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. 2021 Feb 23;59(3):332–340. doi: 10.1007/s12275-021-0660-4

A comprehensive review of SARS-CoV-2 genetic mutations and lessons from animal coronavirus recombination in one health perspective

Woonsung Na 1,#, Hyoungjoon Moon 2,#, Daesub Song 3,✉
PMCID: PMC7901680  PMID: 33624270

Abstract

SARS-CoV-2 was originated from zoonotic coronaviruses and confirmed as a novel beta-coronavirus, which causes serious respiratory illness such as pneumonia and lung failure, COVID-19. In this review, we describe the genetic characteristics of SARS-CoV-2, including types of mutation, and molecular epidemiology, highlighting its key difference from animal coronaviruses. We further summarized the current knowledge on clinical, genetic, and pathological features of several animal coronaviruses and compared them with SARS-CoV-2, as well as recent evidences of interspecies transmission and recombination of animal coronaviruses to provide a better understanding of SARS-CoV-2 infection in One Health perspectives. We also discuss the potential wildlife hosts and zoonotic origin of this emerging virus in detail, that may help mitigate the spread and damages caused by the disease.

Keywords: coronavirus disease 2019, genetic mutations, animal coronavirus, pandemic

Acknowledgments

This research was supported by Korea Mouse Phenotyping Project (NRF-2019M3A9D5A01102797) of the Ministry of Science and ICT through the National Research Foundation, and supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (No. 2020R1C1C1008347).

Footnotes

Conflict of Interest

We have no conflicts of interest to report.

These authors contributed equally to this work.

References

  1. Abdelrahman Z, Li M, Wang X. Comparative review of SARS-CoV-2, SARS-CoV, MERS-CoV, and influenza A respiratory viruses. Front. Immunol. 2020;11:552909. doi: 10.3389/fimmu.2020.552909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Alfano F, Fusco G, Mari V, Occhiogrosso L, Miletti G, Brunetti R, Galiero G, Desario C, Cirilli M, Decaro N. Circulation of pantropic canine coronavirus in autochthonous and imported dogs, Italy. Transbound. Emerg. Dis. 2020;67:1991–1999. doi: 10.1111/tbed.13542. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Belser JA, Katz JM, Tumpey TM. The ferret as a model organism to study influenza A virus infection. Dis. Model. Mech. 2011;4:575–579. doi: 10.1242/dmm.007823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Belsham GJ, Rasmussen TB, Normann P, Vaclavek P, Strandbygaard B, Bøtner A. Characterization of a novel chimeric swine enteric coronavirus from diseased pigs in central eastern Europe in 2016. Transbound. Emerg. Dis. 2016;63:595–601. doi: 10.1111/tbed.12579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Binn LN, Lazar EC, Keenan KP, Huxsoll DL, Marchwicki RH, Strano AJ. Recovery and characterization of a coronavirus from military dogs with diarrhea. Proc. Annu. Meet. US Anim. Health Assoc. 1974;78:359–366. [PubMed] [Google Scholar]
  6. Boley PA, Alhamo MA, Lossie G, Yadav KK, Vasquez-Lee M, Saif LJ, Kenney SP. Porcine deltacoronavirus infection and transmission in poultry, United States. Emerg. Infect. Dis. 2020;26:255–265. doi: 10.3201/eid2602.190346. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Boniotti MB, Papetti A, Lavazza A, Alborali G, Sozzi E, Chiapponi C, Faccini S, Bonilauri P, Cordioli P, Marthaler D. Porcine epidemic diarrhea virus and discovery of a recombinant swine enteric coronavirus, Italy. Emerg. Infect. Dis. 2016;22:83–87. doi: 10.3201/eid2201.150544. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brett TS, Rohani P. Transmission dynamics reveal the impracticality of COVID-19 herd immunity strategies. Proc. Natl. Acad. Sci. USA. 2020;117:25897–25903. doi: 10.1073/pnas.2008087117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Buonavoglia C, Decaro N, Martella V, Elia G, Campolo M, Desario C, Castagnaro M, Tempesta M. Canine coronavirus highly pathogenic for dogs. Emerg. Infect. Dis. 2006;12:492–494. doi: 10.3201/eid1203.050839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cha RH, Yang SH, Moon KC, Joh JS, Lee JY, Shin HS, Kim DK, Kim YS. A case report of a middle east respiratory syndrome survivor with kidney biopsy results. J. Korean Med. Sci. 2016;31:635–640. doi: 10.3346/jkms.2016.31.4.635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chen F, Knutson TP, Rossow S, Saif LJ, Marthaler DG. Decline of transmissible gastroenteritis virus and its complex evolutionary relationship with porcine respiratory coronavirus in the United States. Sci. Rep. 2019;9:3953. doi: 10.1038/s41598-019-40564-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chen Y, Liu Q, Guo D. Emerging coronaviruses: Genome structure, replication, and pathogenesis. J. Med. Virol. 2020;92:418–423. doi: 10.1002/jmv.25681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cook JK, Jackwood M, Jones RC. The long view: 40 years of infectious bronchitis research. Avian Pathol. 2012;41:239–250. doi: 10.1080/03079457.2012.680432. [DOI] [PubMed] [Google Scholar]
  14. de Nova PJG, Cortey M, Díaz I, Puente H, Rubio P, Martín M, Carvajal A. A retrospective study of porcine epidemic diarrhoea virus (PEDV) reveals the presence of swine enteric coronavirus (SeCoV) since 1993 and the recent introduction of a recombinant PEDV-SeCoV in Spain. Transbound. Emerg. Dis. 2020;67:2911–2922. doi: 10.1111/tbed.13666. [DOI] [PubMed] [Google Scholar]
