Detection and characterization of a novel bat-borne coronavirus in Singapore using multiple molecular approaches Free

Abstract

Bats are important reservoirs and vectors in the transmission of emerging infectious diseases. Many highly pathogenic viruses such as SARS-CoV and rabies-related lyssaviruses have crossed species barriers to infect humans and other animals. In this study we monitored the major roost sites of bats in Singapore, and performed surveillance for zoonotic pathogens in these bats. Screening of guano samples collected during the survey uncovered a bat coronavirus () in , commonly known as the lesser dog-faced fruit bat. Using a capture-enrichment sequencing platform, the full-length genome of the bat CoV was sequenced and found to be closely related to the bat coronavirus HKU9 species found in Leschenault’s rousette discovered in the Guangdong and Yunnan provinces.

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2019-08-16
2024-03-28
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References

  1. (CDC) CfDCaP Update: Outbreak of severe acute respiratory syndrome-worldwide, 2003. MMWR Morbidity and mortality weekly report; 2003241–246
  2. Drosten C, Günther S, Preiser W, van der Werf S, Brodt H-R et al. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N Engl J Med 2003; 348:1967–1976 [View Article]
    [Google Scholar]
  3. Al-Abdallat MM, Payne DC, Alqasrawi S, Rha B, Tohme RA et al. Hospital-Associated outbreak of middle East respiratory syndrome coronavirus: a serologic, epidemiologic, and clinical description. Clin Infect Dis 2014; 59:1225–1233 [View Article]
    [Google Scholar]
  4. Zhou P, Fan H, Lan T, Yang X-L, Shi W-F et al. Fatal swine acute diarrhoea syndrome caused by an HKU2-related coronavirus of bat origin. Nature 2018; 556:255–258 [View Article]
    [Google Scholar]
  5. Bennet N. Alarm bells over MERS coronavirus. Lancet Infect Dis 2013; 13:573–574 [View Article]
    [Google Scholar]
  6. Wang L-F, Anderson DE. Viruses in bats and potential spillover to animals and humans. Curr Opin Virol 2019; 34:79–89 [View Article]
    [Google Scholar]
  7. Stadler K, Masignani V, Eickmann M, Becker S, Abrignani S et al. SARS--beginning to understand a new virus. Nat Rev Microbiol 2003; 1:209–218 [View Article]
    [Google Scholar]
  8. WHO Middle East respiratory syndrome coronavirus (MERS-CoV); 2018
  9. McIntosh K, Becker WB, Chanock RM. Growth in suckling-mouse brain of "IBV-like" viruses from patients with upper respiratory tract disease. Proc Natl Acad Sci USA 1967; 58:2268–2273 [View Article]
    [Google Scholar]
  10. van der Hoek L, Pyrc K, Jebbink MF, Vermeulen-Oost W, Berkhout RJM et al. Identification of a new human coronavirus. Nat Med 2004; 10:368–373 [View Article]
    [Google Scholar]
  11. Vetterlein W, Hesse R. [Electron microscopic picture of viral hepatitis in man and mouse]. Arch Exp Veterinarmed 1965; 19:231–240
    [Google Scholar]
  12. Wang LF, Bats CC. Viruses: A New Frontier of Emerging Infectious Diseases Wiley; 2015
    [Google Scholar]
  13. Hu B, Ge X, Wang L-F, Shi Z. Bat origin of human coronaviruses. Virol J 2015; 12:1 [View Article]
    [Google Scholar]
  14. Childs JE, Gordon ER. Surveillance and control of zoonotic agents prior to disease detection in humans. Mt Sinai J Med 2009; 76:421–428 [View Article]
    [Google Scholar]
  15. Saberi A, Gulyaeva AA, Brubacher JL, Newmark PA, Gorbalenya AE. A planarian nidovirus expands the limits of RNA genome size. PLoS Pathog 2018; 14:e1007314 [View Article]
    [Google Scholar]
  16. Kunz TH, Parsons S. Ecological and Behavioral Methods for the Study of Bats , 2nd ed. Baltimore: Johns Hopkins University Press; 2009 p 920
    [Google Scholar]
  17. Meretsky VJ, Brack V, Carter TC, Clawson R, Currie RR et al. Digital photography improves consistency and accuracy of bat counts in Hibernacula. J Wildl Manage 2010; 74:166–173 [View Article]
