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A Comparison of Bovine Torovirus Strains Based on Partial Membrane Glycoprotein (M) Gene Sequences

Year 2021, Volume: 16 Issue: 2, 141 - 148, 31.10.2021
https://doi.org/10.17094/ataunivbd.849058

Abstract

Bovine torovirus (BoTV), which was recently been separated from bovine coronaviruses, is one of the important causative agents of diarrhea in newborn calves. Although the epidemiological data are limited throughout the world, it has been reported in some countries of the world since the early 80’s. In this study, stool samples (n: 150) were taken from 0-30 days old diarrhoeic calves from Elazig, Sivas, and Malatya provinces and were screened by nested RT-PCR method. In 6% (9/150) of the studied samples, 409 bp partial membrane glycoprotein (M) gene was successfully amplified. Some of the positive samples were further sequenced and the 383 nt length data of nine samples were subjected to bioinformatic analysis. The multiple sequence comparison and phylogenetic analyses together revealed that these novel strains presented close identity to previously reported strains from Turkey. The nucleotide identity of the strains was found between 97.13% and 100%. Furthermore, valine-isoleucine substitution (V→I) at 114th position was detected in Turkish strains only (MN717266; MF687255-60), whereas the same substitution at the 144th position was shared between the Turkish (KF188708-11 and KF188714; MF687255-60; MG957145 and MN717266-67) and some of the Chinese-originated isolates. Moreover, four silent mutations were detected in the novel isolates subjected in this study. As a result, we demonstrated the contribution of BToV in the pathogenesis of calf diarrhea and presented new data concerning on the molecular characteristics and the epidemiology of the bovine toroviruses in Turkey.

Supporting Institution

Sivas Cumhuriyet University Scientific Research Project Foundation (CUBAP)

Project Number

VET-029

Thanks

We thank to Mustafa Ozan Atasoy for contribution on the nucleic acid isolation procedures.

