1932

Abstract

The origin of SARS-CoV-2 has evoked heated debate and strong accusations, yet seemingly little resolution. I review the scientific evidence on the origin of SARS-CoV-2 and its subsequent spread through the human population. The available data clearly point to a natural zoonotic emergence within, or closely linked to, the Huanan Seafood Wholesale Market in Wuhan. There is no direct evidence linking the emergence of SARS-CoV-2 to laboratory work conducted at the Wuhan Institute of Virology. The subsequent global spread of SARS-CoV-2 was characterized by a gradual adaptation to humans, with dual increases in transmissibility and virulence until the emergence of the Omicron variant. Of note has been the frequent transmission of SARS-CoV-2 from humans to other animals, marking it as a strongly host generalist virus. Unless lessons from the origin of SARS-CoV-2 are learned, it is inevitable that more zoonotic events leading to more epidemics and pandemics will plague human populations.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-093022-013037
2024-09-26
2025-02-13
Loading full text...

Full text loading...

/deliver/fulltext/virology/11/1/annurev-virology-093022-013037.html?itemId=/content/journals/10.1146/annurev-virology-093022-013037&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Chaudhary N, Weissman D, Whitehead KA. 2021.. mRNA vaccines for infectious diseases: principles, delivery and clinical translation. . Nat. Rev. Drug Discov. 20::81738
    [Crossref] [Google Scholar]
  2. 2.
    Chen Z, Azman AS, Chen X, Zou J, Tian Y, et al. 2022.. Global landscape of SARS-CoV-2 genomic surveillance and data sharing. . Nat. Genet. 54::499507
    [Crossref] [Google Scholar]
  3. 3.
    Holmes EC. 2022.. COVID-19—lessons for zoonotic disease. . Science 375::111415
    [Crossref] [Google Scholar]
  4. 4.
    He W-T, Hou X, Zhao J, Sun J, He H, et al. 2022.. Virome characterization of game animals in China reveals a spectrum of emerging pathogens. . Cell 185::11171129
    [Crossref] [Google Scholar]
  5. 5.
    Delaune D, Hul V, Karlsson EA, Hassanin A, Tey PO, et al. 2021.. A novel SARS-CoV-2 related coronavirus in bats from Cambodia. . Nat. Commun. 12::6563
    [Crossref] [Google Scholar]
  6. 6.
    Han Y, Xu P, Wang Y, Zhao W, Zhang J, et al. 2023.. Panoramic analysis of coronaviruses carried by representative bat species in Southern China to better understand the coronavirus sphere. . Nat. Commun. 14::5537
    [Crossref] [Google Scholar]
  7. 7.
    Hassanin A, Tu V, Görföl T, Ngon L, Pham P, et al. 2023.. Phylogeographic evolution of horseshoe bat sarbecoviruses in Vietnam and implications for the origins of SARS-CoV and SARS-CoV-2. . Preprint. Res. Sq. https://doi.org/10.21203/rs.3.rs-3227228/v1
    [Google Scholar]
  8. 8.
    Temmam S, Vongphayloth K, Baquero E, Munier S, Bonomi M, et al. 2022.. Bat coronaviruses related to SARS-CoV-2 and infectious for human cells. . Nature 604::33036
    [Crossref] [Google Scholar]
  9. 9.
    Wacharapluesadee S, Tan CW, Maneeorn P, Duengkae P, Zhu F, et al. 2021.. Evidence for SARS-CoV-2 related coronaviruses circulating in bats and pangolins in Southeast Asia. . Nat. Commun. 12::972
    [Crossref] [Google Scholar]
  10. 10.
    Zhou P, Yang XL, Wang XG, Hu B, Zhang L, et al. 2020.. A pneumonia outbreak associated with a new coronavirus of probable bat origin. . Nature 579::27073
    [Crossref] [Google Scholar]
  11. 11.
    Cui J, Li F, Shi ZL. 2019.. Origin and evolution of pathogenic coronaviruses. . Nat. Rev. Microbiol. 17::18192
    [Crossref] [Google Scholar]
  12. 12.
    Hu B, Zeng L-P, Yang X-L, Ge X-Y, Zhang W, et al. 2017.. Discovery of a rich gene pool of bat SARS-related coronaviruses provides new insights into the origin of SARS coronavirus. . PLOS Pathog. 13::e1006698
    [Crossref] [Google Scholar]
  13. 13.
    Latinne A, Hu B, Olival KJ, Zhu G, Zhang L, et al. 2020.. Origin and cross-species transmission of bat coronaviruses in China. . Nat. Commun. 11::4235
    [Crossref] [Google Scholar]
  14. 14.
    Yu P, Hu B, Shi ZL, Cui J. 2019.. Geographical structure of bat SARS-related coronaviruses. . Infect. Genet. Evol. 69::22429
    [Crossref] [Google Scholar]
  15. 15.
    Li W, Shi Z, Yu M, Ren W, Smith C, et al. 2005.. Bats are natural reservoirs of SARS-like coronaviruses. . Science 310::67679
    [Crossref] [Google Scholar]
  16. 16.
    Zhou H, Ji J, Chen X, Bi Y, Li J, et al. 2021.. Identification of novel bat coronaviruses sheds light on the evolutionary origins of SARS-CoV-2 and related viruses. . Cell 184::438091
    [Crossref] [Google Scholar]
  17. 17.
