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Evolutionary origins of the SARS-CoV-2 sarbecovirus lineage responsible for the COVID-19 pandemic
Open accessPublished version of a preprint
Abstract
There are outstanding evolutionary questions on the recent emergence of human coronavirus SARS-CoV-2 including the role of reservoir species, the role of recombination and its time of divergence from animal viruses. We find that the sarbecoviruses-the viral subgenus containing SARS-CoV and SARS-CoV-2-undergo frequent recombination and exhibit spatially structured genetic diversity on a regional scale in China. SARS-CoV-2 itself is not a recombinant of any sarbecoviruses detected to date, and its receptor-binding motif, important for specificity to human ACE2 receptors, appears to be an ancestral trait shared with bat viruses and not one acquired recently via recombination. To employ phylogenetic dating methods, recombinant regions of a 68-genome sarbecovirus alignment were removed with three independent methods. Bayesian evolutionary rate and divergence date estimates were shown to be consistent for these three approaches and for two different prior specifications of evolutionary rates based on HCoV-OC43 and MERS-CoV. Divergence dates between SARS-CoV-2 and the bat sarbecovirus reservoir were estimated as 1948 (95% highest posterior density (HPD): 1879-1999), 1969 (95% HPD: 1930-2000) and 1982 (95% HPD: 1948-2009), indicating that the lineage giving rise to SARS-CoV-2 has been circulating unnoticed in bats for decades.
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“Although the proximal origins are unknown, SARS-CoV-2 is thought to derive from a bat SARS-CoV-related coronavirus with a furin cleavage site that enhances the capacity of the virus to infect human cells.48, 49”
From The Lancet Commission on lessons for the future from the COVID-19 pandemic (2022) · cites this paper as [48]
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Meta-analysis to explain unknown causes of the origins of SARS-COV-2
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MethodImmunothrombosis in COVID-19: Implications of Neutrophil Extracellular Traps
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Lung Protection vs. Infection Resolution: Interleukin 10 Suspected of Double-Dealing in COVID-19
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BackgroundShould we discount the laboratory origin of COVID-19?
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“Consistent with other studies (Boni et al., 2020), our inferred substitution rate is 1.06 × 10− 3 (95 % Highest Posterior Density (HPD): 9.9× 10− 5 − 2.14× 10− 3) per site per year and the exponential growth rate of 41 in units of years, corresponding to a doubling time of around 6.14 (95 % HPD:…”
InfluentialShapiro, J. T., Víquez‐R, L., Leopardi, S., Vicente‐Santos, A., Mendenhall, I. H., Frick, W. F., Kading, R. C., Medellín, R. A., Racey, P. A., & Kingston, T. (2021) · Viruses · doi:10.3390/v13071356 · Cited by 43
“For example, increased Sarbecovirus (Genus: Betacoronavirus) sequence data from bats has demonstrated the diversity in this group [184] and why SARS-CoV-2 may have a wide host rage [185].”
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Indels in SARS-CoV-2 occur at template-switching hotspots
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Spatiotemporal spread pattern of the COVID-19 cases in China
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“The present evidence suggests that Orf8 is an evolutionary hot spot in the lineage (14, 15), confirmed by the comparison between SARS-CoV-2 and a pangolin strain: Orf7a exhibits 97.”
BackgroundResultRecombination and lineage-specific mutations linked to the emergence of SARS-CoV-2
Patiño-Galindo, J. Á., Filip, I., Chowdhury, R., Maranas, C. D., Sorger, P. K., AlQuraishi, M., & Rabadán, R. (2021) · Genome Medicine · doi:10.1186/s13073-021-00943-6 · Cited by 36
“occur along many regions of the genome [54].”
BackgroundResultEvolutionary remodelling of N‐terminal domain loops fine‐tunes SARS‐CoV‐2 spike
Cantoni, D. M., Murray, M. J., Kalemera, M. D., Dicken, S. J., Stejskal, L., Brown, G., Lytras, S., Coey, J. D., McKenna, J. P., Bridgett, S., et al. (2022) · EMBO Reports · doi:10.15252/embr.202154322 · Cited by 37
“…of the S2 0 cleavage site, allowing spike preprocessing by intracellular proteases, most notably furin, during virion assembly and release; this has been linked to efficient human-to-human transmission (Boni et al , 2020; Zhou et al , 2020; Hoffmann et al , 2020a; Peacock et al , 2021a, 2021b).”
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“229E and NL63, all from the family, and OC43 and HKU1 from the genus are the other forms of human coronavirus [40].”