References

  • 1. Li H., Zhang B., Yue H., Tang C., 2020. First detection and genomic characteristics of bovine torovirus in dairy calves in China. Archives Virol 165, 1577-1583.
  • 2. Horzinek MC., Weiss M., Ederveen J., 1987. Toroviridae: a pro-posed new family of enveloped RNA viruses. In “Novel diarrhoea viruses, Ciba Foundation Symposium”, Ed., G Brock and Whelan J, No: 128, 162-174, John Wiley & Sons, Chichester.
  • 3. Weiss M., Steck F., Horzinek MC., 1983. Purification and partial characterization of a new enveloped RNA virus (Berne virus). J Gen Virol, 64, 1849-1858.
  • 4. Snijder EJ., Ederveen J., Spaan WJM., Weiss M., Horzinek MC., 1988. Characterization of Berne virus genomic and Messenger RNAs. J Gen Virol, 69, 2135-2144.
  • 5. Draker R., Roper RL., Petric M., Tellier R., 2006. The complete sequence of the bovine torovirus genome. Virus Res, 115, 56-68.
  • 6. Ito M., Tsuchiaka S., Naoi Y., Otomaru K., Sato M., Masuda T., Haga K., Oka T., Yamasato H., Omatsu T., Sugimura S., Aoki H., Furuya T., Katayama Y., Oba M., Shirai J., Katayama K., Mizutani T., Nagai M., 2016. Whole genome analysis of Japanese bovine toroviruses reveals natural recombination between porcine and bovine toroviruses. Infection, Gen and Evolution, 38, 90-95.
  • 7. Brownlie J., 2017. Coronaviridae. In: “Fenner’s Veterinary Virology”, Ed., MacLachlan J., Dubovi JE., 5th edn., 459–461, Elsevier, New York.
  • 8. Woode GN., Reed DE., Runnels PL., Herrig MA., Hill HT., 1982. Studies with an unclassified virus isolated from diarrheic calves. Vet Microbiol, 7, 221-240.
  • 9. Penrith ML., Gerdes GH., 1992. Breda virus-like particles in pigs in South Africa. J S Afr Vet Assoc, 63, 102.
  • 10. Perez E., Kummeling A., Janssen MM., Jimenez C., Alvarado R., Caballero M., Donado P., Dwinger RH., 1998. Infectious agents associated with diarrhoea of calves in the canton of Tilaran, Costa Rica. Prevent Vet Med, 33, 195-205.
  • 11. Matiz K., Kecskemeti S., Kiss I., Adam Z., Tanyi J., Nagy B., 2002. Torovirus detection in faecal specimens of calves and pigs in Hungary: short communication. Acta Veter Hung 50, 293-296.
  • 12. Hoet AE., Nielsen PR., Hasoksuz M., Thomas C., Wittum TE., Saif LJ., 2003. Detection of bovine torovirus and other enteric pathogens in feces from diarrhea cases in cattle. J Vet Diagnostic Invest, 15, 205-212.
  • 13. Haschek B., Klein D., Benetka V., Herrera C., Sommerfeld-Stur I., Vilcek S., Moestl K., Baumgartner W., 2006. Detection of bovine torovirus in neonatal calf diarrhoea in Lower Austria and Styria (Austria). J Vet Med B, Infect Dis Vet Public Health, 53, 160-165.
  • 14. Ito T., Okada N., Fukuyama S., 2007. Epidemiological analysis of bovine torovirus in Japan. Virus Res, 126, 32-37.
  • 15. Park SJ., Oh EH., Park SI., Kim HH., Jeong YJ., Lim GK., Hyun BH., Cho KO., 2008. Molecular epidemiology of bovine toroviruses circulating in South Korea. Vet Microbiol, 126, 364-371.
  • 16. Dhama K., Pawaiya RVS., Chakraborty S., Tiwari R., Verma AK., 2014. Toroviruses of animals and humans: a review. Asian J Anim Vet Advances, 9, 190-201.
  • 17. Gulacti I., Işidan H., Sozdutmaz I., 2014. Detection of bovine torovirus in fecal specimens from calves with diarrhea in Turkey. Arch Virol, 159, 1623-1627.
  • 18. Aita T., Kuwabara M., Murayama K., Sasagawa Y., Yabe S., Higuchi R., Tamura T., Miyazaki A., Tsunemitsu H., 2012. Characterization of epidemic diarrhea outbreaks associated with bovine torovirus in adult cows. Arch Virol, 157, 423-431.
  • 19. Aydin H., Timurkan MO., Kirmizi GA., 2019. Sequence analysis of Turkish field strains of bovine torovirus shows unique amino acid changes in the partial M gene. Asian Pac J of Trop Biomed, 9, 129-134.
  • 20. Turan T., Isidan H., 2018. The first detection and phylogenetic analysis of bovine astrovirus from diarrheic calves in Turkey. Etlik Vet Mikrobiyol Derg, 29, 104-110.
  • 21. Isidan H., Turan T., Atasoy MO., Sözdutmaz I., Irehan B. 2019. Detection and first molecular characterization of three picornaviruses from diarrheic calves in Turkey. Acta Vet Hung, 67, 463-476.
  • 22. Park SI., Jeong C., Kim HH., Park SH., Park SJ., Hyun BH., Yang DK., Kim SK., Kang MI., Cho KO., 2007. Molecular epidemiology of bovine noroviruses in South Korea. Vet Microbiol, 124, 125-133.
  • 23. Kearse M., Moir R., Wilson A., Stones-Havas S., Cheung M., Sturrock S., Buxton S., Cooper A., Markowitz S., Duran C., Thierer T., Ashton B., Meintjes P., Drummond A., 2012. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647-1649.
  • 24. Nogueira JS., Asano KM., de Souza SP., Brandão PE., Richtzenhain LJ., 2013. First detection and molecular diversity of Brazilian bovine torovirus (BToV) strains from young and adult cattle. Res Vet Sci, 95, 799-801.
  • 25. Liebler EM., Klüver S., Pohlenz J., Koopmans M., 1992. The significance of bredavirus as a diarrhea agent in calf herds in Lower Saxony. Dtsch Tierarztl Wochenschr, 99, 195-200.
  • 26. Shi Z., Wang W., Chen C., Zhang X., Wang J., Xu Z., Lan Y., 2020. First report and genetic characterization of bovine torovirus in diarrhoeic calves in China. BMC Vet Res, 16, 272.
  • 27. Ito T., Okada N., Okawa M., Fukuyama S., Shimizu M., 2009. Detection and characterization of bovine torovirus from the respiratory tract in Japanese cattle. Vet Microbiol, 136, 366-371.
  • 28. Kirisawa R., Takeyama A., Koiwa M., Iwai H., 2007. Detection of bovine torovirus in fecal specimens of calves with diarrhea in japan. J Vet Med Sci 69, 471-476.
  • 29. Lojkic I., Kresic N., Simic I., Bedekovic T., 2015. Detection and molecular characterisation of bovine corona and toroviruses from Croatian cattle. BMC Vet Res, 11, 202.
  • 30. Duckmanton L., Carman S., Nagy E., Petric M., 1998. Detection of bovine torovirus in fecal specimens of calves with diarrhea from ontario farms. J Clin Microbiol, 36, 1266-1270.
  • 31. Alkan F., Ozkul A., Oguzoglu TC., Timurkan MO., Caliskan E., Martella V., Burgu I., 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.
  • 32. Aydın H., Timurkan MO., 2018. Buzağı ishallerinde Coronavirusun nukleoprotein gen ve rotavirusun VP7/VP4 gen bölgelerinin kısmi sekansı ve filogenetik analizi. Atatürk Üniv Vet Bil Derg, 13, 211-218.
  • 33. Alkan F., Timurkan MÖ., Karayel İ., 2015. The molecular characterization and detection of Group A rotavirus from calves with diarrhea in Turkish Republic of Northern Cyprus. Kafkas Üniv Vet Fak Derg, 21, 127-130.
  • 34. Smits SL., Lavazza A., Matiz K., Horzinek MC., Koopmans MP., de Groot RJ., 2003. Phylogenetic and evolutionary relationships among torovirus field variants: evidence for multiple intertypic recombination events. J Virol, 77, 9567-9577.
  • 35. Kuwabara M., Wada K., Maeda Y., Miyazaki A., Tsunemitsu H., 2007. First isolation of cytopathogenic bovine torovirus in cell culture from a calf with diarrhea. Clin Vaccin Immunol, 14, 998-1004.