    Wang J, Pan YF, Yang LF, Yang WH, Lv K, et al. 2023.. Individual bat virome analysis reveals co-infection and spillover among bats and virus zoonotic potential. . Nat. Commun. 14::4079
    [Crossref] [Google Scholar]
  18. 18.
    Gilbert M, Mohamed M, Choong SS, Baqi A, Kumaran JV, et al. 2023.. Presence of SARS-CoV-2-like coronaviruses in bats from east coast Malaysia. . Trop. Biomed. 40::27380
    [Crossref] [Google Scholar]
  19. 19.
    Hou YJ, Chiba S, Leist SR, Meganck RM, Martinez DR, et al. 2023.. Host range, transmissibility and antigenicity of a pangolin coronavirus. . Nat. Microbiol. 8::182033
    [Crossref] [Google Scholar]
  20. 20.
    Lam TT-Y, Jia N, Zhang Y-W, Shum MH-H, Juan J-F, et al. 2020.. Identifying SARS-CoV-2 related coronaviruses in Malayan pangolins. . Nature 583::28285
    [Crossref] [Google Scholar]
  21. 21.
    Peng MS, Li JB, Cai ZF, Liu H, Tang X, et al. 2021.. The high diversity of SARS-CoV-2-related coronaviruses in pangolins alerts potential ecological risks. . Zool. Res. 42::83444
    [Google Scholar]
  22. 22.
    Xiao K, Zhai J, Feng Y, Zhou N, Zhang X, et al. 2020.. Isolation of SARS-CoV-2-related coronavirus from Malayan pangolins. . Nature 583::28689
    [Crossref] [Google Scholar]
  23. 23.
    Zhang T, Wu Q, Zhang Z. 2020.. Probable pangolin origin of SARS-CoV-2 associated with the COVID-19 outbreak. . Curr. Biol. 30::134651
    [Crossref] [Google Scholar]
  24. 24.
    Lin X-D, Wang W, Hao Z-Y, Wang Z-X, Guo W-P, et al. 2017.. Extensive diversity of coronaviruses in bats from China. . Virology 507::110
    [Crossref] [Google Scholar]
  25. 25.
    Wang W, Tian JH, Chen X, Hu RX, Lin XD, et al. 2022.. Coronaviruses in wild animals sampled in and around Wuhan at the beginning of COVID-19 emergence. . Virus Evol. 8::veac046
    [Crossref] [Google Scholar]
  26. 26.
    Sánchez CA, Li H, Phelps KL, Zambrana-Torrelio C, Wang LF, et al. 2022.. A strategy to assess spillover risk of bat SARS-related coronaviruses in Southeast Asia. . Nat. Commun. 13::4380
    [Crossref] [Google Scholar]
  27. 27.
    Evans TS, Tan CW, Aung O, Phyu S, Lin H, et al. 2023.. Exposure to diverse sarbecoviruses indicates frequent zoonotic spillover in human communities interacting with wildlife. . Int. J. Infect. Dis. 131::5764
    [Crossref] [Google Scholar]
  28. 28.
    Wang N, Li S-Y, Yang X-L, Huang H-M, Zhang Y-J, et al. 2018.. Serological evidence of bat SARS-related coronavirus infection in humans, China. . Virol. Sin. 33::1047
    [Crossref] [Google Scholar]
  29. 29.
    Yu D, Li H, Xu R, He J. 2003.. Prevalence of IgG antibody to SARS-associated coronavirus in animal traders—Guangdong Province, China, 2003. . MMWR Morb. Mortal. Wkly. Rep. 52::98687
    [Google Scholar]
  30. 30.
    Boni MF, Lemey P, Jiang X, Lam TT-Y, Perry BW, et al. 2020.. Evolutionary origins of the SARS-CoV-2 sarbecovirus lineage responsible for the COVID-19 pandemic. . Nat. Microbiol. 5::140817
    [Crossref] [Google Scholar]
  31. 31.
    de Klerk A, Swanepoel P, Lourens R, Zondo M, Abodunran I, et al. 2022.. Conserved recombination patterns across coronavirus subgenera. . Virus Evol. 8::veac054
    [Crossref] [Google Scholar]
  32. 32.
    Li LL, Wang JL, Ma XH, Sun XM, Li JS, et al. 2021.. A novel SARS-CoV-2 related coronavirus with complex recombination isolated from bats in Yunnan province, China. . Emerg. Microbes Infect. 10::168390
    [Crossref] [Google Scholar]
  33. 33.
    Li X, Giorgi EE, Marichannegowda MH, Foley B, Xiao C, et al. 2020.. Emergence of SARS-CoV-2 through recombination and strong purifying selection. . Sci. Adv. 6::eabb9153
    [Crossref] [Google Scholar]
  34. 34.
    Lytras S, Hughes J, Martin D, Swanepoel P, de Klerk A, et al. 2022.. Exploring the natural origins of SARS-CoV-2 in the light of recombination. . Genome Biol. Evol. 14::evac018
    [Crossref] [Google Scholar]
  35. 35.
    Pekar JE, Lytras S, Ghafari M, Magee AF, Parker E, et al. 2023.. The recency and geographical origins of the bat viruses ancestral to SARS-CoV and SARS-CoV-2. . bioRxiv 12:2023.07.12.548617. https://doi.org/10.1101/2023.07.12.548617
  36. 36.