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“4,6,8 However, when analyzing all non-re-combinant regions (NRRs), we will inevitably find some NRRs with older and some with younger MRCAs than either this estimate from a long fragment or an estimate based on the entire genome, which would effectively be a weighted average of NRR time of the MRCAs…”
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“Indeed, when more distantly related species were used to calibrate the estimation of evolutionary rates, substantially lower estimates were obtained (Boni et al. 2020).”
BackgroundResultInfluentialSpySwitch enables pH- or heat-responsive capture and release for plug-and-display nanoassembly
Vester, S. K., Rahikainen, R., Anuar, I. N. A. K., Hills, R. A., Tan, T. K., & Howarth, M. R. (2022) · Nature Communications · doi:10.1038/s41467-022-31193-8 · Cited by 35
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“However, the unique polybasic furin cleavage site in the SARS-CoV-2 S is not found in pangolin CoVs (42), and SARS-CoV-2 is not a recent recombinant involving any of the CoVs sampled to date (41,43,44).”
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“This is also what is known so far for COVID-19 (Poon et al., 2004; Boni et al., 2020; Ruiz-Aravena et al., 2022; Frutos et al., 2022).”
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“In sarbecoviruses, this was previously observed and related to the emergence of viruses with specific sequence features in the RBM [18,31].”
BackgroundResultInfluentialModular Evolution of Coronavirus Genomes
Vakulenko, Y. A., Deviatkin, A. A., Drexler, J. F., & Lukashev, A. N. (2021) · Viruses · doi:10.3390/v13071270 · Cited by 33
“Of course, this estimate should be used with care because distinct viruses might have different substitution rates [39], and at higher genetic distances saturation of substitutions and other mechanisms may lead to errors in molecular dating of several orders of magnitude [40].”
BackgroundSARS-CoV-2: tracing the origin, tracking the evolution
Voskarides, K. (2022) · BMC Medical Genomics · doi:10.1186/s12920-022-01208-w · Cited by 33
“2021, another team showed that SARSCoV-2 had been evolved long before the pandemic emergence, few decades back (95% HPD: 1930–2000) [20], considering RaTG13 as the closest virus to SARS-CoV-2.”
Conserved recombination patterns across coronavirus subgenera
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“This diversity likely contributes to the 67 viral diversity in bats [14,15], including some that have emerged as pathogenic in people 68 [16,17], such as sarbecoviruses [12].”
BackgroundMacLean, O. A., Lytras, S., Weaver, S., Singer, J. B., Boni, M. F., Lemey, P., Pond, S. L. K., & Robertson, D. L. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.05.28.122366 · Cited by 33
“We therefore separately tested each ORF of 69 Sarbecoviruses including SARS-CoV-2, SARS-CoV-1 and their close relatives (Supplementary table 2), and further separated the two longest ORFs, Orf1ab and Spike, into five putatively non-recombinant regions each, based on Boni et al. (2020) 7 .”
Self-citationAntigenic variation of SARS‐CoV‐2 in response to immune pressure
Forni, D., Cagliani, R., Pontremoli, C., Mozzi, A., Pozzoli, U., Clerici, M., & Sironi, M. (2020) · Molecular Ecology · doi:10.1111/mec.15730 · Cited by 30
Jacob-Dolan, C., Feldman, J. E., McMahan, K., Yu, J., Zahn, R. C., Wegmann, F., Schuitemaker, H., Schmidt, A. G., & Barouch, D. H. (2021) · Journal of Virology · doi:10.1128/jvi.00117-21 · Cited by 32
“Understanding serum responses to multiple CoVs will be necessary for future pandemic preparedness, prediction of responses to CoVs circulating in animal reservoirs, and the potential development of pancoronavirus vaccines (18, 40, 41).”
BackgroundSequencing of SARS-CoV-2 genome using different nanopore chemistries
González-Recio, Ó., Gutiérrez‐Rivas, M., Peiró‐Pastor, R., Aguilera‐Sepúlveda, P., Cano‐Gómez, C., Jiménez‐Clavero, M. Á., & Fernández-Piñero, J. (2021) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-021-11250-w · Cited by 30
“Both consensus reads belonged to the B1 linage (Boni et al. 2020), which carries the D614G mutation, which is thought to arise in Italy at the beginning of the pandemic in Europe, and spread across Europe and later overseas.”
