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Journal of General Virology header logo Journal of General Virology

Volume 104, Issue 8

Genetic diversity, recombination and cross-species transmission of a waterbird gammacoronavirus in the wild Open Access

Abstract

Viruses emerging from wildlife can cause outbreaks in humans and domesticated animals. Predicting the emergence of future pathogens and mitigating their impacts requires an understanding of what shapes virus diversity and dynamics in wildlife reservoirs. In order to better understand coronavirus ecology in wild species, we sampled birds within a coastal freshwater lagoon habitat across 5 years, focussing on a large population of mute swans () and the diverse species that they interact with. We discovered and characterised the full genome of a divergent gammacoronavirus belonging to the species. We investigated the genetic diversity and dynamics of this gammacoronavirus using untargeted metagenomic sequencing of 223 faecal samples from swans of known age and sex, and RT-PCR screening of 1632 additional bird samples. The virus circulated persistently within the bird community; virus prevalence in mute swans exhibited seasonal variations, but did not change with swan age-class or epidemiological year. One whole genome was fully characterised, and revealed that the virus originated from a recombination event involving an undescribed gammacoronavirus species. Multiple lineages of this gammacoronavirus co-circulated within our study population. Viruses from this species have recently been detected in aquatic birds from both the Anatidae and Rallidae families, implying that host species habitat sharing may be important in shaping virus host range. As the host range of the species is not limited to geese, we propose that this species name should be updated to ‘’. Non-invasive sampling of bird coronaviruses may provide a tractable model system for understanding the evolutionary and cross-species dynamics of coronaviruses.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): bird , coronavirus , epidemiology , genetic diversity , recombination and wildlife
Funding
This study was supported by the:
  • Wellcome Trust (Award 220414/Z/20/Z)
    • Principle Award Recipient: SarahC Hill
  • Wellcome Trust (Award 102427/Z/13/Z)
    • Principle Award Recipient: SarahC Hill
  • BBSRC FluMap consortium (Award BB/X006204/1)
    • Principle Award Recipient: StephenH Vickers
  • COVID-19 Genomics UK Consortium (Award COGUK-FUND027)
    • Principle Award Recipient: SarahC Hill
  • Pirbright Institute (Award Pirbright Institute impact award)
    • Principle Award Recipient: SalikNazki
  • UK International Coronavirus Network (Award Roslin Institute career grant)
    • Principle Award Recipient: SarahFrançois
  • John Fell Fund, University of Oxford (Award 0009179)
    • Principle Award Recipient: SarahFrançois
  • BBSRC (Award BB/T008806/1)
    • Principle Award Recipient: SarahFrançois
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2023-08-17
2025-01-18
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References

  1. Woolhouse M, Scott F, Hudson Z, Howey R, Chase-Topping M. Human viruses: discovery and emergence. Phil Trans R Soc B 2012; 367:2864–2871 [View Article]
     [Google Scholar]
  2. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D et al. Global trends in emerging infectious diseases. Nature 2008; 451:990–993 [View Article] [PubMed]
     [Google Scholar]
  3. Delwart E. Animal virus discovery: improving animal health, understanding zoonoses, and opportunities for vaccine development. Curr Opin Virol 2012; 2:344–352 [View Article] [PubMed]
     [Google Scholar]
  4. Woolhouse M, Gaunt E. Ecological origins of novel human pathogens. Crit Rev Microbiol 2007; 33:231–242 [View Article] [PubMed]
     [Google Scholar]
  5. Woolhouse MEJ, Gowtage-Sequeria S. Host range and emerging and reemerging pathogens. Emerg Infect Dis 2005; 11:1842–1847 [View Article] [PubMed]
     [Google Scholar]
  6. Mokili JL, Rohwer F, Dutilh BE. Metagenomics and future perspectives in virus discovery. Curr Opin Virol 2012; 2:63–77 [View Article] [PubMed]
     [Google Scholar]
  7. Greninger AL. A decade of RNA virus metagenomics is (not) enough. Virus Res 2018; 244:218–229 [View Article] [PubMed]
     [Google Scholar]
  8. Shi M, Lin X-D, Chen X, Tian J-H, Chen L-J et al. The evolutionary history of vertebrate RNA viruses. Nature 2018; 556:197–202 [View Article]
     [Google Scholar]
  9. François S, Pybus OG. Towards an understanding of the avian virome. J Gen Virol 2020; 101:785–790 [View Article] [PubMed]
     [Google Scholar]
  10. Sommers P, Chatterjee A, Varsani A, Trubl G. Integrating viral metagenomics into an ecological framework. Annu Rev Virol 2021; 8:133–158 [View Article] [PubMed]
     [Google Scholar]
  11. 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 [View Article] [PubMed]
     [Google Scholar]
  12. Duffy S, Shackelton LA, Holmes EC. Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet 2008; 9:267–276 [View Article] [PubMed]
     [Google Scholar]
  13. Sanjuan R, Nebot MR, Chirico N, Mansky LM, Belshaw R. Viral mutation rates. J Virol 2010; 84:9733–9748 [View Article]
     [Google Scholar]
  14. Lai MMC. RNA recombination in animal and plant viruses. Microbiol Rev 1992; 56:61–79 [View Article] [PubMed]
     [Google Scholar]
  15. Pasternak AO, Spaan WJM, Snijder EJ. Nidovirus transcription: how to make sense?. J Gen Virol 2006; 87:1403–1421 [View Article] [PubMed]
     [Google Scholar]
  16. Woo PCY, Lau SKP, Huang Y, Yuen KY. Coronavirus diversity, phylogeny and interspecies jumping. Exp Biol Med 2009; 234:1117–1127 [View Article] [PubMed]
     [Google Scholar]
  17. Zumla A, Hui DS, Perlman S. Middle East respiratory syndrome. Lancet 2015; 386:995–1007 [View Article] [PubMed]
     [Google Scholar]
  18. Huang C, Wang Y, Li X, Ren L, Zhao J et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 2020; 395:497–506 [View Article] [PubMed]
     [Google Scholar]
  19. Cui J, Li F, Shi ZL. Origin and evolution of pathogenic coronaviruses. Nat Rev Microbiol 2019; 17:181–192 [View Article] [PubMed]
     [Google Scholar]
  20. Anthony SJ, Johnson CK, Greig DJ, Kramer S, Che X et al. Global patterns in coronavirus diversity. Virus Evol 2017; 3:vex012 [View Article] [PubMed]
     [Google Scholar]
  21. Woo PCY, Lau SKP, Lam CSF, Lau CCY, Tsang AKL et al. Discovery of seven novel mammalian and avian coronaviruses in the genus Deltacoronavirus supports bat coronaviruses as the gene source of alphacoronavirus and betacoronavirus and avian coronaviruses as the gene source of gammacoronavirus and deltacoronavirus. J Virol 2012; 86:3995–4008 [View Article] [PubMed]
     [Google Scholar]
  22. de Sales Lima FE, Gil P, Pedrono M, Minet C, Kwiatek O et al. Diverse gammacoronaviruses detected in wild birds from Madagascar. Eur J Wildl Res 2015; 61:635–639 [View Article] [PubMed]
     [Google Scholar]
  23. Domańska-Blicharz K, Miłek-Krupa J, Pikuła A. Diversity of coronaviruses in wild representatives of the Aves class in poland. Viruses 2021; 13:1–19 [View Article] [PubMed]
     [Google Scholar]
  24. Cavanagh D, Naqi SA. Infectious bronchitis. In Saif YM. ed Diseases of Poultry, 11th ed. Ames, IA: Iowa State University Press; 2003 pp 101–120
     [Google Scholar]
  25. Olsen B, Munster VJ, Wallensten A, Waldenström J, Osterhaus A et al. Global patterns of influenza a virus in wild birds. Science 2006; 312:384–388 [View Article] [PubMed]
     [Google Scholar]
  26. International Committee on Taxonomy of Viruses.. Current ICTV Taxonomy Release; 2022 https://ictv.global/taxonomy/
  27. Wille M, Holmes EC. Wild birds as reservoirs for diverse and abundant gamma- and deltacoronaviruses. FEMS Microbiol Rev 2020; 44:631–644 [View Article] [PubMed]
     [Google Scholar]
  28. Perrins CM, Ogilvie MA. A study of the abbotsbury mute swans (Cygnus Olor). Wildfowl 1981; 32:35–47
     [Google Scholar]
  29. Perrins C, McCleery R, Ogilvie M. A study of the breeding mute swans (Cygnus Olor) at Abbotsbury. Wildfowl 1994; 45:1–14
     [Google Scholar]
  30. Hill SC, François S, Thézé J, Smith AL, Simmonds P et al. Impact of host age on viral and bacterial communities in a waterbird population. ISME J 2023; 17:215–226 [View Article] [PubMed]
     [Google Scholar]
  31. Boom R, Sol CJ, Salimans MM, Jansen CL, Wertheim-van Dillen PM et al. Rapid and simple method for purification of nucleic acids. J Clin Microbiol 1990; 28:495–503 [View Article] [PubMed]
     [Google Scholar]