    [Google Scholar]
  18. Santhosh SR, Parida MM, Dash PK, Pateriya A, Pattnaik B et al. Development and evaluation of SYBR green I-based one-step real-time RT-PCR assay for detection and quantitation of Japanese encephalitis virus. J Virol Methods 2007; 143:73–80 [View Article]
    [Google Scholar]
  19. Heaton PR, Johnstone P, McElhinney LM, Cowley R, O'Sullivan E et al. Heminested PCR assay for detection of six genotypes of rabies and rabies-related viruses. Journal of clinical microbiology 1997; 35:2762–2766
    [Google Scholar]
  20. Paixão MdosS, Alves-Martin MF, Tenório MdaS, Starke-Buzetti WA, Alves ML et al. Serology, isolation, and molecular detection of leptospira spp. from the tissues and blood of rats captured in a wild animal preservation centre in brazil. Prev Vet Med 2014; 115:69–73 [View Article]
    [Google Scholar]
  21. Johansson P, Yap G, Low H-T, Siew C-C, Kek R et al. Molecular characterization of two hantavirus strains from different rattus species in Singapore. Virol J 2010; 7:15 [View Article]
    [Google Scholar]
  22. Crameri G, Todd S, Grimley S, McEachern JA, Marsh GA et al. Establishment, immortalisation and characterisation of pteropid bat cell lines. PLoS One 2009; 4:e8266 [View Article]
    [Google Scholar]
  23. Jiang H, Lei R, Ding S-W, Zhu S. Skewer: a fast and accurate adapter trimmer for next-generation sequencing paired-end reads. BMC Bioinformatics 2014; 15:182 [View Article]
    [Google Scholar]
  24. Li H, Durbin R. Fast and accurate short read alignment with burrows-Wheeler transform. Bioinformatics 2009; 25:1754–1760 [View Article]
    [Google Scholar]
  25. Wilm A, Aw PPK, Bertrand D, Yeo GHT, Ong SH et al. LoFreq: a sequence-quality aware, ultra-sensitive variant caller for uncovering cell-population heterogeneity from high-throughput sequencing datasets. Nucleic Acids Res 2012; 40:11189–11201 [View Article]
    [Google Scholar]
  26. Price MN, Dehal PS, Arkin AP. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 2009; 26:1641–1650 [View Article]
    [Google Scholar]
  27. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article]
    [Google Scholar]
  28. Parsons T. Ecological and Behavioral Methods for the Study of Bats Baltimore: Johns Hopkins University Press; 2009
    [Google Scholar]
  29. Rajathurai R, Mammals editor. Reptiles and amphibians in the nature reserves of Singapore- diversity, abundance and distribution. Proceedings of the Nature Reserves Survey Seminar 1997
    [Google Scholar]
  30. de Souza Luna LK, Heiser V, Regamey N, Panning M, Drexler JF et al. Generic detection of coronaviruses and differentiation at the prototype strain level by reverse transcription-PCR and nonfluorescent low-density microarray. J Clin Microbiol 2007; 45:1049–1052 [View Article]
    [Google Scholar]
  31. Horie M, Kobayashi Y, Honda T, Fujino K, Akasaka T et al. An RNA-dependent RNA polymerase gene in bat genomes derived from an ancient negative-strand RNA virus. Sci Rep 2016; 6:25873 [View Article]
    [Google Scholar]
  32. Poch O, Blumberg BM, Bougueleret L, Tordo N. Sequence comparison of five polymerases (L proteins) of unsegmented negative-strand RNA viruses: theoretical assignment of functional domains. J Gen Virol 1990; 71:1153–1162 [View Article]
    [Google Scholar]
  33. Xu X, Liu Y, Weiss S, Arnold E, Sarafianos SG et al. Molecular model of SARS coronavirus polymerase: implications for biochemical functions and drug design. Nucleic Acids Res 2003; 31:7117–7130 [View Article]
    [Google Scholar]
  34. Sangumathi Kamaraj U, Tan JH, Ong XM, Pan L, Chawla T et al. Application of a targeted-enrichment methodology for full-genome sequencing of dengue 1-4, chikungunya and Zika viruses directly from patient samples. PLoS neglected tropical diseases 2019
    [Google Scholar]