BackgroundChaintoutis, S. C., Siarkou, V. I., Mylonakis, M. E., Kazakos, G. M., Skeva, P., Bampali, M., Dimitriou, M., Dovrolis, N., Polizopoulou, Z. S., Karakasiliοtis, I., et al. (2021) · Transboundary and Emerging Diseases · doi:10.1111/tbed.14132 · Cited by 31
Kumar, V., Parate, S., Yoon, S., Lee, G., & Lee, K. W. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.647295 · Cited by 33
Liu, X., Wen, J., Kozak, M., Jiang, Y., & Li, Z. (2021) · Tourism Review · doi:10.1108/tr-01-2021-0034 · Cited by 31
The importance of accessory protein variants in the pathogenicity of SARS-CoV-2
Hassan, S. S., Choudhury, P. P., Dayhoff, G. W., Aljabali, A. A. A., Uhal, B. D., Lundstrom, K. H., Rezaei, N., Pizzol, D., Adadi, P., Lal, A., et al. (2022) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2022.109124 · Cited by 38
“Among previously identified human coronaviruses (HCoVs), Severe Acute Respiratory Syndrome-Coronavirus (SARS-CoV) causing the SARS epidemic in 2002–2004 is the closest member to SARS-CoV-2 [2,3].”
Rationally designed immunogens enable immune focusing following SARS-CoV-2 spike imprinting
Hauser, B. M., Sangesland, M., Denis, K. S., Lam, E. C., Case, J. B., Windsor, I. W., Feldman, J. E., Caradonna, T. M., Kannegieter, T., Diamond, M., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110561 · Cited by 38
Understanding genomic diversity, pan-genome, and evolution of SARS-CoV-2
Parlikar, A., Kalia, K., Sinha, S., Patnaik, S., Sharma, N., Vemuri, S. G., & Sharma, G. (2020) · PeerJ · doi:10.7717/peerj.9576 · Cited by 30
“Viral genome sequencing and multiple sequence alignment of SARS-CoV-2 genomes have revealed its identity with Bat CoV RaTG13 (MN996532) and Pangolin-CoV (Cui, Li & Shi, 2019; Boni et al., 2020; Rehman et al., 2020).”
BackgroundMethodInfluentialAnimal coronaviruses in the light of COVID-19
Domańska-Blicharz, K., Woźniakowski, G., Konopka, B., Niemczuk, K., Welz, M., Rola, J., Socha, W., Orłowska, A., Antas, M., Śmietanka, K., et al. (2020) · Journal of Veterinary Research · doi:10.2478/jvetres-2020-0050 · Cited by 31
SARS-CoV-2: Zoonotic origin of pandemic coronavirus
Vilček, Š. (2020) · Acta Virologica · doi:10.4149/av_2020_302 · Cited by 29
“Divergence dates between SARS-CoV-2 and the bat sarbecovirus reservoir were estimated from 1948 to 1982, indicating that the lineage giving rise to SARS-CoV-2 has been circulating unnoticed in bats for decades (Boni et al., 2020).”
BackgroundOrigin, evolution and global spread of SARS-CoV-2
Zhukova, A., Blassel, L., Lemoine, F., Morel, M. H., Voznica, J., & Gascuel, O. (2020) · Comptes Rendus Biologies · doi:10.5802/crbiol.29 · Cited by 30
Ramazzotti, D., Angaroni, F., Maspero, D., Gambacorti-Passerini, C. B., Antoniotti, M., Graudenzi, A., & Piazza, R. (2021) · Patterns · doi:10.1016/j.patter.2021.100212 · Cited by 29
“In particular, it was hypothesized that SARS-CoV-2 might be a recombinant of an ancestor of Pangolin-CoV and Bat-CoV-RaTG13 [4, 75], whereas more recent findings would suggest that SARS-CoV-2 lineage is the consequence of a direct or indirect zoonotic jump from bats [74].”
Review of potential risk groups for coronavirus disease 2019 (COVID-19)
Naveed, M., Naeem, M., Rahman, M. U., Hilal, M. G., Kakakhel, M. A., Ali, G., & Hassan, A. (2021) · New Microbes and New Infections · doi:10.1016/j.nmni.2021.100849 · Cited by 34
“bats could be the possible primary reservoir for human coronavirus (CoV) [5,6].”
Hassanin, A., Tú, V. T., Curaudeau, M., & Csorba, G. (2021) · Scientific Reports · doi:10.1038/s41598-021-93738-z · Cited by 30
A review of current effective COVID-19 testing methods and quality control
Cheng, L., Lan, L., Ramalingam, M., He, J., Yang, Y., Gao, M., & Shi, Z. (2023) · Archives of Microbiology · doi:10.1007/s00203-023-03579-9 · Cited by 31
Dimonaco, N. J., Salavati, M., & Shih, B. B.-J. (2020) · Viruses · doi:10.3390/v13010049 · Cited by 29
“The relationship of SARS-CoV-2 to other SARS-like coronaviruses, the possible role of bats and pangolins as reservoir species and the role of recombination in its emergence are of great interest [9].”