    Heighton SP, Gaubert P. 2021.. A timely systematic review on pangolin research, commercialization, and popularization to identify knowledge gaps and produce conservation guidelines. . Biol. Conserv. 256::109042
    [Crossref] [Google Scholar]
  37. 37.
    Liu P, Chen W, Chen JP. 2019.. Viral metagenomics revealed Sendai virus and coronavirus infection of Malayan pangolins (Manis javanica). . Viruses 12::11
    [Crossref] [Google Scholar]
  38. 38.
    Liang X, Chen X, Zhai J, Li X, Zhang X, et al. 2023.. Pathogenicity, tissue tropism and potential vertical transmission of SARSr-CoV-2 in Malayan pangolins. . PLOS Pathog. 19::e1011384
    [Crossref] [Google Scholar]
  39. 39.
    Liu MQ, Lin HF, Li J, Chen Y, Luo Y, et al. 2023.. A SARS-CoV-2-related virus from Malayan pangolin causes lung infection without severe disease in human ACE2-transgenic mice. . J. Virol. 97::e0171922
    [Crossref] [Google Scholar]
  40. 40.
    Chen J, Yang X, Si H, Gong Q, Que T, et al. 2023.. A bat MERS-like coronavirus circulates in pangolins and utilizes human DPP4 and host proteases for cell entry. . Cell 186::85063
    [Crossref] [Google Scholar]
  41. 41.
    Shi W, Shi M, Que TC, Cui XM, Ye RZ, et al. 2022.. Trafficked Malayan pangolins contain viral pathogens of humans. . Nat. Microbiol. 7::125969
    [Crossref] [Google Scholar]
  42. 42.
    Holmes EC, Goldstein SA, Rasmussen AL, Robertson DL, Crits-Christoph A, et al. 2021.. The origins of SARS-CoV-2: a critical review. . Cell 184::484856
    [Crossref] [Google Scholar]
  43. 43.
    Chan A, Ridley M. 2021.. Viral: The Search for the Origin of COVID-19. New York:: Harper Collins
    [Google Scholar]
  44. 44.
    Worobey M, Levy JI, Serrano LMM, Crits-Christoph A, Pekar JE, et al. 2022.. The Huanan Seafood Wholesale Market in Wuhan was the early epicenter of the COVID-19 pandemic. . Science 377::95159
    [Crossref] [Google Scholar]
  45. 45.
    Worobey M. 2021.. Dissecting the early COVID-19 cases in Wuhan. . Science 374::12024
    [Crossref] [Google Scholar]
  46. 46.
    Pekar JE, Magee A, Parker E, Moshiri N, Izhikevich K, et al. 2022.. The molecular epidemiology of multiple zoonotic origins of SARS-CoV-2. . Science 377::96066
    [Crossref] [Google Scholar]
  47. 47.
    Crits-Christoph A, Levy JI, Pekar JE, Goldstein SA, Singh R, et al. 2023.. Genetic tracing of market wildlife and viruses at the epicenter of the COVID-19 pandemic. . bioRxiv 2023.09.13.557637. https://doi.org/10.1101/2023.09.13.557637
  48. 48.
    WHO (World Health Organ.). 2021.. WHO-convened global study of origins of SARS-CoV-2: China Part. Rep. , World Health Organ., Geneva:
    [Google Scholar]
  49. 49.
    Xiao X, Newman C, Buesching CD, Macdonald DW, Zhou Z-M. 2021.. Animal sales from Wuhan wet markets immediately prior to the COVID-19 pandemic. . Sci. Rep. 11::11898
    [Crossref] [Google Scholar]
  50. 50.
    Zhang Y-Z, Holmes EC. 2020.. A genomic perspective on the origin and emergence of SARS-CoV-2. . Cell 181::22327
    [Crossref] [Google Scholar]
  51. 51.
    Liu WJ, Liu P, Lei W, Jia Z, He Z, et al. 2023.. Surveillance of SARS-CoV-2 at the Huanan Seafood Market. . Nature. https://doi.org/10.1038/s41586-023-06043-2
    [Google Scholar]
  52. 52.
    Guan Y, Zheng BJ, He YQ, Liu XL, Zhuang ZX, et al. 2003.. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. . Science 302::27678
    [Crossref] [Google Scholar]
  53. 53.
    Wang M, Yan M, Xu H, Liang W, Kan B, et al. 2005.. SARS-CoV infection in a restaurant from palm civet. . Emerg. Infect. Dis. 11::186065
    [Crossref] [Google Scholar]
  54. 54.
    Kan B, Wang M, Jing H, Xu H, Jiang X, et al. 2005.. Molecular evolution analysis and geographic investigation of severe acute respiratory syndrome coronavirus-like virus in palm civets at an animal market and on farms. . J. Virol. 79::11892900
    [Crossref] [Google Scholar]
  55. 55.
    Freuling CM, Breithaupt A, Müller T, Sehl J, Balkema-Buschmann A, et al. 2020.. Susceptibility of raccoon dogs for experimental SARS-CoV-2 infection. . Emerg. Infect. Dis. 26::298285
    [Crossref] [Google Scholar]
  56. 56.
    Xia X. 2021.. Dating the common ancestor from an NCBI tree of 83688 high-quality and full-length SARS-CoV-2 genomes. . Viruses 13::1790
    [Crossref] [Google Scholar]
  57. 57.