  35. Briese T, Kapoor A, Mishra N, Jain K, Kumar A et al. Virome capture sequencing enables sensitive viral diagnosis and comprehensive Virome analysis. MBio 2015; 6:e01491–15 [View Article]
    [Google Scholar]
  36. Dung TTN, Duy PT, Sessions OM, Sangumathi UK, Phat VV et al. A universal genome sequencing method for rotavirus A from human fecal samples which identifies segment reassortment and multi-genotype mixed infection. BMC Genomics 2017; 18:324 [View Article]
    [Google Scholar]
  37. Miyazato P, Katsuya H, Fukuda A, Uchiyama Y, Matsuo M et al. Application of targeted enrichment to next-generation sequencing of retroviruses integrated into the host human genome. Sci Rep 2016; 6:28324 [View Article]
    [Google Scholar]
  38. Hussain S, Pan J, Chen Y, Yang Y, Xu J et al. Identification of novel subgenomic RNAs and noncanonical transcription initiation signals of severe acute respiratory syndrome coronavirus. J Virol 2005; 79:5288–5295 [View Article]
    [Google Scholar]
  39. Watanabe S, Masangkay JS, Nagata N, Morikawa S, Mizutani T et al. Bat coronaviruses and experimental infection of bats, the Philippines. Emerg Infect Dis 2010; 16:1217–1223 [View Article]
    [Google Scholar]
  40. Woo PCY, Wang M, Lau SKP, Xu H, Poon RWS et al. Comparative analysis of twelve genomes of three novel group 2C and group 2D coronaviruses reveals unique group and subgroup features. J Virol 2007; 81:1574–1585 [View Article]
    [Google Scholar]
  41. Luo Y, Li B, Jiang R-D, Hu B-J, Luo D-S et al. Longitudinal surveillance of Betacoronaviruses in fruit bats in Yunnan Province, China during 2009-2016. Virol Sin 2018; 33:87–95 [View Article]
    [Google Scholar]
  42. Mendenhall IH, Borthwick S, Neves ES, Low D, Linster M et al. Identification of a lineage D Betacoronavirus in cave nectar bats (Eonycteris spelaea) in Singapore and an overview of lineage D reservoir ecology in Se Asian bats. Transbound Emerg Dis 2017; 64:1790–1800 [View Article]
    [Google Scholar]
  43. World Health Organization A 2015; Who publishes list of top emerging diseases likely to cause major epidemics. www.who.int/medicines/ebola-treatment/WHO-list-of-top-emerging-diseases/en/
  44. Wang LF, Eaton BT, Bats EBT. Bats, civets and the emergence of SARS. Curr Top Microbiol Immunol 2007; 315:325–344
    [Google Scholar]
  45. Hassell JM, Begon M, Ward MJ, Fèvre EM. Urbanization and disease emergence: dynamics at the Wildlife-Livestock-Human interface. Trends Ecol Evol 2017; 32:55–67 [View Article]
    [Google Scholar]
  46. Moratelli R, Calisher CH. Bats and zoonotic viruses: can we confidently link bats with emerging deadly viruses?. Mem Inst Oswaldo Cruz 2015; 110:1–22 [View Article]
    [Google Scholar]
  47. Moureau G, Cook S, Lemey P, Nougairede A, Forrester NL et al. New insights into flavivirus evolution, taxonomy and biogeographic history, extended by analysis of canonical and alternative coding sequences. PLoS One 2015; 10:e0117849-e [View Article]
    [Google Scholar]
  48. Sabir JSM, Lam TT-Y, Ahmed MMM, Li L, Shen Y et al. Co-circulation of three camel coronavirus species and recombination of MERS-CoVs in Saudi Arabia. Science 2016; 351:81–84 [View Article]
    [Google Scholar]
  49. Tao Y, Shi M, Chommanard C, Queen K, Zhang J et al. Surveillance of bat coronaviruses in Kenya identifies relatives of human coronaviruses NL63 and 229E and their recombination history. J Virol 2017; 91: [View Article]
    [Google Scholar]
  50. Xu L, Zhang F, Yang W, Jiang T, Lu G et al. Detection and characterization of diverse alpha- and betacoronaviruses from bats in China. Virol Sin 2016; 31:69–77 [View Article]
    [Google Scholar]
  51. Eco Health Alliance 2015; Predict. https://www.ecohealthalliance.org/program/predict
  52. Global Virome Project 2018; Lowering the risk of harm from future viral outbreaks. http://www.globalviromeproject.org/
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