrane fusion in insect cells. Virology 1991, 180, 395–399. [Google Scholar] [CrossRef]
- Ballesteros, M.L.; Sánchez, C.M.; Enjuanes, L. Two amino acid changes at the N-terminus of transmissible gastroenteritis coronavirus spike protein result in the loss of enteric tropism. Virology 1997, 227, 278–288. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fazakerley, J.K.; Parker, S.E.; Bloom, F.; Buchmeier, M.J. The V5A13.1 envelope glycoprotein deletion mutant of mouse hepatitis virus type-4 is nueroattenuated by its reduced rate of spread in the central nervous system. Virology 1992, 187, 178–188. [Google Scholar] [CrossRef]
- Gallagher, T.M.; Buchmeier, M.J. Coronavirus spike proteins in viral entry and pathogenesis. Virology 2001, 279, 371–374. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hingley, S.T.; Gombold, J.L.; Lavi, E.; Weiss, S.R. MHV-A59 fusion mutants are attenuated and display altered hepatotropism. Virology 1994, 200, 1–10. [Google Scholar] [CrossRef] [PubMed]
- Fulton, R.W.; Step, D.L.; Wahrmund, J.; Burge, L.J.; Payton, M.E.; Cook, B.J.; Burken, D.; Richards, C.J.; Confer, A.W. Bovine coronavirus (BCV) infections in transported commingled beef cattle and sole-source ranch calves. Can. J. Vet. Res. 2011, 75, 11–195. [Google Scholar]
- Jeong, J.H.; Kim, G.Y.; Yoon, S.S.; Park, S.J.; Kim, Y.J.; Sung, C.M.; Shin, S.S.; Lee, B.J.; Kang, M.I.; Park, N.Y.; et al. Molecular analysis of S gene of spike glycoprotein of winter dysentery bovine coronavirus circulating in Korea during 2002–2003. Virus Res. 2005, 108, 207–212. [Google Scholar] [CrossRef]
- Kanno, T.; Hatama, S.; Ishihara, R.; Uchida, I. Molecular analysis of the S glycoprotein gene of bovine coronavirus isolated in Japan from 1999 to 2006. J. Gen. Virol. 2007, 88, 1218–1244. [Google Scholar] [CrossRef]
- Paton, D.J.; Christiansen, K.H.; Alenius, S.; Cranwell, M.P.; Pritchard, G.C.; Drew, T.W. Prevalence of antibodies to bovine virus diarrhoea virus and other viruses in bulk tank milk in England and Wales. Vet. Rec. 1998, 142, 385–391. [Google Scholar] [CrossRef]
- Park, S.J.; Lim, G.K.; Park, S.I.; Kim, H.H.; Koh, H.B.; Cho, K.O. Detection and molecular characterization of calf diarrhoea bovine coronaviruses circulating in South Korea during 2004–2005. Zoonoses Public Health 2007, 54, 223–230. [Google Scholar] [CrossRef]
- Alekseev, K.P.; Valsova, A.N.; Jung, K.; Hosoksuz, M.; Zhang, X.; Halpin, R.; Wang, S.; Ghedin, E.; Spiro, D.; Saif, L.J. Bovine-like coronaviruses isolated from four species of captive wild ruminants are homologous to bovine coronavirus based on complete genomic sequences. J. Virol. 2008, 82, 12422–12431. [Google Scholar] [CrossRef] [Green Version]
- Decaro, N.; Martella, V.; Elia, G.; Campolo, M.; Mari, V.; Desario, C.; Lucente, M.S.; Lorusso, A.; Greco, G.; Corrente, M.; et al. Biological and genetic analysis of a bovine-like coronavirus isolated from water buffalo (Bubalus bubalis) calves. Virology 2008, 370, 213–222. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hasoksuz, M.; Alekseev, K.; Vlasova, A.; Zhang, X.; Spiro, D.; Halpin, R.; Wang, S.; Ghedin, E.; & Saif, L.J. Biologic, antigenic, and full-length genomic characterization of a bovine-like coronavirus isolated from a giraffe. J. Virol. 2007, 81, 4981–4990. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tsunamitsu, H.; el-Kanawati, Z.R.; Smith, D.R.; Reed, H.H.; Saif, L.J. Isolation of coronaviruses antigenically indistinguishable from bovine coronavirus from wild ruminants with diarrhea. J. Clin. Microbiol. 1995, 33, 3264–3269. [Google Scholar] [CrossRef] [Green Version]
- Zhang, X.; Herbst, W.; Kousoulas, K.G.; Storz, J. Biological and genetic characterization of a hemagglutinating coronavirus isolated from a diarrhoeic child. J. Med. Virol. 1994, 44, 152–161. [Google Scholar] [CrossRef]
- Bidokhi, M.R.; Tråvén, M.; Krishna, N.K.; Munir, M.; Belák, S.; Alenius, S.; Cortey, M. Evolutionary dynamics of bovine coronaviruses: natural selection pattern of the spike gene implies adaptive evolution of the strains. J. Gen. Virol. 2013, 94, 2036–2049. [Google Scholar] [CrossRef]
- Chouljenko, V.N.; Kousoulas, K.G.; Lin, X.; Storz, S. Nucleotide and predicted amino acid sequences of all genes encoded by the 3’ genomic portion (9.5Kb) of respiratory bovine coronaviruses and comparisons among respiratory and enteric coronaviruses. Virus Genes 1998, 17, 33–42. [Google Scholar] [CrossRef]
- Liu, L.; Hägglund, S.; Hakhverdyan, M.; Alenius, S.; Larsen, L.E.; Belák, S. Molecular epidemiology of bovine coronavirus on the basis of comparative analyses of the S gene. J. Clin. Microbiol. 2006, 44, 957–960. [Google Scholar] [CrossRef] [Green Version]
- Martínez, N.; Brandão, P.E.; de Souza, S.P.; Barrera, M.; Santana, N.; de Arce, H.D.; Pérez, L.J. Molecular and phylogenetic analysis of bovine coronavirus based on the spike glycoprotein gene. Infect. Genet. Evol. 2012, 12, 1870–1878. [Google Scholar] [CrossRef]
- Rekik, M.R.; Dae, S. Comparative sequence analysis of a polymorphic region of the spike glycoprotein S1 subunit of enteric bovine coronavirus isolates. Arch. Virol. 1994, 135, 319–331. [Google Scholar] [CrossRef]
- Kanno, T.; Kamiyoshi, T.; Ishihara, R.; Hatama, S.; Ushida, I. Phylogenetic studies of bovine coronaviruses isolated in Japan. J. Vet. Med. Sci. 2009, 71, 83–86. [Google Scholar] [CrossRef] [Green Version]
- Kumar, S.; Stecher, G.; Li, M.; Knyaz, C.; Tamura, K. MEGA X: Molecular evolutionary genetic analysis across computing platforms. Mol. Biol. Evol. 2018, 35, 1547–1549. [Google Scholar] [CrossRef] [PubMed]
- Matthijnssens, J.; Ciarlet, M.; Heiman, E.; Arijs, I.; Delbeke, T.; McDonald, S.M.; Palombo, E.A.; Iturriza-Gómara, M.; Maes, P.; Patton, J.T.; et al. Full genome-based classification of rotaviruses reveals a common origin between human Wa-like and porcine rotavirus strains and human DS-1-like and bovine rotavirus strains. J. Virol. 2008, 82, 3204–3219. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Matthijnssens, J.; Ciarlet, M.; Rahman, M.; Attoui, H.; Bányai, K.; Estes, M.K.; Gentsch, J.R.; Iturriza-Gómara, M.; Kirkwood, C.D.; Martella, V.; et al. Recommendations for the classification of group A rotaviruses using all 11 genomic RNA segments. Arch. Virol. 2008, 153, 1621–1629. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Suzuki, T.; Murakami, S.; Takahashi, O.; Kodera, A.; Masuda, T.; Itoh, S.; Miyazaki, A.; Ohashi, S.; Tsutsui, T. Molecular characterization of pig epidemic diarrhoea viruses isolated in Japan from 2013 to 2014. Infect. Genet. Evol. 2015, 36, 363–368. [Google Scholar] [CrossRef]
- Suzuki, T.; Shibahara, T.; Imai, N.; Yamamoto, T.; Ohashi, S. Genetic characterization and pathogenicity of Japanese porcine deltacoronavirus. Infect. Genet. Evol. 2018, 61, 176–182. [Google Scholar] [CrossRef] [PubMed]
- Lai, M.M.; Cavanagh, D. The molecular biology of coronaviruses. Adv. Virus Res. 1997, 48, 1–100. [Google Scholar] [PubMed]
- McBride, R.; van Zyl, M.; Fielding, R. The coronavirus nucleocapsid is a multifunctional protein. Viruses 2014, 6, 2991–3018. [Google Scholar] [CrossRef] [Green Version]
Whole Genome | ORF1 | ORF2 | ORF3 (HE) | ORF4 (S) | ORF5 | ORF6 | ORF7 | ORF8 (E) | ORF9 (M) | ORF10 (N) | |
---|---|---|---|---|---|---|---|---|---|---|---|
Among classical genotypes | 99.7–99.8 | 99.6–99.8 | 99.5–99.6 | 99.7–99.9 | 99.6–99.8 | 100 | 98.4–100 | 99.4–99.7 | 99.2–99.6 | 99.6–100 | 99.6–100 |
Among US wild ruminant genotypes (Among 67 Japanese BCoV isolates) | 98.8–100 (99.0–100) | 99.1–100 (99.1–100) | 97.7–100 (97.7–100) | 98.1–100 (98.5–100) | 98.2–100 (98.4–100) | 87.5–100 (90.5–100) | 91.2–100 (91.2–100) | 97.8–100 (97.8–100) | 97.6–100 (98.0–100) | 98.4–100 (98.7–100) | 98.3–100 (98.3–100) |
Between classical and US wild ruminant genotypes | 98.2–99.2 | 98.4–99.3 | 96.9–98.5 | 96.9–98.6 | 97.4–98.9 | 89.1–98.7 | 85.6–95.8 | 97.5–98.4 | 98.0–100 | 97.9–99.4 | 97.5–99.1 |
Cut-off value | 98.8 | 99.1 | 98.0 | 98.3 | 98.3 | ND | ND | 97.8 | ND | 98.6 | 98.4 |
Geno-Types a | 1 (n = 4) | 2 (n =1) | 3 (n =1) | 4 (n = 26) | 5 (n = 1) | 6 (n = 1) | 7 (n = 6) | 8 (n = 14) | 9 (n = 2) | 10 (n = 4) | 11 (n = 4) | 12 (n = 4) | 13 (n = 20) | 14 (n = 65) |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
1 | 99.6–99.8 | 98.6–98.8 | 98.2–98.5 | 97.9–98.9 | 98.4–98.7 | 98.1–98.3 | 97.6–98.1 | 97.3–98.0 | 97.5–97.8 | 97.6–97.9 | 97.6–98.0 | 97.4–97.7 | 97.6–98.5 | 97.4–98.1 |
2 | 98.8 | 97.9–98.6 | 98.5 | 98.1 | 97.9–98.2 | 97.6–98.0 | 97.8–97.9 | 97.8–97.9 | 97.8–98.1 | 97.6–97.7 | 97.7–98.4 | 97.5–98.0 | ||
3 | 97.7–98.3 | 98.2 | 97.9 | 97.4–97.8 | 97.1–97.6 | 97.3–97.5 | 97.5 | 97.4–97.6 | 97.2–97.3 | 97.3–98.0 | 97.1–97.7 | |||
4 | 98.7–100 | 98.2–98.8 | 98.1–98.7 | 97.7–98.7 | 97.3–98.4 | 97.6–98.2 | 97.7–98.4 | 97.7–98.4 | 97.4–98.1 | 97.9–99.2 | 98.2–99.4 | |||
5 | 99.0 | 98.3–98.7 | 97.9–98.4 | 98.1 | 98.3–98.4 | 98.1–98.4 | 98.0–98.1 | 97.7–98.5 | 97.7–98.2 | |||||
6 | 98.4–98.8 | 97.9–98.4 | 98.1 | 98.5 | 98.1–98.6 | 98.0–98.1 | 97.6–98.3 | 97.6–98.1 | ||||||
7 | 99.0–100 | 98.2–98.9 | 98.4–98.9 | 98.6–99.0 | 98.3–99.1 | 98.1–98.6 | 97.4–98.3 | 97.2–98.1 | ||||||
8 | 98.9–100 | 98.2–98.8 | 98.2–98.8 | 97.9–99.0 | 98.0–98.5 | 97.0–98.1 | 96.9–97.9 | |||||||
9 | 98.7 | 98.4–98.5 | 98.3–98.9 | 98.4–98.6 | 97.3–97.9 | 97.0–97.7 | ||||||||
10 | 100 | 98.6–99.0 | 98.2–98.4 | 97.5–98.2 | 97.2–97.8 | |||||||||
11 | 98.9–99.4 | 98.4–99.2 | 97.3–98.2 | 97.1–97.9 | ||||||||||
12 | 98.8–99.0 | 97.1–97.9 | 97.0–97.6 | |||||||||||
13 | 98.5–99.8 | 97.5–98.6 | ||||||||||||
14 | 98.7–100 |
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Suzuki, T.; Otake, Y.; Uchimoto, S.; Hasebe, A.; Goto, Y. Genomic Characterization and Phylogenetic Classification of Bovine Coronaviruses Through Whole Genome Sequence Analysis. Viruses 2020, 12, 183. https://doi.org/10.3390/v12020183
Suzuki T, Otake Y, Uchimoto S, Hasebe A, Goto Y. Genomic Characterization and Phylogenetic Classification of Bovine Coronaviruses Through Whole Genome Sequence Analysis. Viruses. 2020; 12(2):183. https://doi.org/10.3390/v12020183
Chicago/Turabian StyleSuzuki, Tohru, Yoshihiro Otake, Satoko Uchimoto, Ayako Hasebe, and Yusuke Goto. 2020. "Genomic Characterization and Phylogenetic Classification of Bovine Coronaviruses Through Whole Genome Sequence Analysis" Viruses 12, no. 2: 183. https://doi.org/10.3390/v12020183