Bovine Torovirus Suşlarının Kısmi Membran Glikoprotein (M) Gen Dizilerine Göre Karşılaştırılması

Year 2021, Volume: 16 Issue: 2, 141 - 148, 31.10.2021
https://doi.org/10.17094/ataunivbd.849058

Abstract

Bovine torovirus (BoTV), sığır koronavirüslerinden yakın bir zamanda ayrılmış olup yenidoğan buzağıların önemli viral ishal etkenlerinden birisidir. Epidemiyolojik veriler dünya çapında kısıtlı olmakla beraber, bu virüs diğer bazı ülkelerde 80’lerin başından itibaren bildirilmiştir. Bu çalışmada Elazığ, Sivas ve Malatya illerinden 0-30 günlük ishalli buzağılardan alınan dışkı örnekleri (n:150) nested RT-PCR metodu ile tarandı. Çalışılan örneklerin % 6’sında (9/150) 409 bç. kısmi M geni başarılı bir biçimde amplifiye edildi. Pozitif örneklerin bazıları seçilerek sekanslandı ve 9 adet örneğin 383 bazlık sekansı biyoinformatik analizde kullanıldı. Çalışmada GenBank’ta yer alan verilerle birlikte yapılan filogenetik analizler yeni bulunan izolatların da daha önce Türkiye’den bildirilenlerle benzer olduğunu ortaya koymuştur. Dizi analizi yaptırılan izolatların nükleotid benzerliği 97.13% ile 100% arasında bulunmuştur. Valin-izolöysin (V→I) mutasyonu 114. pozisyonda yalnızca Türk suşlarında mevcutken 144. pozisyonda bazı Türk ve Çin suşlarında gözlemlenmiştir. Öte yandan sadece bu çalışmada ortaya çıkarılan yeni Türk izolatlarında 4 adet sessiz mutasyon olduğu ortaya konuldu. Sonuç olarak, ortaya konulan bu bilimsel veriler ile sığır toroviruslarının moleküler karakteristiği ve epidemiyolojisine katkı sağlandı.