Syal, S. (2021) · Journal of Urban Management · doi:10.1016/j.jum.2021.05.004 · Cited by 34
Design, immunogenicity, and efficacy of a pan-sarbecovirus dendritic-cell targeting vaccine
Coléon, S., Wiedemann, A., Surénaud, M., Lacabaratz, C., Hüe, S., Prague, M., Cervantes-Gonzalez, M., Wang, Z., Ellis, J., Sansoni, A., et al. (2022) · EBioMedicine · doi:10.1016/j.ebiom.2022.104062 · Cited by 29
A Tale of Three Recent Pandemics: Influenza, HIV and SARS-CoV-2
Miranda, M., Pingarilho, M., Pimentel, V., Torneri, A., Seabra, S. G., Libin, P., & Abecasis, A. B. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.889643 · Cited by 29
Saville, J. W., Berezuk, A., Srivastava, S. S., & Subramaniam, S. (2022) · Chemical Reviews · doi:10.1021/acs.chemrev.1c01062 · Cited by 32
The diversity of the glycan shield of sarbecoviruses related to SARS-CoV-2
Allen, J. D., Ivory, D. P., Song, G., He, W., Capozzola, T., Yong, P., Burton, D. R., Andrabi, R., & Crispin, M. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112307 · Cited by 32
“15 Viruses isolated from Rhinolophus sinicus , such as WIV-1-CoV and RsSHC014-CoV, have been shown to recognize human ACE2 and replicate efficiently in human primary airway epithelial cells, 16,17 highlighting the threat to human health that bat CoVs present.”
Neutralizing activity of Sputnik V vaccine sera against SARS-CoV-2 variantsPreprint
Ikegame, S., Siddiquey, M. N. A., Hung, C.-T., Haas, G. D., Brambilla, L., Oguntuyo, K. Y., Kowdle, S., Vilardo, A. E., Edelstein, A., Perandones, C., et al. (2021) · medRxiv · doi:10.1101/2021.03.31.21254660 · Cited by 30
Rapid characterization of a Delta-Omicron SARS-CoV-2 recombinant detected in EuropePreprint
Simon‐Lorière, E., Montagutelli, X., Lemoine, F., Donati, F., Touret, F., Bourret, J., Prot, M., Munier, S., Attia, M., Conquet, L., et al. (2022) · Research Square · doi:10.21203/rs.3.rs-1502293/v1 · Cited by 29
Sarbecovirus RBD indels and specific residues dictating multi-species ACE2 adaptiveness
Si, J.-Y., Chen, Y.-M., Sun, Y.-H., Gu, M.-X., Huang, M.-L., Shi, L.-L., Yu, X., Yang, X., Xiong, Q., Ma, C.-B., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-53029-3 · Cited by 25
“Sarbecov-iruses exhibit extensive genetic diversity in RBM, likely arising from frequent recombination and the high selective pressure associated with inter-species host jumping in bats and pangolins, underscoring the risks of the emergence and outbreak of new human sarbecovirus 19 – 23 .”
Detection of coronavirus in vampire bats (Desmodusrotundus) in southern Brazil
Alves, R. S., Olegário, J. D. C., Weber, M. N., da Silva, M. S., Canova, R., Sauthier, J. T., Baumbach, L. F., Witt, A. A., Varela, A. P. M., Mayer, F. Q., et al. (2021) · Transboundary and Emerging Diseases · doi:10.1111/tbed.14150 · Cited by 28
Evolution, Ecology, and Zoonotic Transmission of Betacoronaviruses: A Review
Jelinek, H. F., Mousa, M., Alefishat, E. A., Osman, W. M., Spence, I., Bu, D., Feng, S. F., Byrd, J. H., Magni, P. A., Sahibzada, S., et al. (2021) · Frontiers in Veterinary Science · doi:10.3389/fvets.2021.644414 · Cited by 28
“Thus, SARS-CoV-2 may have diverged from its ancestral bat sarbecovirus reservoir sometime between 1948 and 1982 and circulated in bats for some time (174).”
