Evolutionary history, potential intermediate animal host, and cross-species analyses of SARS-CoV-2
Corresponding Author
Xingguang Li
Hubei Engineering Research Center of Viral Vector, Wuhan University of Bioengineering, Wuhan, China
Correspondence Dr Xingguang Li and Prof Yi Li, Hubei Engineering Research Center of Viral Vector, Wuhan University of Bioengineering, Wuhan, 430415, China.
Email: [email protected] (X. L.) and [email protected] (Y. L.) Prof Brian T. Foley, HIV Databases, Theoretical Biology and Biophysics Group, Los Alamos National Laboratory, Los Alamos, NM 87544.
Email: [email protected] Dr Antoine Chaillon, Department of Medicine, University of California San Diego, La Jolla, CA 92093-0679.
Email: [email protected]
Search for more papers by this authorJunjie Zai
Immunology Innovation Team, School of Medicine, Ningbo University, Ningbo, China
Search for more papers by this authorQiang Zhao
Precision Cancer Center Airport Center, Tianjin Cancer Hospital Airport Hospital, Tianjin, China
Search for more papers by this authorQing Nie
Department of Microbiology, Weifang Center for Disease Control and Prevention, Weifang, China
Search for more papers by this authorCorresponding Author
Yi Li
Hubei Engineering Research Center of Viral Vector, Wuhan University of Bioengineering, Wuhan, China
Correspondence Dr Xingguang Li and Prof Yi Li, Hubei Engineering Research Center of Viral Vector, Wuhan University of Bioengineering, Wuhan, 430415, China.
Email: [email protected] (X. L.) and [email protected] (Y. L.) Prof Brian T. Foley, HIV Databases, Theoretical Biology and Biophysics Group, Los Alamos National Laboratory, Los Alamos, NM 87544.
Email: [email protected] Dr Antoine Chaillon, Department of Medicine, University of California San Diego, La Jolla, CA 92093-0679.
Email: [email protected]
Search for more papers by this authorCorresponding Author
Brian T. Foley
HIV Databases, Theoretical Biology and Biophysics Group, Los Alamos National Laboratory, Los Alamos, New Mexico
Correspondence Dr Xingguang Li and Prof Yi Li, Hubei Engineering Research Center of Viral Vector, Wuhan University of Bioengineering, Wuhan, 430415, China.
Email: [email protected] (X. L.) and [email protected] (Y. L.) Prof Brian T. Foley, HIV Databases, Theoretical Biology and Biophysics Group, Los Alamos National Laboratory, Los Alamos, NM 87544.
Email: [email protected] Dr Antoine Chaillon, Department of Medicine, University of California San Diego, La Jolla, CA 92093-0679.
Email: [email protected]
Search for more papers by this authorCorresponding Author
Antoine Chaillon
Department of Medicine, University of California San Diego, La Jolla, California
Correspondence Dr Xingguang Li and Prof Yi Li, Hubei Engineering Research Center of Viral Vector, Wuhan University of Bioengineering, Wuhan, 430415, China.
Email: [email protected] (X. L.) and [email protected] (Y. L.) Prof Brian T. Foley, HIV Databases, Theoretical Biology and Biophysics Group, Los Alamos National Laboratory, Los Alamos, NM 87544.
Email: [email protected] Dr Antoine Chaillon, Department of Medicine, University of California San Diego, La Jolla, CA 92093-0679.
Email: [email protected]
Search for more papers by this authorCorresponding Author
Xingguang Li
Hubei Engineering Research Center of Viral Vector, Wuhan University of Bioengineering, Wuhan, China
Correspondence Dr Xingguang Li and Prof Yi Li, Hubei Engineering Research Center of Viral Vector, Wuhan University of Bioengineering, Wuhan, 430415, China.
Email: [email protected] (X. L.) and [email protected] (Y. L.) Prof Brian T. Foley, HIV Databases, Theoretical Biology and Biophysics Group, Los Alamos National Laboratory, Los Alamos, NM 87544.
Email: [email protected] Dr Antoine Chaillon, Department of Medicine, University of California San Diego, La Jolla, CA 92093-0679.