  32. Endoh D, Mizutani T, Kirisawa R, Maki Y, Saito H et al. Species-independent detection of RNA virus by representational difference analysis using non-ribosomal hexanucleotides for reverse transcription. Nucleic Acids Res 2005; 33:1–11 [View Article] [PubMed]
     [Google Scholar]
  33. Cotten M, Oude Munnink B, Canuti M, Deijs M, Watson SJ et al. Full genome virus detection in fecal samples using sensitive nucleic acid preparation, deep sequencing, and a novel iterative sequence classification algorithm. PLoS One 2014; 9:e93269 [View Article] [PubMed]
     [Google Scholar]
  34. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet j 2011; 17:10 [View Article]
     [Google Scholar]
  35. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 2008; 18:821–829 [View Article] [PubMed]
     [Google Scholar]
  36. Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods 2015; 12:59–60 [View Article] [PubMed]
     [Google Scholar]
  37. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article] [PubMed]
     [Google Scholar]
  38. Langmead B. Aligning short sequencing reads with Bowtie. Curr Protoc Bioinformatics 2010; 11: [View Article] [PubMed]
     [Google Scholar]
  39. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9:357–359 [View Article] [PubMed]
     [Google Scholar]
  40. Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast fourier transform. Nucleic Acids Res 2002; 30:3059–3066 [View Article] [PubMed]
     [Google Scholar]
  41. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article] [PubMed]
     [Google Scholar]
  42. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M et al. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012; 28:1647–1649 [View Article] [PubMed]
     [Google Scholar]
  43. Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast fourier transform. Nucleic Acids Res 2002; 30:3059–3066 [View Article] [PubMed]
     [Google Scholar]
  44. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010; 26:2460–2461 [View Article] [PubMed]
     [Google Scholar]
  45. de Groot RJ, Baker SC, Baric R, Enjuanes L, Gorbalenya AE et al. Family Coronaviridae. In King A, Adams M, Cartens E, Lefkowitz E. eds Virus Taxonomy Classification and Nomenclature of Viruses: Ninth Report of the International Committee on the Taxonomy of Viruses San Diego, CA: Academic Press; 2012 pp 806–828
     [Google Scholar]
  46. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010; 59:307–321 [View Article] [PubMed]
     [Google Scholar]
  47. Posada D. jModelTest: phylogenetic model averaging. Mol Biol Evol 2008; 25:1253–1256 [View Article] [PubMed]
     [Google Scholar]
  48. Sagulenko P, Puller V, Neher RA. Treetime: maximum-likelihood phylodynamic analysis. Virus Evol 2018; 4:vex042 [View Article] [PubMed]
     [Google Scholar]
  49. Martin D, Rybicki E. RDP: detection of recombination amongst aligned sequences. Bioinformatics 2000; 16:562–563 [View Article] [PubMed]
     [Google Scholar]
  50. Padidam M, Sawyer S, Fauquet CM. Possible emergence of new geminiviruses by frequent recombination. Virology 1999; 265:218–225 [View Article] [PubMed]
     [Google Scholar]
  51. Posada D, Crandall K. Evaluation of methods for detecting recombination from DNA sequences: empirical data. Mol Biol Evol 2002; 19:708–717 [View Article] [PubMed]
     [Google Scholar]
  52. Smith JM. Analyzing the mosaic structure of genes. J Mol Evol 1992; 34:126–129 [View Article] [PubMed]
     [Google Scholar]
  53. Martin DP, Posada D, Crandall KA, Williamson C. A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Res Hum Retroviruses 2005; 21:98–102 [View Article] [PubMed]
     [Google Scholar]
  54. Gibbs MJ, Armstrong JS, Gibbs AJ. Sister-scanning: a monte carlo procedure for assessing signals in recombinant sequences. Bioinformatics 2000; 16:573–582 [View Article] [PubMed]
     [Google Scholar]
  55. Weiller GF. Phylogenetic profiles: a graphical method for detecting genetic recombinations in homologous sequences. Mol Biol Evol 1998; 15:326–335 [View Article] [PubMed]
     [Google Scholar]
  56. Boni MF, Posada D, Feldman MW. An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 2007; 176:1035–1047 [View Article] [PubMed]
     [Google Scholar]
  57. Martin DP, Murrell B, Golden M, Khoosal A, Muhire B. RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol 2015; 1:1–5 [View Article] [PubMed]
     [Google Scholar]
  58. Lole KS, Bollinger RC, Paranjape RS, Gadkari D, Kulkarni SS et al. Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol 1999; 73:152–160 [View Article] [PubMed]
     [Google Scholar]
  59. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article] [PubMed]
     [Google Scholar]
  60. Charmantier A, Perrins C, McCleery RH, Sheldon BC. Quantitative genetics of age at reproduction in wild swans: support for antagonistic pleiotropy models of senescence. Proc Natl Acad Sci 2006; 103:6587–6592 [View Article] [PubMed]
     [Google Scholar]
  61. Plummer M. JAGS version 4.3.0 user manual. n.d https://sourceforge.net/projects/mcmc-jags/files/Manuals/ accessed 10 April 2023
  62. R Foundation for Statistical Computing, Vienna A. R Core Team. R A language and environment for statistical computing; 2022 https://www.r-project.org/
  63. Papineau A, Berhane Y, Wylie TN, Wylie KM, Sharpe S et al. Genome organization of Canada goose coronavirus, a novel species identified in a mass die-off of Canada geese. Sci Rep 2019; 9:5954 [View Article] [PubMed]
     [Google Scholar]
  64. Wille M, Shi M, Klaassen M, Hurt AC, Holmes EC. Virome heterogeneity and connectivity in waterfowl and shorebird communities. ISME J 2019; 13:2603–2616 [View Article] [PubMed]
     [Google Scholar]
  65. Chu DKW, Leung CYH, Gilbert M, Joyner PH, Ng EM et al. Avian coronavirus in wild aquatic birds. J Virol 2011; 85:12815–12820 [View Article] [PubMed]
     [Google Scholar]
  66. Zhuang Q, Liu S, Zhang X, Jiang W, Wang K et al. Surveillance and taxonomic analysis of the coronavirus dominant in pigeons in China. Transbound Emerg Dis 2020; 67:1981–1990 [View Article] [PubMed]
     [Google Scholar]
  67. Muradrasoli S, Bálint A, Wahlgren J, Waldenström J, Belák S et al. Prevalence and phylogeny of coronaviruses in wild birds from the bering strait area (Beringia). PLoS One 2010; 5:e13640 [View Article] [PubMed]
     [Google Scholar]
  68. Lefkowitz EJ, Dempsey DM, Hendrickson RC, Orton RJ, Siddell SG et al. Virus taxonomy: the database of the International Committee on Taxonomy of Viruses (ICTV). Nucleic Acids Res 2018; 46:D708–D717 [View Article] [PubMed]
     [Google Scholar]
  69. Frost TM, Calbrade NA, Birtles GA, Hall C, Robinson AE et al. Waterbirds in the UK 2019/20: The Wetland Bird Survey BTO/RSPB/JNCC. Thetford; 2021
     [Google Scholar]
  70. Pybus OG, Perrins CM, Choudhury B, Manvell RJ, Nunez A et al. The ecology and age structure of a highly pathogenic avian influenza virus outbreak in wild mute swans. Parasitology 2012; 139:1914–1923 [View Article] [PubMed]
     [Google Scholar]
  71. Hill SC, Manvell RJ, Schulenburg B, Shell W, Wikramaratna PS et al. Antibody responses to avian influenza viruses in wild birds broaden with age. Proc Biol Sci 2016; 283:20162159 [View Article] [PubMed]
     [Google Scholar]
  72. Hill SC, Hansen R, Watson S, Coward V, Russell C et al. Comparative micro-epidemiology of pathogenic avian influenza virus outbreaks in a wild bird population. Philos Trans R Soc Lond B Biol Sci 2019; 374:20180259 [View Article] [PubMed]
     [Google Scholar]
  73. Martin DP, Biagini P, Lefeuvre P, Golden M, Roumagnac P et al. Recombination in eukaryotic single stranded DNA viruses. Viruses 2011; 3:1699–1738 [View Article] [PubMed]
     [Google Scholar]
  74. Thor SW, Hilt DA, Kissinger JC, Paterson AH, Jackwood MW. Recombination in avian gamma-coronavirus infectious bronchitis virus. Viruses 2011; 3:1777–1799 [View Article] [PubMed]
     [Google Scholar]
  75. Jackwood MW, Hall D, Handel A. Molecular evolution and emergence of avian gammacoronaviruses. Infect Genet Evol 2012; 12:1305–1311 [View Article] [PubMed]
     [Google Scholar]
  76. Gallagher TM, Buchmeier MJ. Coronavirus spike proteins in viral entry and pathogenesis. Virology 2001; 279:371–374 [View Article] [PubMed]
     [Google Scholar]
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Genetic diversity, recombination and cross-species transmission of a waterbird gammacoronavirus in the wild
J. Gen. Virol. 104, 001883 (2023); https://doi.org/10.1099/jgv.0.001883
/content/journal/jgv/10.1099/jgv.0.001883
/content/journal/jgv/10.1099/jgv.0.001883
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