Project Number

VET-029

References

  • 1. Li H., Zhang B., Yue H., Tang C., 2020. First detection and genomic characteristics of bovine torovirus in dairy calves in China. Archives Virol 165, 1577-1583.
  • 2. Horzinek MC., Weiss M., Ederveen J., 1987. Toroviridae: a pro-posed new family of enveloped RNA viruses. In “Novel diarrhoea viruses, Ciba Foundation Symposium”, Ed., G Brock and Whelan J, No: 128, 162-174, John Wiley & Sons, Chichester.
  • 3. Weiss M., Steck F., Horzinek MC., 1983. Purification and partial characterization of a new enveloped RNA virus (Berne virus). J Gen Virol, 64, 1849-1858.
  • 4. Snijder EJ., Ederveen J., Spaan WJM., Weiss M., Horzinek MC., 1988. Characterization of Berne virus genomic and Messenger RNAs. J Gen Virol, 69, 2135-2144.
  • 5. Draker R., Roper RL., Petric M., Tellier R., 2006. The complete sequence of the bovine torovirus genome. Virus Res, 115, 56-68.
  • 6. Ito M., Tsuchiaka S., Naoi Y., Otomaru K., Sato M., Masuda T., Haga K., Oka T., Yamasato H., Omatsu T., Sugimura S., Aoki H., Furuya T., Katayama Y., Oba M., Shirai J., Katayama K., Mizutani T., Nagai M., 2016. Whole genome analysis of Japanese bovine toroviruses reveals natural recombination between porcine and bovine toroviruses. Infection, Gen and Evolution, 38, 90-95.
  • 7. Brownlie J., 2017. Coronaviridae. In: “Fenner’s Veterinary Virology”, Ed., MacLachlan J., Dubovi JE., 5th edn., 459–461, Elsevier, New York.
  • 8. Woode GN., Reed DE., Runnels PL., Herrig MA., Hill HT., 1982. Studies with an unclassified virus isolated from diarrheic calves. Vet Microbiol, 7, 221-240.
  • 9. Penrith ML., Gerdes GH., 1992. Breda virus-like particles in pigs in South Africa. J S Afr Vet Assoc, 63, 102.
  • 10. Perez E., Kummeling A., Janssen MM., Jimenez C., Alvarado R., Caballero M., Donado P., Dwinger RH., 1998. Infectious agents associated with diarrhoea of calves in the canton of Tilaran, Costa Rica. Prevent Vet Med, 33, 195-205.
  • 11. Matiz K., Kecskemeti S., Kiss I., Adam Z., Tanyi J., Nagy B., 2002. Torovirus detection in faecal specimens of calves and pigs in Hungary: short communication. Acta Veter Hung 50, 293-296.
  • 12. Hoet AE., Nielsen PR., Hasoksuz M., Thomas C., Wittum TE., Saif LJ., 2003. Detection of bovine torovirus and other enteric pathogens in feces from diarrhea cases in cattle. J Vet Diagnostic Invest, 15, 205-212.
  • 13. Haschek B., Klein D., Benetka V., Herrera C., Sommerfeld-Stur I., Vilcek S., Moestl K., Baumgartner W., 2006. Detection of bovine torovirus in neonatal calf diarrhoea in Lower Austria and Styria (Austria). J Vet Med B, Infect Dis Vet Public Health, 53, 160-165.
  • 14. Ito T., Okada N., Fukuyama S., 2007. Epidemiological analysis of bovine torovirus in Japan. Virus Res, 126, 32-37.
  • 15. Park SJ., Oh EH., Park SI., Kim HH., Jeong YJ., Lim GK., Hyun BH., Cho KO., 2008. Molecular epidemiology of bovine toroviruses circulating in South Korea. Vet Microbiol, 126, 364-371.
  • 16. Dhama K., Pawaiya RVS., Chakraborty S., Tiwari R., Verma AK., 2014. Toroviruses of animals and humans: a review. Asian J Anim Vet Advances, 9, 190-201.
  • 17. Gulacti I., Işidan H., Sozdutmaz I., 2014. Detection of bovine torovirus in fecal specimens from calves with diarrhea in Turkey. Arch Virol, 159, 1623-1627.
  • 18. Aita T., Kuwabara M., Murayama K., Sasagawa Y., Yabe S., Higuchi R., Tamura T., Miyazaki A., Tsunemitsu H., 2012. Characterization of epidemic diarrhea outbreaks associated with bovine torovirus in adult cows. Arch Virol, 157, 423-431.
  • 19. Aydin H., Timurkan MO., Kirmizi GA., 2019. Sequence analysis of Turkish field strains of bovine torovirus shows unique amino acid changes in the partial M gene. Asian Pac J of Trop Biomed, 9, 129-134.
  • 20. Turan T., Isidan H., 2018. The first detection and phylogenetic analysis of bovine astrovirus from diarrheic calves in Turkey. Etlik Vet Mikrobiyol Derg, 29, 104-110.
  • 21. Isidan H., Turan T., Atasoy MO., Sözdutmaz I., Irehan B. 2019. Detection and first molecular characterization of three picornaviruses from diarrheic calves in Turkey. Acta Vet Hung, 67, 463-476.
  • 22. Park SI., Jeong C., Kim HH., Park SH., Park SJ., Hyun BH., Yang DK., Kim SK., Kang MI., Cho KO., 2007. Molecular epidemiology of bovine noroviruses in South Korea. Vet Microbiol, 124, 125-133.
  • 23. Kearse M., Moir R., Wilson A., Stones-Havas S., Cheung M., Sturrock S., Buxton S., Cooper A., Markowitz S., Duran C., Thierer T., Ashton B., Meintjes P., Drummond A., 2012. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647-1649.
  • 24. Nogueira JS., Asano KM., de Souza SP., Brandão PE., Richtzenhain LJ., 2013. First detection and molecular diversity of Brazilian bovine torovirus (BToV) strains from young and adult cattle. Res Vet Sci, 95, 799-801.
  • 25. Liebler EM., Klüver S., Pohlenz J., Koopmans M., 1992. The significance of bredavirus as a diarrhea agent in calf herds in Lower Saxony. Dtsch Tierarztl Wochenschr, 99, 195-200.
  • 26. Shi Z., Wang W., Chen C., Zhang X., Wang J., Xu Z., Lan Y., 2020. First report and genetic characterization of bovine torovirus in diarrhoeic calves in China. BMC Vet Res, 16, 272.
  • 27. Ito T., Okada N., Okawa M., Fukuyama S., Shimizu M., 2009. Detection and characterization of bovine torovirus from the respiratory tract in Japanese cattle. Vet Microbiol, 136, 366-371.
  • 28. Kirisawa R., Takeyama A., Koiwa M., Iwai H., 2007. Detection of bovine torovirus in fecal specimens of calves with diarrhea in japan. J Vet Med Sci 69, 471-476.
  • 29. Lojkic I., Kresic N., Simic I., Bedekovic T., 2015. Detection and molecular characterisation of bovine corona and toroviruses from Croatian cattle. BMC Vet Res, 11, 202.
  • 30. Duckmanton L., Carman S., Nagy E., Petric M., 1998. Detection of bovine torovirus in fecal specimens of calves with diarrhea from ontario farms. J Clin Microbiol, 36, 1266-1270.
  • 31. Alkan F., Ozkul A., Oguzoglu TC., Timurkan MO., Caliskan E., Martella V., Burgu I., 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.
  • 32. Aydın H., Timurkan MO., 2018. Buzağı ishallerinde Coronavirusun nukleoprotein gen ve rotavirusun VP7/VP4 gen bölgelerinin kısmi sekansı ve filogenetik analizi. Atatürk Üniv Vet Bil Derg, 13, 211-218.
  • 33. Alkan F., Timurkan MÖ., Karayel İ., 2015. The molecular characterization and detection of Group A rotavirus from calves with diarrhea in Turkish Republic of Northern Cyprus. Kafkas Üniv Vet Fak Derg, 21, 127-130.
  • 34. Smits SL., Lavazza A., Matiz K., Horzinek MC., Koopmans MP., de Groot RJ., 2003. Phylogenetic and evolutionary relationships among torovirus field variants: evidence for multiple intertypic recombination events. J Virol, 77, 9567-9577.
  • 35. Kuwabara M., Wada K., Maeda Y., Miyazaki A., Tsunemitsu H., 2007. First isolation of cytopathogenic bovine torovirus in cell culture from a calf with diarrhea. Clin Vaccin Immunol, 14, 998-1004.
There are 35 citations in total.