Email: [email protected]
Search for more papers by this authorJunjie Zai
Immunology Innovation Team, School of Medicine, Ningbo University, Ningbo, China
Search for more papers by this authorQiang Zhao
Precision Cancer Center Airport Center, Tianjin Cancer Hospital Airport Hospital, Tianjin, China
Search for more papers by this authorQing Nie
Department of Microbiology, Weifang Center for Disease Control and Prevention, Weifang, China
Search for more papers by this authorCorresponding Author
Yi Li
Hubei Engineering Research Center of Viral Vector, Wuhan University of Bioengineering, Wuhan, China
Correspondence Dr Xingguang Li and Prof Yi Li, Hubei Engineering Research Center of Viral Vector, Wuhan University of Bioengineering, Wuhan, 430415, China.
Email: [email protected] (X. L.) and [email protected] (Y. L.) Prof Brian T. Foley, HIV Databases, Theoretical Biology and Biophysics Group, Los Alamos National Laboratory, Los Alamos, NM 87544.
Email: [email protected] Dr Antoine Chaillon, Department of Medicine, University of California San Diego, La Jolla, CA 92093-0679.
Email: [email protected]
Search for more papers by this authorCorresponding Author
Brian T. Foley
HIV Databases, Theoretical Biology and Biophysics Group, Los Alamos National Laboratory, Los Alamos, New Mexico
Correspondence Dr Xingguang Li and Prof Yi Li, Hubei Engineering Research Center of Viral Vector, Wuhan University of Bioengineering, Wuhan, 430415, China.
Email: [email protected] (X. L.) and [email protected] (Y. L.) Prof Brian T. Foley, HIV Databases, Theoretical Biology and Biophysics Group, Los Alamos National Laboratory, Los Alamos, NM 87544.
Email: [email protected] Dr Antoine Chaillon, Department of Medicine, University of California San Diego, La Jolla, CA 92093-0679.
Email: [email protected]
Search for more papers by this authorCorresponding Author
Antoine Chaillon
Department of Medicine, University of California San Diego, La Jolla, California
Correspondence Dr Xingguang Li and Prof Yi Li, Hubei Engineering Research Center of Viral Vector, Wuhan University of Bioengineering, Wuhan, 430415, China.
Email: [email protected] (X. L.) and [email protected] (Y. L.) Prof Brian T. Foley, HIV Databases, Theoretical Biology and Biophysics Group, Los Alamos National Laboratory, Los Alamos, NM 87544.
Email: [email protected] Dr Antoine Chaillon, Department of Medicine, University of California San Diego, La Jolla, CA 92093-0679.
Email: [email protected]
Search for more papers by this authorXingguang Li, Junjie Zai, and Qiang Zhao contributed equally to this study.
Abstract
To investigate the evolutionary history of the recent outbreak of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in China, a total of 70 genomes of virus strains from China and elsewhere with sampling dates between 24 December 2019 and 3 February 2020 were analyzed. To explore the potential intermediate animal host of the SARS-CoV-2 virus, we reanalyzed virome data sets from pangolins and representative SARS-related coronaviruses isolates from bats, with particular attention paid to the spike glycoprotein gene. We performed phylogenetic, split network, transmission network, likelihood-mapping, and comparative analyses of the genomes. Based on Bayesian time-scaled phylogenetic analysis using the tip-dating method, we estimated the time to the most recent common ancestor and evolutionary rate of SARS-CoV-2, which ranged from 22 to 24 November 2019 and 1.19 to 1.31 × 10−3 substitutions per site per year, respectively. Our results also revealed that the BetaCoV/bat/Yunnan/RaTG13/2013 virus was more similar to the SARS-CoV-2 virus than the coronavirus obtained from the two pangolin samples (SRR10168377 and SRR10168378). We also identified a unique peptide (PRRA) insertion in the human SARS-CoV-2 virus, which may be involved in the proteolytic cleavage of the spike protein by cellular proteases, and thus could impact host range and transmissibility. Interestingly, the coronavirus carried by pangolins did not have the RRAR motif. Therefore, we concluded that the human SARS-CoV-2 virus, which is responsible for the recent outbreak of COVID-19, did not come directly from pangolins.
Highlights
We identified a unique peptide (PRRA) insertion in the human SARS-CoV-2 virus, which may be involved in the proteolytic cleavage of the spike protein by cellular proteases, and thus could impact host range and transmissibility.
CONFLICT OF INTERESTS
The authors declare that there are no conflict of interests.
Supporting Information
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jmv25731-sup-0001-Figure_S1.tif2.9 MB | Supporting information |
jmv25731-sup-0002-Figure_S2.tif1.1 MB | Supporting information |
jmv25731-sup-0003-Figure_S3.tif3.5 MB | Supporting information |
jmv25731-sup-0004-Figure_S4.tif1.2 MB | Supporting information |
jmv25731-sup-0005-Figure_S5.tif1 MB | Supporting information |
jmv25731-sup-0006-Figure_S6.png20 KB | Supporting information |
jmv25731-sup-0007-TableS1.xlsx23.1 KB | Supporting information |
jmv25731-sup-0008-supmat.docx12.6 KB | Supporting information |
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REFERENCES
- 1Chan JFW, Yuan S, Kok KH, et al. A familial cluster of pneumonia associated with the 2019 novel coronavirus indicating person-to-person transmission: a study of a family cluster. Lancet. 2020; 395: 514-523. https://doi.org/10.1016/S0140-6736(20)30154-9
- 2Li Q, Guan X, Wu P, et al. Early transmission dynamics in Wuhan, China, of novel coronavirus-infected pneumonia. N Engl J Med. 2020:NEJMoa2001316. https://doi.org/10.1056/NEJMoa2001316
- 3Su S, Wong G, Shi W, et al. Epidemiology, genetic recombination, and pathogenesis of coronaviruses. Trends Microbiol. 2016; 24: 490-502. https://doi.org/10.1016/j.tim.2016.03.003
- 4Drosten C, Günther S, Preiser W, et al. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N Engl J Med. 2003; 348: 1967-1976. https://doi.org/10.1056/NEJMoa030747
- 5Ksiazek TG, Erdman D, Goldsmith CS, et al. A novel coronavirus associated with severe acute respiratory syndrome. N Engl J Med. 2003; 348: 1953-1966. https://doi.org/10.1056/NEJMoa030781
- 6Zhong N, Zheng B, Li Y, et al. Epidemiology and cause of severe acute respiratory syndrome (SARS) in Guangdong, People's Republic of China, in February, 2003. Lancet. 2003; 362: 1353-1358. https://doi.org/10.1016/s0140-6736(03)14630-2
- 7Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus AD, Fouchier RA. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med. 2012; 367: 1814-1820. https://doi.org/10.1056/NEJMoa1211721
- 8de Groot RJ, Baker SC, Baric RS, et al. Middle East respiratory syndrome coronavirus (MERS-CoV): announcement of the Coronavirus Study Group. J Virol. 2013; 87: 7790-7792. https://doi.org/10.1128/JVI.01244-13
- 9Lau SKP, Li KSM, Huang Y, et al. Ecoepidemiology and complete genome comparison of different strains of severe acute respiratory syndrome-related Rhinolophus bat coronavirus in China reveal bats as a reservoir for acute, self-limiting infection that allows recombination events. J Virol. 2010; 84: 2808-2819. https://doi.org/10.1128/JVI.02219-09
- 10Guan Y, Zheng BJ, He YQ, et al. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science. 2003; 302: 276-278. https://doi.org/10.1126/science.1087139
- 11Lau SKP, Woo PCY, Li KSM, et al. Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc Natl Acad Sci U S A. 2005; 102: 14040-14045. https://doi.org/10.1073/pnas.0506735102
- 12Li W, Shi Z, Yu M, et al. Bats are natural reservoirs of SARS-like coronaviruses. Science. 2005; 310: 676-679. https://doi.org/10.1126/science.1118391
- 13Song HD, Tu CC, Zhang GW, 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. https://doi.org/10.1073/pnas.0409608102