  15. Decaro N, Buonavoglia C. An update on canine coronaviruses: viral evolution and pathobiology. Vet. Microbiol. 2008;132:221–234. doi: 10.1016/j.vetmic.2008.06.007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Decaro N, Mari V, Elia G, Addie DD, Camero M, Lucente MS, Martella V, Buonavoglia C. Recombinant canine coronaviruses in dogs, Europe. Emerg. Infect. Dis. 2010;16:41–47. doi: 10.3201/eid1601.090726. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Decaro N, Martella V, Saif LJ, Buonavoglia C. COVID-19 from veterinary medicine and one health perspectives: What animal coronaviruses have taught us. Res. Vet. Sci. 2020;131:21–23. doi: 10.1016/j.rvsc.2020.04.009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Domańska-Blicharz K, Woźniakowski G, Konopka B, Niemczuk K, Welz M, Rola J, Socha W, Orłowska A, Antas M, Śmietanka K, et al. Animal coronaviruses in the light of COVID-19. J. Vet. Res. 2020;64:333–345. doi: 10.2478/jvetres-2020-0050. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Dye C, Temperton N, Siddell SG. Type I feline coronavirus spike glycoprotein fails to recognize aminopeptidase N as a functional receptor on feline cell lines. J. Gen. Virol. 2007;88:1753–1760. doi: 10.1099/vir.0.82666-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Edwards CE, Yount BL, Graham RL, Leist SR, Hou YJ, Dinnon KH, 3rd, Sims AC, Swanstrom J, Gully K, Scobey TD, et al. Swine acute diarrhea syndrome coronavirus replication in primary human cells reveals potential susceptibility to infection. Proc. Natl. Acad. Sci. USA. 2020;117:26915–26925. doi: 10.1073/pnas.2001046117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Epidemiology Working Group for NCIP Epidemic ResponseChinese Center for Disease ControlPrevention The epidemiological characteristics of an outbreak of 2019 novel coronavirus diseases (COVID-19) in China. Chin. J. Epidemiol. 2020;41:145–151. [Google Scholar]
  22. Fiscus SA, Teramoto YA. Antigenic comparison of feline coronavirus isolates: evidence for markedly different peplomer glycoproteins. J. Virol. 1987;61:2607–2613. doi: 10.1128/JVI.61.8.2607-2613.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Gu J, Gong E, Zhang B, Zheng J, Gao Z, Zhong Y, Zou W, Zhan J, Wang S, Xie Z, et al. Multiple organ infection and the pathogenesis of SARS. J. Exp. Med. 2005;202:415–424. doi: 10.1084/jem.20050828. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Guo R, Fan B, Chang X, Zhou J, Zhao Y, Shi D, Yu Z, He K, Li B. Characterization and evaluation of the pathogenicity of a natural recombinant transmissible gastroenteritis virus in China. Virology. 2020;545:24–32. doi: 10.1016/j.virol.2020.03.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Gussow AB, Auslander N, Faure G, Wolf YI, Zhang F, Koonin EV. Genomic determinants of pathogenicity in SARS-CoV-2 and other human coronaviruses. Proc. Natl. Acad. Sci. USA. 2020;117:15193–15199. doi: 10.1073/pnas.2008176117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hasoksuz M, Alekseev K, Vlasova A, Zhang X, Spiro D, Halpin R, Wang S, Ghedin E, Saif LJ. Biologic, antigenic, and full-length genomic characterization of a bovine-like coronavirus isolated from a giraffe. J. Virol. 2007;81:4981–4990. doi: 10.1128/JVI.02361-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Herrewegh AA, Smeenk I, Horzinek MC, Rottier PJ, de Groot RJ. Feline coronavirus type II strains 79–1683 and 79–1146 originate from a double recombination between feline coronavirus type I and canine coronavirus. J. Virol. 1998;72:4508–4514. doi: 10.1128/JVI.72.5.4508-4514.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Jaimes JA, Millet JK, Stout AE, André NM, Whittaker GR. A tale of two viruses: the distinct spike glycoproteins of feline coronaviruses. Viruses. 2020;12:83. doi: 10.3390/v12010083. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Jaimes JA, Whittaker GR. Feline coronavirus: Insights into viral pathogenesis based on the spike protein structure and function. Virology. 2018;517:108–121. doi: 10.1016/j.virol.2017.12.027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kang S, Yang M, Hong Z, Zhang L, Huang Z, Chen X, He S, Zhou Z, Zhou Z, Chen Q, et al. Crystal structure of SARS-CoV-2 nucleocapsid protein RNA binding domain reveals potential unique drug targeting sites. Acta Pharm. Sin. B. 2020;10:1228–1238. doi: 10.1016/j.apsb.2020.04.009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Krishnamoorthy S, Swain B, Verma RS, Gunthe SS. SARS-CoV, MERS-CoV, and 2019-nCoV viruses: an overview of origin, evolution, and genetic variations. VirusDisease. 2020;31:411–423. doi: 10.1007/s13337-020-00632-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Lam TT, Jia N, Zhang YW, Shum MH, Jiang JF, Zhu HC, Tong YG, Shi YX, Ni XB, Liao YS, et al. Identifying SARS-CoV-2-related coronaviruses in Malayan pangolins. Nature. 2020;583:282–285. doi: 10.1038/s41586-020-2169-0. [DOI] [PubMed] [Google Scholar]
  33. Lee PI, Hsueh PR. Emerging threats from zoonotic coronaviruses-from SARS and MERS to 2019-nCoV. J. Microbiol. Immunol. Infect. 2020;53:365–367. doi: 10.1016/j.jmii.2020.02.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Ma T, Xu L, Ren M, Shen J, Han Z, Sun J, Zhao Y, Liu S. Novel genotype of infectious bronchitis virus isolated in China. Vet. Microbiol. 2019;230:178–186. doi: 10.1016/j.vetmic.2019.01.020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Meli M, Kipar A, Müller C, Jenal K, Gönczi E, Borel N, Gunn-Moore D, Chalmers S, Lin F, Reinacher M, et al. High viral loads despite absence of clinical and pathological findings in cats experimentally infected with feline coronavirus (FCoV) type i and in naturally FCoV-infected cats. J. Feline Med. Surg. 2004;6:69–81. doi: 10.1016/j.jfms.2003.08.007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Mercatelli D, Giorgi FM. Geographic and genomic distribution of SARS-CoV-2 mutations. Front. Microbiol. 2020;11:1800. doi: 10.3389/fmicb.2020.01800. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Najimudeen SM, Hassan MSH, Cork SC, Abdul-Careem MF. Infectious bronchitis coronavirus infection in chickens: multiple system disease with immune suppression. Pathogens. 2020;9:779. doi: 10.3390/pathogens9100779. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Pedersen NC, Liu H, Scarlett J, Leutenegger CM, Golovko L, Kennedy H, Kamal FM. Feline infectious peritonitis: Role of the feline coronavirus 3c gene in intestinal tropism and pathogenicity based upon isolates from resident and adopted shelter cats. Virus Res. 2012;165:17–28. doi: 10.1016/j.virusres.2011.12.020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Plans-Rubió P. The vaccination coverage required to establish herd immunity against influenza viruses. Prev. Med. 2012;55:72–77. doi: 10.1016/j.ypmed.2012.02.015. [DOI] [PubMed] [Google Scholar]
  40. Pratelli A, Martella V, Decaro N, Tinelli A, Camero M, Cirone F, Elia G, Cavalli A, Corrente M, Greco G, et al. Genetic diversity of a canine coronavirus detected in pups with diarrhoea in Italy. J. Virol. Methods. 2003;110:9–17. doi: 10.1016/S0166-0934(03)00081-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Puelles VG, Lütgehetmann M, Lindenmeyer MT, Sperhake JP, Wong MN, Allweiss L, Chilla S, Heinemann A, Wanner N, Liu S, et al. Multiorgan and renal tropism of SARS-CoV-2. N Engl. J. Med. 2020;383:590–592. doi: 10.1056/NEJMc2011400. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Regan AD, Whittaker GR. Utilization of DC-SIGN for entry of feline coronaviruses into host cells. J. Virol. 2008;82:11992–11996. doi: 10.1128/JVI.01094-08. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Sanchez-Morgado JM, Poynter S, Morris TH. Molecular characterization of a virulent canine coronavirus BGF strain. Virus Res. 2004;104:27–31. doi: 10.1016/j.virusres.2004.02.038. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Shiba N, Maeda K, Kato H, Mochizuki M, Iwata H. Differentiation of feline coronavirus type I and II infections by virus neutralization test. Vet. Microbiol. 2007;124:348–352. doi: 10.1016/j.vetmic.2007.04.031. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Song HD, Tu CC, Zhang GW, Wang SY, Zheng K, Lei LC, Chen QX, Gao YW, Zhou HQ, Xiang H, et al. Cross-host evolution of severe acute respiratory syndrome coronavirus in palm civet and human. Proc. Natl. Acad. Sci. USA. 2005;102:2430–2435. doi: 10.1073/pnas.0409608102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Sun W, Wang L, Huang H, Wang W, Cao L, Zhang J, Zheng M, Lu H. Genetic characterization and phylogenetic analysis of porcine deltacoronavirus (PDCoV) in Shandong province, China. Virus Res. 2020;278:197869. doi: 10.1016/j.virusres.2020.197869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Tang X, Wu C, Li X, Song Y, Yao X, Wu X, Duan Y, Zhang H, Wang Y, Qian Z. On the origin and continuing evolution of SARS-CoV-2. Natl. Sci. Rev. 2020;7:1012–1023. doi: 10.1093/nsr/nwaa036. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Tekes G, Thiel HJ. Feline coronaviruses: pathogenesis of feline infectious peritonitis. Adv. Virus Res. 2016;96:193–218. doi: 10.1016/bs.aivir.2016.08.002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Tennant BJ, Gaskell RM, Kelly DF, Carter SD, Gaskell CJ. Canine coronavirus infection in the dog following oronasal inoculation. Res. Vet. Sci. 1991;51:11–18. doi: 10.1016/0034-5288(91)90023-H. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Terada Y, Matsui N, Noguchi K, Kuwata R, Shimoda H, Soma T, Mochizuki M, Maeda K. Emergence of pathogenic coronaviruses in cats by homologous recombination between feline and canine coronaviruses. PLoS ONE. 2014;9:e106534. doi: 10.1371/journal.pone.0106534. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Toyoshima Y, Nemoto K, Matsumoto S, Nakamura Y, Kiyotani K. SARS-CoV-2 genomic variations associated with mortality rate of COVID-19. J. Hum. Genet. 2020;65:1075–1082. doi: 10.1038/s10038-020-0808-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Ugurel OM, Ata O, Turgut-Balik D. An updated analysis of variations in SARS-CoV-2 genome. Turk. J. Biol. 2020;44:157–167. doi: 10.3906/biy-2005-111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Vlasova A, Wang Q, Jung K, Langel S, Malik YS, Saif L. Porcine coronaviruses. In: Malik Y, Singh R, Yadav M, editors. Emerging and transboundary animal viruses. Singapore: Springer; 2020. pp. 79–110. [Google Scholar]
  54. Ward JM, Munn RJ, Gribble DH, Dungworth DL. An observation of feline infectious peritonitis. Vet. Rec. 1968;83:416–417. doi: 10.1136/vr.83.16.416. [DOI] [PubMed] [Google Scholar]
  55. Wen J, Cheng Y, Ling R, Dai Y, Huang B, Huang W, Zhang S, Jiang Y. Antibody-dependent enhancement of coronavirus. Int. J. Infect. Dis. 2020;100:483–489. doi: 10.1016/j.ijid.2020.09.015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Wille M, Holmes EC. Wild birds as reservoirs for diverse and abundant gamma- and deltacoronaviruses. FEMS Microbiol. Rev. 2020;44:631–644. doi: 10.1093/femsre/fuaa026. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Wong ACP, Li X, Lau SKP, Woo PCY. Global epidemiology of bat coronaviruses. Viruses. 2019;11:174. doi: 10.3390/v11020174. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Xu S, Li Y. Beware of the second wave of COVID-19. Lancet. 2020;395:1321–1322. doi: 10.1016/S0140-6736(20)30845-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Xu Z, Zhong H, Zhou Q, Du Y, Chen L, Zhang Y, Xue C, Cao Y. A highly pathogenic strain of porcine deltacoronavirus caused watery diarrhea in newborn piglets. Virol. Sin. 2018;33:131–141. doi: 10.1007/s12250-018-0003-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Yang YL, Yu JQ, Huang YW. Swine enteric alphacoronavirus (swine acute diarrhea syndrome coronavirus): an update three years after its discovery. Virus Res. 2020;285:198024. doi: 10.1016/j.virusres.2020.198024. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Zhang X, Deng T, Lu J, Zhao P, Chen L, Qian M, Guo Y, Qiao H, Xu Y, Wang Y, et al. Molecular characterization of variant infectious bronchitis virus in china, 2019: implications for control programmes. Transbound. Emerg. Dis. 2020;67:1349–1355. doi: 10.1111/tbed.13477. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Zhang, G., Li, B., Yoo, D., Qin, T., Zhang, X., Jia, Y., and Cui, S., 2020b. Animal coronaviruses and SARS-CoV-2. Transbound. Emerg. Dis. 1–14, Early View. doi: 10.1111/tbed.13791. [DOI] [PMC free article] [PubMed]
  63. Zhang Z, Shen L, Gu X. Evolutionary dynamics of MERS-CoV: Potential recombination, positive selection and transmission. Sci. Rep. 2016;6:25049. doi: 10.1038/srep25049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Zhang T, Wu Q, Zhang Z. Probable pangolin origin of SARS-CoV-2 associated with the COVID-19 outbreak. Curr. Biol. 2020;30:1346–1351. doi: 10.1016/j.cub.2020.03.022. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Zhang X, Zhu Y, Zhu X, Chen J, Shi H, Shi D, Dong H, Feng L. ORF3a deletion in field strains of porcine-transmissible gastroenteritis virus in China: a hint of association with porcine respiratory coronavirus. Transbound. Emerg. Dis. 2017;64:698–702. doi: 10.1111/tbed.12634. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Zhou P, Fan H, Lan T, Yang XL, Shi WF, Zhang W, Zhu Y, Zhang YW, Xie QM, Mani S, et al. Fatal swine acute diarrhoea syndrome caused by an HKU2-related coronavirus of bat origin. Nature. 2018;556:255–258. doi: 10.1038/s41586-018-0010-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Zhou H, Zhang M, Tian X, Shao H, Qian K, Ye J, Qin A. Identification of a novel recombinant virulent avian infectious bronchitis virus. Vet. Microbiol. 2017;199:120–127. doi: 10.1016/j.vetmic.2016.12.038. [DOI] [PMC free article] [PubMed] [Google Scholar]

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