1887

Abstract

Bats are important reservoir hosts for emerging viruses, including coronaviruses that cause diseases in people. Although there have been several studies on the pathogenesis of coronaviruses in humans and surrogate animals, there is little information on the interactions of these viruses with their natural bat hosts. We detected a coronavirus in the intestines of 53/174 hibernating little brown bats (Myotis lucifugus), as well as in the lungs of some of these individuals. Interestingly, the presence of the virus was not accompanied by overt inflammation. Viral RNA amplified from little brown bats in this study appeared to be from two distinct clades. The sequences in clade 1 were very similar to the archived sequence derived from little brown bats and the sequences from clade 2 were more closely related to the archived sequence from big brown bats. This suggests that two closely related coronaviruses may circulate in little brown bats. Sequence variation among coronavirus detected from individual bats suggested that infection occurred prior to hibernation, and that the virus persisted for up to 4 months of hibernation in the laboratory. Based on the sequence of its genome, the coronavirus was placed in the Alphacoronavirus genus, along with some human coronaviruses, bat viruses and the porcine epidemic diarrhoea virus. The detection and identification of an apparently persistent coronavirus in a local bat species creates opportunities to understand the dynamics of coronavirus circulation in bat populations.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000898
2017-08-25
2019-10-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/98/9/2297.html?itemId=/content/journal/jgv/10.1099/jgv.0.000898&mimeType=html&fmt=ahah

References

  1. Ge XY, Li JL, Yang XL, Chmura AA, Zhu G et al. Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature 2013;503:535–538 [CrossRef][PubMed]
    [Google Scholar]
  2. Corman VM, Ithete NL, Richards LR, Schoeman MC, Preiser W et al. Rooting the phylogenetic tree of middle East respiratory syndrome coronavirus by characterization of a conspecific virus from an African bat. J Virol 2014;88:11297–11303 [CrossRef][PubMed]
    [Google Scholar]
  3. Ithete NL, Stoffberg S, Corman VM, Cottontail VM, Richards LR et al. Close relative of human Middle East respiratory syndrome coronavirus in bat, South Africa. Emerg Infect Dis 2013;19:1697–1699 [CrossRef][PubMed]
    [Google Scholar]
  4. Memish ZA, Mishra N, Olival KJ, Fagbo SF, Kapoor V et al. Middle East respiratory syndrome coronavirus in bats, Saudi Arabia. Emerg Infect Dis 2013;19:1819–1823 [CrossRef][PubMed]
    [Google Scholar]
  5. Yang Y, du L, Liu C, Wang L, Ma C et al. Receptor usage and cell entry of bat coronavirus HKU4 provide insight into bat-to-human transmission of MERS coronavirus. Proc Natl Acad Sci USA 2014;111:12516–12521 [CrossRef][PubMed]
    [Google Scholar]
  6. WHO 2003; Summary of probable SARS cases with onset of illness from 1 November 2002 to 31 July 2003 World Health Organization. [Based on data as of 31 December 2003]. Available fromwww.who.int/csr/sars/country/table2004_04_21/en/
  7. WHO 2012; WHO updates on MERS World Health Organization. [Since September 2012 until September 6]. Available fromwww.who.int/emergencies/mers-cov/en/
  8. Huang YW, Dickerman AW, Piñeyro P, Li L, Fang L et al. Origin, evolution, and genotyping of emergent porcine epidemic diarrhea virus strains in the United States. MBio 2013;4:e00737-13 [CrossRef][PubMed]
    [Google Scholar]
  9. Paarlberg PL. Updated estimated economic welfare impacts of porcine epidemic diarrhea virus (PEDV). Department of Agricultural Economics, Purdue University 2014
  10. Han HJ, Wen HL, Zhou CM, Chen FF, Luo LM et al. Bats as reservoirs of severe emerging infectious diseases. Virus Res 2015;205:1–6 [CrossRef][PubMed]
    [Google Scholar]
  11. Hu B, Ge X, Wang LF, Shi Z. Bat origin of human coronaviruses. Virol J 2015;12:221 [CrossRef][PubMed]
    [Google Scholar]
  12. de Wit E, van Doremalen N, Falzarano D, Munster VJ. SARS and MERS: recent insights into emerging coronaviruses. Nat Rev Microbiol 2016;14:523–534 [CrossRef][PubMed]
    [Google Scholar]
  13. Munster VJ, Adney DR, van Doremalen N, Brown VR, Miazgowicz KL et al. Replication and shedding of MERS-CoV in Jamaican fruit bats (Artibeus jamaicensis). Sci Rep 2016;6:21878 [CrossRef][PubMed]
    [Google Scholar]
  14. 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 [CrossRef][PubMed]
    [Google Scholar]
  15. Gu J, Korteweg C. Pathology and pathogenesis of severe acute respiratory syndrome. Am J Pathol 2007;170:1136–1147 [CrossRef][PubMed]
    [Google Scholar]
  16. Singh SK. Middle East respiratory syndrome virus pathogenesis. Semin Respir Crit Care Med 2016;37:572–577 [CrossRef][PubMed]
    [Google Scholar]
  17. Madson DM, Magstadt DR, Arruda PH, Hoang H, Sun D et al. Pathogenesis of porcine epidemic diarrhea virus isolate (US/Iowa/18984/2013) in 3-week-old weaned pigs. Vet Microbiol 2014;174:60–68 [CrossRef][PubMed]
    [Google Scholar]
  18. Jung K, Saif LJ. Porcine epidemic diarrhea virus infection: etiology, epidemiology, pathogenesis and immunoprophylaxis. Vet J 2015;204:134–143 [CrossRef][PubMed]
    [Google Scholar]
  19. Mcguire LP, Turner JM, Warnecke L, Mcgregor G, Bollinger TK et al. White-Nose syndrome disease severity and a comparison of diagnostic methods. Ecohealth 2016;13:60–71 [CrossRef][PubMed]
    [Google Scholar]
  20. Misra V, Dumonceaux T, Dubois J, Willis C, Nadin-Davis S et al. Detection of polyoma and corona viruses in bats of Canada. J Gen Virol 2009;90:2015–2022 [CrossRef][PubMed]
    [Google Scholar]
  21. Warnecke L, Turner JM, Bollinger TK, Lorch JM, Misra V et al. Inoculation of bats with European geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome. Proc Natl Acad Sci USA 2012;109:6999–7003 [CrossRef][PubMed]
    [Google Scholar]
  22. Wevers BA, Van der Hoek L. Recently discovered human coronaviruses. Clin Lab Med 2009;29:715–724 [CrossRef][PubMed]
    [Google Scholar]
  23. Osborne C, Cryan PM, O'Shea TJ, Oko LM, Ndaluka C et al. Alphacoronaviruses in New World bats: prevalence, persistence, phylogeny, and potential for interaction with humans. PLoS One 2011;6:e19156 [CrossRef][PubMed]
    [Google Scholar]
  24. Dominguez SR, O'Shea TJ, Oko LM, Holmes KV. Detection of group 1 coronaviruses in bats in North America. Emerg Infect Dis 2007;13:1295–1300 [CrossRef][PubMed]
    [Google Scholar]
  25. Strong JE, Wong G, Jones SE, Grolla A, Theriault S et al. Stimulation of Ebola virus production from persistent infection through activation of the Ras/MAPK pathway. Proc Natl Acad Sci USA 2008;105:17982–17987 [CrossRef][PubMed]
    [Google Scholar]
  26. Mizutani T, Fukushi S, Saijo M, Kurane I, Morikawa S. Regulation of p90RSK phosphorylation by SARS-CoV infection in Vero E6 cells. FEBS Lett 2006;580:1417–1424 [CrossRef][PubMed]
    [Google Scholar]
  27. Palacios G, Jabado O, Renwick N, Briese T, Lipkin WI. Severe acute respiratory syndrome coronavirus persistence in vero cells. Chin Med J 2005;118:451–459[PubMed]
    [Google Scholar]
  28. Plowright RK, Eby P, Hudson PJ, Smith IL, Westcott D et al. Ecological dynamics of emerging bat virus spillover. Proc Biol Sci 2015;282:20142124 [CrossRef][PubMed]
    [Google Scholar]
  29. Zhao Z, Li H, Wu X, Zhong Y, Zhang K et al. Moderate mutation rate in the SARS coronavirus genome and its implications. BMC Evol Biol 2004;4:21 [CrossRef][PubMed]
    [Google Scholar]
  30. Ge XY, Wang N, Zhang W, Hu B, Li B et al. Coexistence of multiple coronaviruses in several bat colonies in an abandoned mineshaft. Virol Sin 2016;31:31–40 [CrossRef][PubMed]
    [Google Scholar]
  31. Lassnig C, Sanchez CM, Egerbacher M, Walter I, Majer S et al. Development of a transgenic mouse model susceptible to human coronavirus 229E. Proc Natl Acad Sci USA 2005;102:8275–8280 [CrossRef][PubMed]
    [Google Scholar]
  32. Trujillo-Ortega ME, Beltrán-Figueroa R, García-Hernández ME, Juárez-Ramírez M, Sotomayor-González A et al. Isolation and characterization of porcine epidemic diarrhea virus associated with the 2014 disease outbreak in Mexico: case report. BMC Vet Res 2016;12:132 [CrossRef][PubMed]
    [Google Scholar]
  33. Field H, Jordan D, Edson D, Morris S, Melville D et al. Spatiotemporal aspects of Hendra virus infection in pteropid bats (Flying-Foxes) in Eastern Australia. PLoS One 2015;10:e0144055 [CrossRef][PubMed]
    [Google Scholar]
  34. Plowright RK, Peel AJ, Streicker DG, Gilbert AT, Mccallum H et al. Transmission or within-host dynamics driving pulses of zoonotic viruses in reservoir-host populations. PLoS Negl Trop Dis 2016;10:e0004796 [CrossRef][PubMed]
    [Google Scholar]
  35. Andrews S. 2010; FastQC: a quality control tool for high throughput sequence data. Available Online Atwww.bioinformatics.babraham.ac.uk/projects/fastqc/
  36. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014;30:2114–2120 [CrossRef][PubMed]
    [Google Scholar]
  37. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 2013;14:R36 [CrossRef][PubMed]
    [Google Scholar]
  38. Cunningham F, Amode MR, Barrell D, Beal K, Billis K et al. Ensembl 2015. Nucleic Acids Res 2015;43:D662–D669 [CrossRef][PubMed]
    [Google Scholar]
  39. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The sequence alignment/Map format and SAMtools. Bioinformatics 2009;25:2078–2079 [CrossRef][PubMed]
    [Google Scholar]
  40. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010;26:841–842 [CrossRef][PubMed]
    [Google Scholar]
  41. Valderrama X, Misra V. Novel Brn3a cis-acting sequences mediate transcription of human trkA in neurons. J Neurochem 2008;105:425–435 [CrossRef][PubMed]
    [Google Scholar]
  42. Banerjee A, Rapin N, Miller M, Griebel P, Zhou Y et al. Generation and characterization of Eptesicus fuscus (Big brown bat) kidney cell lines immortalized using the Myotis polyomavirus large T-antigen. J Virol Methods 2016;237:166–173 [CrossRef][PubMed]
    [Google Scholar]
  43. Li KB, K-b L. CLUSTALW-MPI: CLUSTALW analysis using distributed and parallel computing. Bioinformatics 2003;19:1585–1586[PubMed][CrossRef]
    [Google Scholar]
  44. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016;33:1870–1874 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000898
Loading
/content/journal/jgv/10.1099/jgv.0.000898
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error