- 14Chinese SMEC. Molecular evolution of the SARS coronavirus during the course of the SARS epidemic in China. Science. 2004; 303: 1666-1669. https://doi.org/10.1126/science.1092002
- 15Wang M, Yan M, Xu H, et al. SARS-CoV infection in a restaurant from palm civet. Emerg Infect Dis. 2005; 11: 1860-1865. https://doi.org/10.3201/eid1112.041293
- 16Müller MA, Corman VM, Jores J, et al. MERS coronavirus neutralizing antibodies in camels, Eastern Africa, 1983-1997. Emerg Infect Dis. 2014; 20: 2093-2095. https://doi.org/10.3201/eid2012.141026
- 17Chu DKW, Poon LLM, Gomaa MM, et al. MERS coronaviruses in dromedary camels, Egypt. Emerg Infect Dis. 2014; 20: 1049-1053. https://doi.org/10.3201/eid2006.140299
- 18Zhou P, Yang X-L, Wang X-G, et al. Discovery of a novel coronavirus associated with the recent pneumonia outbreak in humans and its potential bat origin. Preprint at BioRxiv. 2020. https://doi.org/10.1101/2020.01.22.914952
- 19Lu R, Zhao X, Li J, et al. Genomic characterisation and epidemiology of 2019 novel coronavirus: implications for virus origins and receptor binding. Lancet. 2020; 395: 565-574. https://doi.org/10.1016/S0140-6736(20)30251-8
- 20Liu P, Chen W, Chen JP. Viral metagenomics revealed sendai virus and coronavirus infection of Malayan pangolins (Manis javanica). Viruses. 2019; 11: 979. https://doi.org/10.3390/v11110979
- 21Elbe S, Buckland-Merrett G. Data, disease and diplomacy: GISAID's innovative contribution to global health. Glob Chall. 2017; 1: 33-46. https://doi.org/10.1002/gch2.1018
- 22Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013; 30: 772-780. https://doi.org/10.1093/molbev/mst010
- 23Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser. 1999; 41: 95-98. https://doi.org/citeulike-article-id:691774
- 24Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol. 2006; 23: 254-267. https://doi.org/10.1093/molbev/msj030
- 25Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods. 2012; 9: 772. https://doi.org/10.1038/nmeth.2109
- 26Schmidt HA, von Haeseler A. Maximum-likelihood analysis using TREE-PUZZLE. Curr Protoc Bioinformatics. 2007; 6: 6. https://doi.org/10.1002/0471250953.bi0606s17 Chapter 6, Unit 6
- 27Schmidt HA, Strimmer K, Vingron M, von Haeseler A. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics. 2002; 18: 502-504. https://doi.org/10.1093/bioinformatics/18.3.502
- 28Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987; 4: 406-425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
- 29Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980; 16: 111-120. https://doi.org/10.1007/bf01731581
- 30Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016; 33: 1870-1874. https://doi.org/10.1093/molbev/msw054
- 31Tamura K, Nei M, Kumar S. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci USA. 2004; 101: 11030-11035. https://doi.org/10.1073/pnas.0404206101
- 32Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010; 59: 307-321. https://doi.org/10.1093/sysbio/syq010
- 33Lanave C, Preparata G, Saccone C, Serio G. A new method for calculating evolutionary substitution rates. J Mol Evol. 1984; 20: 86-93. https://doi.org/10.1007/bf02101990
- 34Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 1985; 39: 783-791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
- 35Rambaut A, Lam TT, Max Carvalho L, Pybus OG. Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol. 2016; 2:vew007. https://doi.org/10.1093/ve/vew007
- 36Sagulenko P, Puller V, Neher RA. TreeTime: maximum-likelihood phylodynamic analysis. Virus Evol. 2018; 4:vex042. https://doi.org/10.1093/ve/vex042
- 37Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012; 29: 1969-1973. https://doi.org/10.1093/molbev/mss075
- 38Suchard MA, Rambaut A. Many-core algorithms for statistical phylogenetics. Bioinformatics. 2009; 25: 1370-1376. https://doi.org/10.1093/bioinformatics/btp244
- 39Zhao Z, Li H, Wu X, et al. Moderate mutation rate in the SARS coronavirus genome and its implications. BMC Evol Biol. 2004; 4: 21. https://doi.org/10.1186/1471-2148-4-21
- 40Cotten M, Watson SJ, Kellam P, et al. Transmission and evolution of the Middle East respiratory syndrome coronavirus in Saudi Arabia: a descriptive genomic study. Lancet. 2013; 382: 1993-2002. https://doi.org/10.1016/S0140-6736(13)61887-5
- 41Cotten M, Watson SJ, Zumla AI, et al. Spread, circulation, and evolution of the Middle East respiratory syndrome coronavirus. mBio. 2014; 5, https://doi.org/10.1128/mBio.01062-13
- 42Drummond AJ, Ho SY, Phillips MJ, Rambaut A. Relaxed phylogenetics and dating with confidence. PLoS Biol. 2006; 4:e88. https://doi.org/10.1371/journal.pbio.0040088
- 43Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA. Posterior summarization in Bayesian phylogenetics using tracer 1.7. Syst Biol. 2018; 67: 901-904. https://doi.org/10.1093/sysbio/syy032
- 44Kosakovsky Pond SL, Weaver S, Leigh Brown AJ, Wertheim JO. HIV-TRACE (TRAnsmission Cluster Engine): a tool for large scale molecular epidemiology of HIV-1 and other rapidly evolving pathogens. Mol Biol Evol. 2018; 35: 1812-1819. https://doi.org/10.1093/molbev/msy016
- 45Lole KS, Bollinger RC, Paranjape RS, 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
- 46Li X, Wang W, Zhao X, et al. Transmission dynamics and evolutionary history of 2019-nCoV. J Med Virol. 2020:jmv.25701. https://doi.org/10.1002/jmv.25701
- 47Li X, Zai J, Wang X, Li Y. Potential of large 'first generation' human-to-human transmission of 2019-nCoV. J Med Virol. 2020; 92: 448-454. https://doi.org/10.1002/jmv.25693
- 48Li W, Wicht O, van Kuppeveld FJM, He Q, Rottier PJM, Bosch BJ. A single point mutation creating a furin cleavage site in the spike protein renders porcine epidemic diarrhea coronavirus trypsin independent for cell entry and fusion. J Virol. 2015; 89: 8077-8081. https://doi.org/10.1128/JVI.00356-15
- 49Jaimes JA, Millet JK, Goldstein ME, Whittaker GR, Straus MR. A fluorogenic peptide cleavage assay to screen for proteolytic activity: applications for coronavirus spike protein activation. J Vis Exp. 2019. https://doi.org/10.3791/58892
- 50Kleine-Weber H, Elzayat MT, Hoffmann M, Pohlmann S. Functional analysis of potential cleavage sites in the MERS-coronavirus spike protein. Sci Rep. 2018; 8:16597. https://doi.org/10.1038/s41598-018-34859-w
- 51Falcigno L, Oliva R, D'Auria G, et al. Structural investigation of the HIV-1 envelope glycoprotein gp160 cleavage site 3: role of site-specific mutations. ChemBioChem. 2004; 5: 1653-1661. https://doi.org/10.1002/cbic.200400181
- 52Moulard M, Decroly E. Maturation of HIV envelope glycoprotein precursors by cellular endoproteases. Biochim Biophys Acta. 2000; 1469: 121-132. https://doi.org/10.1016/s0304-4157(00)00014-9
- 53Moulard M, Hallenberger S, Garten W, Klenk HD. Processing and routage of HIV glycoproteins by furin to the cell surface. Virus Res. 1999; 60: 55-65. https://doi.org/10.1016/s0168-1702(99)00002-7
- 54Decroly E, Vandenbranden M, Ruysschaert JM, et al. The convertases furin and PC1 can both cleave the human immunodeficiency virus (HIV)-1 envelope glycoprotein gp160 into gp120 (HIV-1 SU) and gp41 (HIV-I TM). J Biol Chem. 1994; 269: 12240-12247.