    Duchene S, Featherstone L, Haritopoulou-Sinanidou M, Rambaut A, Lemey P, Baele G. 2020.. Temporal signal and the phylodynamic threshold of SARS-CoV-2. . Virus Evol. 6::veaa061
    [Crossref] [Google Scholar]
  58. 58.
    Roberts DL, Rossman JS, Jarić I. 2021.. Dating first cases of COVID-19. . PLOS Pathog. 17::e1009620
    [Crossref] [Google Scholar]
  59. 59.
    Fongaro G, Stoco PH, Souza DSM, Grisard EC, Magri ME, et al. 2021.. The presence of SARS-CoV-2 RNA in human sewage in Santa Catarina, Brazil, November 2019. . Sci. Total Environ. 778::146198
    [Crossref] [Google Scholar]
  60. 60.
    Deslandes A, Berti V, Tandjaoui-Lambotte Y, Alloui C, Carbonnelle E, et al. 2020.. SARS-CoV-2 was already spreading in France in late December 2019. . Int. J. Antimicrob. Agents 55::106006
    [Crossref] [Google Scholar]
  61. 61.
    Amendola A, Bianchi S, Gori M, Colzani D, Canuti M, et al. 2021.. Evidence of SARS-CoV-2 RNA in an oropharyngeal swab specimen, Milan, Italy, early December 2019. . Emerg. Infect. Dis. 27::64850
    [Crossref] [Google Scholar]
  62. 62.
    Amendola A, Canuti M, Bianchi S, Kumar S, Fappani C, et al. 2022.. Molecular evidence for SARS-CoV-2 in samples collected from patients with morbilliform eruptions since late 2019 in Lombardy, northern Italy. . Environ. Res. 215::113979
    [Crossref] [Google Scholar]
  63. 63.
    Apolone G, Montomoli E, Manenti A, Boeri M, Sabia F, et al. 2021.. Unexpected detection of SARS-CoV-2 antibodies in the prepandemic period in Italy. . Tumori 107::44651
    [Crossref] [Google Scholar]
  64. 64.
    Bianchi S, Fappani C, Gori M, Canuti M, Colzani D, et al. 2023.. Serological investigation of SARS-CoV-2 infection in patients with suspect measles, 2017–2022. . Virol. J. 20::160
    [Crossref] [Google Scholar]
  65. 65.
    Canuti M, Bianchi S, Kolbl O, Pond SLK, Kumar S, et al. 2022.. Waiting for the truth: Is reluctance in accepting an early origin hypothesis for SARS-CoV-2 delaying our understanding of viral emergence?. BMJ Glob. Health 7::e008386
    [Crossref] [Google Scholar]
  66. 66.
    Gianotti R, Barberis M, Fellegara G, Galván-Casas C, Gianotti E. 2021.. COVID-19-related dermatosis in November 2019: Could this case be Italy's patient zero?. Br. J. Dermatol. 184::97071
    [Crossref] [Google Scholar]
  67. 67.
    La Rosa G, Mancini P, Bonanno Ferraro G, Veneri C, Iaconelli M, et al. 2021.. SARS-CoV-2 has been circulating in northern Italy since December 2019: evidence from environmental monitoring. . Sci. Total Environ. 750::141711
    [Crossref] [Google Scholar]
  68. 68.
    Bahry D. 2023.. Rational discourse on virology and pandemics. . mBio 14::e0031323
    [Crossref] [Google Scholar]
  69. 69.
    Bloom JD, Chan YA, Baric RS, Bjorkman PJ, Cobey S, et al. 2021.. Investigate the origins of COVID-19. . Science 372::694
    [Crossref] [Google Scholar]
  70. 70.
    Harrison NL, Sachs JD. 2022.. A call for an independent inquiry into the origin of the SARS-CoV-2 virus. . PNAS 119::e2202769119
    [Crossref] [Google Scholar]
  71. 71.
    Maxmen A, Mallapaty S. 2021.. The COVID lab-leak hypothesis: what scientists do and don't know. . Nature 594::31315
    [Crossref] [Google Scholar]
  72. 72.
    Relman DA. 2020.. Opinion: To stop the next pandemic, we need to unravel the origins of COVID-19. . PNAS 117::2924648
    [Crossref] [Google Scholar]
  73. 73.
    van Helden J, Butler CD, Achaz G, Canard B, Casane D, et al. 2021.. An appeal for an objective, open, and transparent scientific debate about the origin of SARS-CoV-2. . Lancet 398::14024
    [Crossref] [Google Scholar]
  74. 74.
    Holmes EC. 2022.. The COVID lab leak theory is dead. Here's how we know the virus came from a Wuhan market. . Conversation, Aug. 15. https://theconversation.com/the-covid-lab-leak-theory-is-dead-heres-how-we-know-the-virus-came-from-a-wuhan-market-188163
    [Google Scholar]
  75. 75.
    Ge X-Y, Wang N, Zhang W, Hu B, Li B, et al. 2016.. Coexistence of multiple coronaviruses in several bat colonies in an abandoned mineshaft. . Virol. Sin. 31::3140
    [Crossref] [Google Scholar]
  76. 76.
    Yang XL, Hu B, Wang B, Wang MN, Zhang Q, et al. 2015.. Isolation and characterization of a novel bat coronavirus closely related to the direct progenitor of severe acute respiratory syndrome coronavirus. . J. Virol. 90::325356
    [Crossref] [Google Scholar]
  77. 77.
    Cohen J. 2020.. Wuhan coronavirus hunter Shi Zhengli speaks out. . Science 369::48788
    [Crossref] [Google Scholar]
  78. 78.
    Calvert J, Arbuthnott G. 2023.. What really went on inside the Wuhan lab weeks before Covid erupted. . Sunday Times. June 10. https://www.thetimes.co.uk/article/inside-wuhan-lab-covid-pandemic-china-america-qhjwwwvm0
    [Google Scholar]
  79. 79.
    Zhan SH, Deverman BE, Chan YA. 2020.. SARS-CoV-2 is well adapted for humans. What does this mean for re-emergence?. bioRxiv 2020.05.01.073262. https://doi.org/10.1101/2020.05.01.073262
  80. 80.
    Hui KPY, Ho JCW, Cheung MC, Ng KC, Ching RHH, et al. 2022.. SARS-CoV-2 Omicron variant replication in human bronchus and lung ex vivo. . Nature 603::71520
    [Crossref] [Google Scholar]
  81. 81.
    Korber B, Fischer WM, Gnanakaran S, Yoon H, Theiler J, et al. 2020.. Tracking changes in SARS-CoV-2 spike: evidence that D614G increases infectivity of the COVID-19 virus. . Cell 182::81227
    [Crossref] [Google Scholar]
  82. 82.
    Zhou B, Thao TTN, Hoffmann D, Taddeo A, Ebert N, et al. 2021.. SARS-CoV-2 spike D614G change enhances replication and transmission. . Nature 592::12227
    [Crossref] [Google Scholar]
  83. 83.
    Telenti A, Arvin A, Corti D, Diamond MS, García-Sastre A, et al. 2021.. After the pandemic: perspectives on the future trajectory of COVID-19. . Nature 596::495504
    [Crossref] [Google Scholar]
  84. 84.
    Bloom JD. 2021.. Recovery of deleted deep sequencing data sheds more light on the early Wuhan SARS-CoV-2 epidemic. . Mol. Biol. Evol. 38::521124
    [Crossref] [Google Scholar]
  85. 85.
    MacLean OA, Lytras S, Weaver S, Singer JB, Boni MF, et al. 2021.. Natural selection in the evolution of SARS-CoV-2 in bats created a generalist virus and highly capable human pathogen. . PLOS Biol. 19::e3001115
    [Crossref] [Google Scholar]
  86. 86.
    Andersen KG, Rambaut A, Lipkin WI, Holmes EC, Garry RF. 2020.. The proximal origin of SARS-CoV-2. . Nat. Med. 26::45052
    [Crossref] [Google Scholar]
  87. 87.
    Coutard B, Valle C, de Lamballerie X, Canard B, Seidah NG, Decroly E. 2020.. The spike glycoprotein of the new coronavirus 2019-nCoV contains a furin-like cleavage site absent in CoV of the same clade. . Antiviral Res. 176::104742
    [Crossref] [Google Scholar]
  88. 88.
    Garry RF. 2022.. SARS-CoV-2 furin cleavage site was not engineered. . PNAS 119::e2211107119
    [Crossref] [Google Scholar]
  89. 89.
    Peacock TP, Goldhill DH, Zhou J, Baillon L, Frise R, et al. 2021.. The furin cleavage site in the SARS-CoV-2 spike protein is required for transmission in ferrets. . Nat. Microbiol. 6::899909
    [Crossref] [Google Scholar]
  90. 90.
    Wu Y, Zhao S. 2020.. Furin cleavage sites naturally occur in coronaviruses. . Stem. Cell Res. 50::102115
    [Crossref] [Google Scholar]
  91. 91.
    Sasaki M, Uemura K, Sato A, Toba S, Sanaki T, et al. 2021.. SARS-CoV-2 variants with mutations at the S1/S2 cleavage site are generated in vitro during propagation in TMPRSS2-deficient cells. . PLOS Pathog. 17::e1009233
    [Crossref] [Google Scholar]
  92. 92.
    Yount B, Denison MR, Weiss SR, Baric RS. 2002.. Systematic assembly of a full-length infectious cDNA of mouse hepatitis virus strain A59. . J. Virol. 76::1106578
    [Crossref] [Google Scholar]
  93. 93.
    Follis KE, York J, Nunberg JH. 2006.. Furin cleavage of the SARS coronavirus spike glycoprotein enhances cell-cell fusion but does not affect virion entry. . Virology 350::35869
    [Crossref] [Google Scholar]
  94. 94.
    Zhou H, Chen X, Hu T, Li J, Song H, et al. 2020.. A novel bat coronavirus closely related to SARS-CoV-2 contains natural insertions at the S1/S2 cleavage site of the spike protein. . Curr. Biol. 30::2196203
    [Crossref] [Google Scholar]
  95. 95.
    Baigent SJ, McCauley JW. 2003.. Influenza type A in humans, mammals and birds: determinants of virus virulence, host-range and interspecies transmission. . Bioessays 25::65771
    [Crossref] [Google Scholar]
  96. 96.
    Wu F, Zhao S, Yu B, Chen Y-M, Wang W, et al. 2020.. A new coronavirus associated with human respiratory disease in China. . Nature 579::26569
    [Crossref] [Google Scholar]
  97. 97.
    Dou E, Kuo L. 2021.. A scientist adventurer and China's ‘Bat Woman’ are under scrutiny as coronavirus lab-leak theory gets another look. . Washington Post, June 3. https://www.washingtonpost.com/world/asia_pacific/coronavirus-bats-china-wuhan/2021/06/02/772ef984-beb2-11eb-922a-c40c9774bc48_story.html
    [Google Scholar]
  98. 98.
    Volz E, Mishra S, Chand M, Barrett JC, Johnson R, et al. 2021.. Assessing transmissibility of SARS-CoV-2 lineage B.1.1.7 in England. . Nature 593::26669
    [Crossref] [Google Scholar]
  99. 99.
    Vöhringer HS, Sanderson T, Sinnott M, De Maio N, Nguyen T, et al. 2021.. Genomic reconstruction of the SARS-CoV-2 epidemic in England. . Nature 600::50611
    [Crossref] [Google Scholar]
  100. 100.
    Tegally H, San JE, Cotten M, Moir M, Tegomoh B, et al. 2022.. The evolving SARS-CoV-2 epidemic in Africa: insights from rapidly expanding genomic surveillance. . Science 378::eabq5358
    [Crossref] [Google Scholar]
  101. 101.
    Viana R, Moyo S, Amoako DG, Tegally H, Scheepers C, et al. 2022.. Rapid epidemic expansion of the SARS-CoV-2 Omicron variant in southern Africa. . Nature 603::67986
    [Crossref] [Google Scholar]
  102. 102.
    Wilkinson E, Giovanetti M, Tegally H, San JE, Lessells R, et al. 2021.. A year of genomic surveillance reveals how the SARS-CoV-2 pandemic unfolded in Africa. . Science 374::42331
    [Crossref] [Google Scholar]
  103. 103.
    Eckerle LD, Lu X, Sperry SM, Choi L, Denison MR. 2007.. High fidelity of murine hepatitis virus replication is decreased in nsp14 exoribonuclease mutants. . J. Virol. 81::1213544
    [Crossref] [Google Scholar]
  104. 104.
    Smith EC, Blanc H, Vignuzzi M, Denison MR. 2013.. Coronaviruses lacking exoribonuclease activity are susceptible to lethal mutagenesis: evidence for proofreading and potential therapeutics. . PLOS Pathog. 9::e1003565
    [Crossref] [Google Scholar]
  105. 105.
    De Maio N, Walker CR, Turakhia Y, Lanfear R, Corbett-Detig R, Goldman N. 2021.. Mutation rates and selection on synonymous mutations in SARS-CoV-2. . Genome Biol. Evol. 13::evab087
    [Crossref] [Google Scholar]
  106. 106.
    Di Giorgio S, Martignano F, Torcia MG, Mattiuz G, Conticello SG. 2020.. Evidence for host-dependent RNA editing in the transcriptome of SARS-CoV-2. . Sci. Adv. 6::eabb5813
    [Crossref] [Google Scholar]
  107. 107.
    Nakata Y, Ode H, Kubota M, Kasahara T, Matsuoka K, et al. 2023.. Cellular APOBEC3A deaminase drives mutations in the SARS-CoV-2 genome. . Nucleic Acids Res. 51::78395
    [Crossref] [Google Scholar]
  108. 108.
    Ratcliff J, Simmonds P. 2021.. Potential APOBEC-mediated RNA editing of the genomes of SARS-CoV-2 and other coronaviruses and its impact on their longer term evolution. . Virology 556::6272
    [Crossref] [Google Scholar]
  109. 109.
    Neher RA. 2022.. Contributions of adaptation and purifying selection to SARS-CoV-2 evolution. . Virus Evol. 8::veac113
    [Crossref] [Google Scholar]
  110. 110.
    Sanderson T, Hisner R, Donovan-Banfield I, Hartman H, Løchen A, et al. 2023.. A molnupiravir-associated mutational signature in global SARS-CoV-2 genomes. . Nature 623::594600
    [Crossref] [Google Scholar]
  111. 111.
    Ignatieva A, Hein J, Jenkins PA. 2022.. Ongoing recombination in SARS-CoV-2 revealed through genealogical reconstruction. . Mol. Biol. Evol. 39::msac028
    [Crossref] [Google Scholar]
  112. 112.
    Jackson B, Boni MF, Bull MJ, Colleran A, Colquhoun RM, et al. 2021.. Generation and transmission of interlineage recombinants in the SARS-CoV-2 pandemic. . Cell 184::517988
    [Crossref] [Google Scholar]
  113. 113.
    Turakhia Y, Thornlow B, Hinrichs A, McBroome J, Ayala N, et al. 2022. Pandemic-scale phylogenomics reveals the SARS-CoV-2 recombination landscape. . Nature 609::99497
    [Crossref] [Google Scholar]
  114. 114.
    VanInsberghe D, Neish AS, Lowen AC, Koelle K. 2021.. Recombinant SARS-CoV-2 genomes circulated at low levels over the first year of the pandemic. . Virus Evol. 7::veab059
    [Crossref] [Google Scholar]
  115. 115.
    Gribble J, Stevens LJ, Agostini ML, Anderson-Daniels J, Chappell JD, et al. 2021.. The coronavirus proofreading exoribonuclease mediates extensive viral recombination. . PLOS Pathog. 17::e1009226
    [Crossref] [Google Scholar]
  116. 116.
    Tamura T, Ito J, Uriu K, Zahradnik J, Kida I, et al. 2023.. Virological characteristics of the SARS-CoV-2 XBB variant derived from recombination of two Omicron subvariants. . Nat. Commun. 14::2800
    [Crossref] [Google Scholar]
  117. 117.
    Bouhaddou M, Reuschl AK, Polacco BJ, Thorne LG, Ummadi MR, et al. 2023.. SARS-CoV-2 variants evolve convergent strategies to remodel the host response. . Cell 186::4597614
    [Crossref] [Google Scholar]
  118. 118.
    Wrobel AG, Benton DJ, Roustan C, Borg A, Hussain S, et al. 2022.. Evolution of the SARS-CoV-2 spike protein in the human host. . Nat. Commun. 13::1178
    [Crossref] [Google Scholar]
  119. 119.
    Grubaugh ND, Petrone ME, Holmes EC. 2020.. We shouldn't worry when a virus mutates during disease outbreaks. . Nat. Microbiol. 5::52930
    [Crossref] [Google Scholar]
  120. 120.
    Carabelli AM, Peacock TP, Thorne LG, Harvey WT, Hughes J, et al. 2023.. SARS-CoV-2 variant biology: immune escape, transmission and fitness. . Nat. Rev. Microbiol. 21::16277
    [Google Scholar]
  121. 121.
    Tsui JL, McCrone JT, Lambert B, Bajaj S, Inward RPD, et al. 2023.. Genomic assessment of invasion dynamics of SARS-CoV-2 Omicron BA.1. . Science 381::33643
    [Crossref] [Google Scholar]
  122. 122.
    Uriu K, Ito J, Kosugi Y, Tanaka YL, Mugita Y, et al. 2023.. Transmissibility, infectivity, and immune evasion of the SARS-CoV-2 BA.2.86 variant. . Lancet Infect. Dis. 23::e46061
    [Crossref] [Google Scholar]
  123. 123.
    Wang Q, Guo Y, Liu L, Schwanz LT, Li Z, et al. 2023.. Antigenicity and receptor affinity of SARS-CoV-2 BA.2.86 spike. . Nature 624::63944
    [Crossref] [Google Scholar]
  124. 124.
    Cao Y, Wang J, Jian F, Xiao T, Song W, et al. 2022.. Omicron escapes the majority of existing SARS-CoV-2 neutralizing antibodies. . Nature 602::65763
    [Crossref] [Google Scholar]
  125. 125.
    Chen DY, Chin CV, Kenney D, Tavares AH, Khan N, et al. 2023.. Spike and nsp6 are key determinants of SARS-CoV-2 Omicron BA.1 attenuation. . Nature 615::14350
    [Crossref] [Google Scholar]
  126. 126.
    Planas D, Saunders N, Maes P, Guivel-Benhassine F, Planchais C, et al. 2022.. Considerable escape of SARS-CoV-2 Omicron to antibody neutralization. . Nature 602::67175
    [Crossref] [Google Scholar]
  127. 127.
    Shuai H, Chan JF, Hu B, Chai Y, Yuen TT, et al. 2022.. Attenuated replication and pathogenicity of SARS-CoV-2 B.1.1.529 Omicron. . Nature 603::69399
    [Crossref] [Google Scholar]
  128. 128.
    Suzuki R, Yamasoba D, Kimura I, Wang L, Kishimoto M, et al. 2022.. Attenuated fusogenicity and pathogenicity of SARS-CoV-2 Omicron variant. . Nature 603::7005
    [Crossref] [Google Scholar]
  129. 129.
    Kimura I, Yamasoba D, Tamura T, Nao N, Suzuki T, et al. 2022.. Virological characteristics of the SARS-CoV-2 Omicron BA.2 subvariants, including BA.4 and BA. . 5:. Cell 185::39924007
    [Crossref] [Google Scholar]
  130. 130.
    Tian D, Sun Y, Xu H, Ye Q. 2022.. The emergence and epidemic characteristics of the highly mutated SARS-CoV-2 Omicron variant. . J. Med. Virol. 94::237683
    [Crossref] [Google Scholar]
  131. 131.
    Simon-Loriere E, Schwartz O. 2022.. Towards SARS-CoV-2 serotypes?. Nat. Rev. Microbiol. 20::18788
    [Crossref] [Google Scholar]
  132. 132.
    Meng B, Abdullahi A, Ferreira IATM, Goonawardane N, Saito A, et al. 2022.. Altered TMPRSS2 usage by SARS-CoV-2 Omicron impacts infectivity and fusogenicity. . Nature 603::70614
    [Crossref] [Google Scholar]
  133. 133.
    Wei C, Shan KJ, Wang W, Zhang S, Huan Q, Qian W. 2021.. Evidence for a mouse origin of the SARS-CoV-2 Omicron variant. . J. Genet. Genom. 48::111121
    [Crossref] [Google Scholar]
  134. 134.
    McBride DS, Garushyants SK, Franks J, Magee AF, Overend SH, et al. 2023.. Accelerated evolution of SARS-CoV-2 in free-ranging white-tailed deer. . Nat. Commun. 14::5105
    [Crossref] [Google Scholar]
  135. 135.
    Tarcsai KR, Corolciuc O, Tordai A, Ongrádi J. 2022.. SARS-CoV-2 infection in HIV-infected patients: potential role in the high mutational load of the Omicron variant emerging in South Africa. . GeroScience 44::233745
    [Crossref] [Google Scholar]
  136. 136.
    Cele S, Karim F, Lustig G, San JE, Hermanus T, et al. 2022.. SARS-CoV-2 prolonged infection during advanced HIV disease evolves extensive immune escape. . Cell Host Microbe 30::15462
    [Crossref] [Google Scholar]
  137. 137.
    Weigang S, Fuchs J, Zimmer G, Schnepf D, Kern L, et al. 2021.. Within-host evolution of SARS-CoV-2 in an immunosuppressed COVID-19 patient as a source of immune escape variants. . Nat. Commun. 12::6405
    [Crossref] [Google Scholar]
  138. 138.
    Chandler JC, Bevins SN, Ellis JW, Linder TJ, Tell RM, et al. 2021.. SARS-CoV-2 exposure in wild white-tailed deer (Odocoileus virginianus). . PNAS 118::e2114828118
    [Crossref] [Google Scholar]
  139. 139.
    Hale VL, Dennis PM, McBride DS, Nolting JM, Madden C, et al. 2022.. SARS-CoV-2 infection in free-ranging white-tailed deer. . Nature 602::48186
    [Crossref] [Google Scholar]
  140. 140.
    Koeppel KN, Mendes A, Strydom A, Rotherham L, Mulumba M, Venter M. 2022.. SARS-CoV-2 reverse zoonoses to pumas and lions. , South Africa. Viruses 14::120
    [Google Scholar]
  141. 141.
    Kuchipudi SV, Surendran-Nair M, Ruden RM, Yon M, Nissly RH, et al. 2022.. Multiple spillovers from humans and onward transmission of SARS-CoV-2 in white-tailed deer. . PNAS 119::e2121644119
    [Crossref] [Google Scholar]
  142. 142.
    Lu L, Sikkema RS, Velkers FC, Nieuwenhuijse DF, Fischer EAJ, et al. 2021.. Adaptation, spread and transmission of SARS-CoV-2 in farmed minks and associated humans in the Netherlands. . Nat. Commun. 12::6802
    [Crossref] [Google Scholar]
  143. 143.
    McAloose D, Laverack M, Wang L, Killian ML, Caserta LC, et al. 2020.. From people to Panthera: natural SARS-CoV-2 infection in tigers and lions at the Bronx Zoo. . mBio 11::e02220-20
    [Crossref] [Google Scholar]
  144. 144.
    Oreshkova N, Molenaar RJ, Vreman S, Harders F, Oude Munnink BB, et al. 2020.. SARS-CoV-2 infection in farmed minks, the Netherlands, April and May 2020. . Eurosurveillance 25::2001005
    [Crossref] [Google Scholar]
  145. 145.
    Oude Munnink BB, Sikkema RS, Nieuwenhuijse DF, Molenaar RJ, Munger E, et al. 2021.. Transmission of SARS-CoV-2 on mink farms between humans and mink and back to humans. . Science 371::17277
    [Crossref] [Google Scholar]
  146. 146.
    Shi J, Wen Z, Zhong G, Yang H, Wang C, et al. 2020.. Susceptibility of ferrets, cats, dogs, and other domesticated animals to SARS-coronavirus 2. . Science 368::101620
    [Crossref] [Google Scholar]
  147. 147.
    Yen HL, Sit THC, Brackman CJ, Chuk SSY, Gu H, et al. 2022.. Transmission of SARS-CoV-2 delta variant (AY.127) from pet hamsters to humans, leading to onward human-to-human transmission: a case study. . Lancet 399::107078
    [Crossref] [Google Scholar]
  148. 148.
    Damas J, Hughes GM, Keough KC, Painter CA, Persky NS, et al. 2020.. Broad host range of SARS-CoV-2 predicted by comparative and structural analysis of ACE2 in vertebrates. . PNAS 117::2231122
    [Crossref] [Google Scholar]
  149. 149.
    Niu S, Wang J, Bai B, Wu L, Zheng A, et al. 2021.. Molecular basis of cross-species ACE2 interactions with SARS-CoV-2-like viruses of pangolin origin. . EMBO J. 40::e107786
    [Crossref] [Google Scholar]
  150. 150.
    Roundy CM, Nunez CM, Thomas LF, Auckland LD, Tang W, et al. 2022.. High seroprevalence of SARS-CoV-2 in white-tailed deer (Odocoileus virginianus) at one of three captive cervid facilities in Texas. . Microbiol. Spectr. 10::e0057622
    [Crossref] [Google Scholar]
  151. 151.
    Woo PCY, Lau SKP, Chu C-M, Chan K-H, Tsoi H-W, et al. 2005.. Characterization and complete genome sequence of a novel coronavirus, coronavirus HKU1, from patients with pneumonia. . J. Virol. 79::88495
    [Crossref] [Google Scholar]
  152. 152.
    Keusch GT, Amuasi JH, Anderson DE, Daszak P, Eckerle I, et al. 2022.. Pandemic origins and a One Health approach to preparedness and prevention: solutions based on SARS-CoV-2 and other RNA viruses. . PNAS 119::e2202871119
    [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-virology-093022-013037
Loading
/content/journals/10.1146/annurev-virology-093022-013037
Loading

Data & Media loading...

  • Article Type: Review Article
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