BackgroundLive animal markets: Identifying the origins of emerging infectious diseases
Galindo-González, J. R. (2021) · Current Opinion in Environmental Science & Health · doi:10.1016/j.coesh.2021.100310 · Cited by 30
A Glimpse on the Evolution of RNA Viruses: Implications and Lessons from SARS-CoV-2
Šimičić, P., & Lepej, S. Ž. (2022) · Viruses · doi:10.3390/v15010001 · Cited by 30
Evolutionary rate of SARS-CoV-2 increases during zoonotic infection of farmed mink
Porter, A. F., Purcell, D. F. J., Howden, B. P., & Duchêne, S. (2023) · Virus Evolution · doi:10.1093/ve/vead002 · Cited by 30
“CoV that circulate in the Chinese horseshoe bats (Rhinolophus affinis and Rhinolophus malayanus) are the closest known relatives to SARS-CoV-2 (although, with estimated divergence from SARS-CoV-2 between 1948 and 1982) (10-12).”
BackgroundA Critical Analysis of the Evidence for the SARS-CoV-2 Origin Hypotheses
Alwine, J. C., Casadevall, A., Enquist, L. W., Goodrum, F. D., & Imperiale, M. J. (2023) · Journal of Virology · doi:10.1128/jvi.00365-23 · Cited by 31
“245 Recombination within the Sarbecovirus subgenus to which SARS-CoV-2 belongs 246 is exceedingly common (18, 22, 23).”
BackgroundShooting at a Moving Target—Effectiveness and Emerging Challenges for SARS-CoV-2 Vaccine Development
Günl, F., Mecate-Zambrano, A., Rehländer, S., Hinse, S., Ludwig, S., & Brunotte, L. (2021) · Vaccines · doi:10.3390/vaccines9101052 · Cited by 27
The adaptation of SARS-CoV-2 to humans
Tosta, E. (2021) · Memórias do Instituto Oswaldo Cruz · doi:10.1590/0074-02760210127 · Cited by 27
“(13) Phylogenetic comparative analyses of bat SARSr-CoV and SARS-CoV-2 estimate that they shared a most recent common ancestor approximately 40-50 years ago, indicating that the lineage giving rise to SARS-CoV-2 has been circulating unnoticed in bats for decades.(14,15) It is estimated that more than two-thirds of SAR…”
Jermiin, L. S., Catullo, R. A., & Holland, B. R. (2020) · NAR Genomics and Bioinformatics · doi:10.1093/nargab/lqaa041 · Cited by 27
“Science Provide accurate estimates of the evolution of, for example, species (1-4) Provide accurate estimates of evolutionary processes at the molecular level (5,6) Addressing macroevolutionary questions pertaining to birds and mammals (7,8) Understand biogeographic patterns and diversity (9,10) Reconstruction of ance…”
BackgroundAn Early Pandemic Analysis of SARS-CoV-2 Population Structure and Dynamics in Arizona
Ladner, J. T., Larsen, B. B., Bowers, J. R., Hepp, C. M., Bolyen, E. K., Folkerts, M., Sheridan, K. L., Pfeiffer, A., Yaglom, H. D., Lemmer, D., et al. (2020) · mBio · doi:10.1128/mbio.02107-20 · Cited by 27
“In late 2019, a novel positive-sense RNA virus, family Coronaviridae, genus Betacoronavirus, and subgenus Sarbecovirus, emerged in the human population due to cross-species transmission from an unknown host (1, 2).”
Boeger, W. A., Brooks, D. R., Trivellone, V., Agosta, S. J., & Hoberg, E. P. (2022) · Transboundary and Emerging Diseases · doi:10.1111/tbed.14557 · Cited by 27
Ghosh, S. B., Al-Sharify, Z. T., Maleka, M. F., Onyeaka, H. N., Maleke, M., Maolloum, A., Godoy, L., Meskini, M., Rami, M. R., Ahmadi, S., et al. (2022) · Environmental Science and Pollution Research · doi:10.1007/s11356-022-21652-6 · Cited by 30
Bat-Associated Microbes: Opportunities and Perils, An Overview
Dhivahar, J., Parthasarathy, A., Krishnan, K., Kovi, B. S., & Pandian, G. N. (2022) · Heliyon · doi:10.1016/j.heliyon.2023.e22351 · Cited by 28
“A recent analysis of the Sarbeco virus lineage, which contains SARS and SARS-CoV-2, showed that those two branches undergo frequent recombination [297].”
BackgroundMethodNeutralizing activity of Sputnik V vaccine sera against SARS-CoV-2 variantsPreprint
Ikegame, S., Siddiquey, M. N. A., Hung, C.-T., Haas, G. D., Brambilla, L., Oguntuyo, K. Y., Kowdle, S., