1
Comprehensive genetic analysis of the first near-complete genome of bovine coronavirus and partial genome of bovine rotavirus in Türkiye through metagenomics
PDF
PDF_SM

Keywords

Bovine coronavirus
bovine rotavirus
calf diarrhoea
metagenomics
near-complete genome

How to Cite

Aksoy, E., Azkur, A. K., & Miraloglu, İbrahim H. (2024). Comprehensive genetic analysis of the first near-complete genome of bovine coronavirus and partial genome of bovine rotavirus in Türkiye through metagenomics. Veterinaria Italiana, 60(1). https://doi.org/10.12834/VetIt.3372.22817.2

Abstract

Obtaining the complete or near-complete genome sequence of pathogens is becoming increasingly crucial for epidemiology, virology, clinical science and practice. This study aimed to detect viruses and conduct genetic characterization of genomes using metagenomics in order to identify the viral agents responsible for a calf's diarrhoea. The findings showed that bovine coronavirus (BCoV) and bovine rotavirus (BRV) are the primary viral agents responsible for the calf's diarrhoea. The current study successfully obtained the first-ever near-complete genome sequence of a bovine coronavirus (BCoV) from Türkiye. The G+C content was 36.31% and the genetic analysis revealed that the Turkish BCoV strain is closely related to respiratory BCoV strains from France and Ireland, with high nucleotide sequence and amino acid identity and similarity. In the present study, analysis of the S protein of the Turkish BCoV strain revealed the presence of 13 amino acid insertions, one of which was found to be shared with the French respiratory BCoV. The study also identified a BRV strain through metagenomic analysis and detected multiple mutations within the structural and non-structural proteins of the BRV strain, suggesting that the BRV Kirikkale strain may serve as an ancestor for reassortants with interspecies transmission, especially involving rotaviruses that infect rabbits and giraffes.

https://doi.org/10.12834/VetIt.3372.22817.2
PDF
PDF_SM

References

Abi K. mo, Zhang Q., Zhang B., Zhou L., Yue H. & Tang C. 2020. An emerging novel bovine coronavirus with a 4-amino-acid insertion in the receptor-binding domain of the hemagglutinin-esterase gene. Arch Virol, 165, 3011–3015.

Aksoy E. & Azkur A.K. 2023. Genome characterization of a Turkish bovine rotavirus field isolate by shotgun metagenomics. Arch Virol, 168, 159.

Aksoy E., Kara E., Yagci B.B. & Azkur A.K. 2021. Investigation of Bovine Coronavirus and Bovine Rotavirus in Calves with Neonatal Diarrhea in Kırıkkale and Surrounding Provinces. MAKU J Health Sci Inst, 9, 38–46.

Alekseev K.P., Vlasova A.N., Jung K., Hasoksuz M., Zhang X., Halpin R., et al. 2008. Bovine-Like Coronaviruses Isolated from Four Species of Captive Wild Ruminants Are Homologous to Bovine Coronaviruses, Based on Complete Genomic Sequences. J Virol, 82, 12422–12431.

Alkan F., Ozkul A., Oguzoglu T.C., Timurkan M.O., Caliskan E., Martella V., et al. 2010. Distribution of G (VP7) and P (VP4) genotypes of group A bovine rotaviruses from Turkish calves with diarrhea, 1997-2008. Vet Microbiol, 141, 231–237.

Azkur A.K. & Aksoy E. 2018. Prevention of Calf Diseases. Lalahan Hay Araşt Enst Derg , 58, 56–63.

Bahoussi A.N., Shah P.T., Guo Y.Y., Liu Y., Wu C. & Xing L. 2022. Evolutionary adaptation of bovine coronavirus (BCoV): Screening of natural recombinations across the complete genomes. J Basic Microbiol. , 2022. , 10.1002/jobm.202200548.

Bidokhti M.R.M., Tråvén M., Krishna N.K., Munir M., Belák S., Alenius S., et al. 2013. Evolutionary dynamics of bovine coronaviruses: Natural selection pattern of the spike gene implies adaptive evolution of the strains. Journal of General Virology, 94, 2036–2049.

Brian D.A. & Baric R.S. 2005. Coronavirus Genome Structure and Replication. Curr Top Microbiol Immunol, 287, 1-30.

Butt A.M., Nasrullah I. & Tong Y. 2014. Genome-wide analysis of codon usage and influencing factors in chikungunya viruses. PLoS One, 9.

Castells M., Victoria M., Colina R., Musto H. & Cristina J. 2017. Genome-wide analysis of codon usage bias in Bovine Coronavirus. Virol J, 14.

Choga W.T., Letsholo S.L., Marobela-Raborokgwe C., Gobe I., Mazwiduma M., Maruapula D., et al. 2023. Near-complete genome of SARS-CoV-2 Delta variant of concern identified in a symptomatic dog (Canis lupus familiaris) in Botswana. Vet Med Sci, 9.

Chouljenko V.N., Kousoulas K.G., Lin X. & Storz J. 1998. Nucleotide and Predicted Amino Acid Sequences of All Genes Encoded by the 3 H Genomic Portion (9.5 kb) of Respiratory Bovine Coronaviruses and Comparisons Among Respiratory and Enteric Coronaviruses. Virus Genes, 17, 33–42.

Datamonkey Adaptive Evolution Server. 2023. (https://www.datamonkey.org/ accessed on 3 July 2023).

David E. dos S., Fonseca E. da C., de Carvalho J.F.N., Marinho R. dos S.S., Duro R.L.S., Komninakis S.V., et al. 2022. Metagenomics applied to the detection of diarrhea viruses in humans: Systematic Review. Acta Trop, 227.

Delport W., Poon A.F.Y., Frost S.D.W. & Kosakovsky Pond S.L. 2010. Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics, 26, 2455–2457.

EMBOSS: cusp. 2023. (https://emboss.bioinformatics.nl/cgi-bin/emboss/cusp accessed on 20 June 2023).

Franzo G., Drigo M., Legnardi M., Grassi L., Pasotto D., Menandro M.L., et al. 2020. Bovine Coronavirus: Variability, Evolution, and Dispersal Patterns of a No Longer Neglected Betacoronavirus. Viruses, 12.

Fritzen J.T.T., Oliveira M. V., Lorenzetti E., Alfieri A.F. & Alfieri A.A. 2020. Genotype constellation of a rotavirus A field strain with an uncommon G8P[11] genotype combination in a rotavirus-vaccinated dairy cattle herd. Arch Virol, 165, 1855–1861.

Fukuda Y., Araki K., Hara M., Yamashita Y., Adachi S., Honjo S., et al. 2023. Sequence analysis of a feline- and porcine-origin G3P[9] rotavirus A strain in a child with acute gastroenteritis in Japan. Arch Virol, 168, 45.

Gauthier N.P.G., Nelson C., Bonsall M.B., Locher K., Charles M., MacDonald C., et al. 2021. Nanopore metagenomic sequencing for detection and characterization of SARS-CoV-2 in clinical samples. PLoS One, 16.

Gélinas AM, Boutin M, Sasseville AM & Dea S. 2001. Bovine coronaviruses associated with enteric and respiratory diseases in Canadian dairy cattle display different reactivities to anti-HE monoclonal antibodies and distinct amino acid changes in their HE, S and ns4.9 protein. Virus Res, 76, 43–57.

Ghosh S., Taniguchi K., Aida S., Ganesh B. & Kobayashi N. 2013. Whole genomic analyses of equine group A rotaviruses from Japan: Evidence for bovine-to-equine interspecies transmission and reassortment events. Vet Microbiol, 166, 474–485.

Hasoksuz M., Sreevatsan S., Cho K.-O., Hoet A.E., Saif Linda J & Saif L J. 2002. Molecular analysis of the S1 subunit of the spike glycoprotein of respiratory and enteric bovine coronavirus isolates. Virus Res, 84, 101–109.

ICTV. 2021. Virus Taxonomy: 2021 Release. . (https://ictv.global/taxonomy accessed on 14 February 2023).

Karayel I., Fehér E., Marton S., Coskun N., Bányai K. & Alkan F. 2017. Putative vaccine breakthrough event associated with heterotypic rotavirus infection in newborn calves, Turkey, 2015. Vet Microbiol, 201, 7–13.

Karayel-Hacioglu I., Timurkan M.O., Pellegrini F., Marton S., Gul B., Bányai K., et al. 2022. Whole-genome analysis of a rare G15P group A rotavirus detected at a dairy cattle farm. Journal of General Virology, 103, 001808.

Kim J.H., Jang J.H., Yoon S.W., Noh J.Y., Ahn M.J., Kim Y., et al. 2018. Detection of bovine coronavirus in nasal swab of non-captive wild water deer, Korea. Transbound Emerg Dis, 65, 627–631.

Komoto S., Adah M.I., Ide T., Yoshikawa T. & Taniguchi K. 2016. Whole genomic analysis of human and bovine G8P rotavirus strains isolated in Nigeria provides evidence for direct bovine-to-human interspecies transmission. Infection, Genetics and Evolution, 43, 424–433.

Kosakovsky Pond S.L. & Frost S.D.W. 2005. Not so different after all: A comparison of methods for detecting amino acid sites under selection. Mol Biol Evol, 22, 1208–1222.

Lestari F.B., Chandranoi K., Chuchaona W., Vongpunsawad S. & Poovorawan Y. 2023. A G3P rotavirus strain with an unusual genome constellation in a diarrheic cat in Thailand. Arch Virol, 168, 24.

Lizarazo E., Couto N., Vincenti-Gonzalez M., Raangs E.C., Velasco Z., Bethencourt S., et al. 2019. Applied shotgun metagenomics approach for the genetic characterization of dengue viruses. J Biotechnol, 306S, 100009.

Lorenz I., Fagan J. & More S.J. 2011. Calf health from birth to weaning. II. Management of diarrhoea in pre-weaned calves. Ir Vet J, 64, 9.

Martella V., Bányai K., Matthijnssens J., Buonavoglia C. & Ciarlet M. 2010. Zoonotic aspects of rotaviruses. Vet Microbiol, 140, 246–255.

Martin D.P., Murrell B., Golden M., Khoosal A. & Muhire B. 2015. RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evol, 1.

Matthijnssens J., Ciarlet M., Heiman E., Arijs I., Delbeke T., McDonald S.M., et al. 2008. 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, 82, 3204–3219.

Matthijnssens J., Ciarlet M., McDonald S.M., Attoui H., Bányai K., Brister J.R., et al. 2011. Uniformity of rotavirus strain nomenclature proposed by the Rotavirus Classification Working Group (RCWG). Arch Virol, 156, 1397–1413.

Murrell B., Moola S., Mabona A., Weighill T., Sheward D., Kosakovsky Pond S.L., et al. 2013. FUBAR: a fast, unconstrained bayesian approximation for inferring selection. Mol Biol Evol, 30, 1196–1205.

O’Shea H., Mulherin E., Matthijnssens J., McCusker M.P., Collins P.J., Cashman O., et al. 2014. Complete genomic sequence analyses of the first group A giraffe rotavirus reveals close evolutionary relationship with rotaviruses infecting other members of the Artiodactyla. Vet Microbiol, 170, 151–156.

Pathak A., Gulati B.R., Maan S., Mor S., Kumar D., Soman R., et al. 2022. Complete Genome Sequencing Reveals Unusual Equine Rotavirus A of Bat Origin from India. J Virol, 96, e0140822.

Schoondermark-van de Ven E., van Ranst M., de Bruin W., van den Hurk P., Zeller M., Matthijnssens J., et al. 2013. Rabbit colony infected with a bovine-like G6P rotavirus strain. Vet Microbiol, 166, 154–164.

SIAS. 2023. SIAS. (http://imed.med.ucm.es/Tools/sias.html accessed on 14 February 2023).

Suzuki T., Otake Y., Uchimoto S., Hasebe A. & Goto Y. 2020. Genomic characterization and phylogenetic classification of bovine coronaviruses through whole genome sequence analysis. Viruses, 12, 183.

Tacharoenmuang R., Komoto S., Guntapong R., Ide T., Singchai P., Upachai S., et al. 2018. Characterization of a G10P rotavirus strain from a diarrheic child in Thailand: Evidence for bovine-to-human zoonotic transmission. Infection, Genetics and Evolution, 63, 43–57.

Timurkan M. 2012. Farklı hayvan türlerinde saptanan rotavirusların VP4, VP6, VP7 ve NSP4 gen bölgelerinin moleküler karakterizasyonu. Ankara Universitesi Saglik Bilimleri Enstitusu.

Tsoleridis T., Chappell J.G., Monchatre-Leroy E., Umhang G., Shi M., Bennett M., et al. 2019. Discovery and prevalence of divergent RNA viruses in European field voles and rabbits. Viruses, 12, 47.

Tsugawa T. & Hoshino Y. 2008. Whole genome sequence and phylogenetic analyses reveal human rotavirus G3P strains Ro1845 and HCR3A are examples of direct virion transmission of canine/feline rotaviruses to humans. Virology, 380, 344–353.

Vlasova A.N. & Saif L.J. 2021. Bovine Coronavirus and the Associated Diseases. Front Vet Sci, 8, 643220.

Workman A.M., McDaneld T.G., Harhay G.P., Das S., Loy J.D. & Hause B.M. 2022. Recent Emergence of Bovine Coronavirus Variants with Mutations in the Hemagglutinin-Esterase Receptor Binding Domain in U.S. Cattle. Viruses, 14, 2125.

Yandle Z., Gonzalez G., Carr M., Matthijnssens J. & De Gascun C. 2023. A viral metagenomic protocol for nanopore sequencing of group A rotavirus. J Virol Methods, 312, 114664.

Zhang X., Hasoksuz M., Spiro D., Halpin R., Wang S., Vlasova A., et al. 2007. Quasispecies of bovine enteric and respiratory coronaviruses based on complete genome sequences and genetic changes after tissue culture adaptation. Virology, 363, 1–10.

Zhang X.M., Herbst W., Kousoulas K.G. & Storz J. 1994. Biological and Genetic Characterization of a Hemagglutinating Coronavirus Isolated From a Diarrhoeic Child. J Med Virol, 44152–161.

Zhu Q., Su M., Li Z., Wang X., Qi S., Zhao F., et al. 2022. Epidemiological survey and genetic diversity of bovine coronavirus in Northeast China. Virus Res, 308, 198632.

Copyright (c) 2024 Emel Aksoy, Ahmet Kursat Azkur, İbrahim Halil Miraloglu