Details

Primary Language English
Subjects Health Care Administration
Journal Section Araştırma Makaleleri
Authors

Turhan Turan 0000-0002-4223-1734

Hakan Işıdan

Project Number VET-029
Publication Date October 31, 2021
Published in Issue Year 2021 Volume: 16 Issue: 2

Cite

APA Turan, T., & Işıdan, H. (2021). A Comparison of Bovine Torovirus Strains Based on Partial Membrane Glycoprotein (M) Gene Sequences. Atatürk Üniversitesi Veteriner Bilimleri Dergisi, 16(2), 141-148. https://doi.org/10.17094/ataunivbd.849058
AMA Turan T, Işıdan H. A Comparison of Bovine Torovirus Strains Based on Partial Membrane Glycoprotein (M) Gene Sequences. Atatürk Üniversitesi Veteriner Bilimleri Dergisi. October 2021;16(2):141-148. doi:10.17094/ataunivbd.849058
Chicago Turan, Turhan, and Hakan Işıdan. “A Comparison of Bovine Torovirus Strains Based on Partial Membrane Glycoprotein (M) Gene Sequences”. Atatürk Üniversitesi Veteriner Bilimleri Dergisi 16, no. 2 (October 2021): 141-48. https://doi.org/10.17094/ataunivbd.849058.
EndNote Turan T, Işıdan H (October 1, 2021) A Comparison of Bovine Torovirus Strains Based on Partial Membrane Glycoprotein (M) Gene Sequences. Atatürk Üniversitesi Veteriner Bilimleri Dergisi 16 2 141–148.
IEEE T. Turan and H. Işıdan, “A Comparison of Bovine Torovirus Strains Based on Partial Membrane Glycoprotein (M) Gene Sequences”, Atatürk Üniversitesi Veteriner Bilimleri Dergisi, vol. 16, no. 2, pp. 141–148, 2021, doi: 10.17094/ataunivbd.849058.
ISNAD Turan, Turhan - Işıdan, Hakan. “A Comparison of Bovine Torovirus Strains Based on Partial Membrane Glycoprotein (M) Gene Sequences”. Atatürk Üniversitesi Veteriner Bilimleri Dergisi 16/2 (October 2021), 141-148. https://doi.org/10.17094/ataunivbd.849058.
JAMA Turan T, Işıdan H. A Comparison of Bovine Torovirus Strains Based on Partial Membrane Glycoprotein (M) Gene Sequences. Atatürk Üniversitesi Veteriner Bilimleri Dergisi. 2021;16:141–148.
MLA Turan, Turhan and Hakan Işıdan. “A Comparison of Bovine Torovirus Strains Based on Partial Membrane Glycoprotein (M) Gene Sequences”. Atatürk Üniversitesi Veteriner Bilimleri Dergisi, vol. 16, no. 2, 2021, pp. 141-8, doi:10.17094/ataunivbd.849058.
Vancouver Turan T, Işıdan H. A Comparison of Bovine Torovirus Strains Based on Partial Membrane Glycoprotein (M) Gene Sequences. Atatürk Üniversitesi Veteriner Bilimleri Dergisi. 2021;16(2):141-8.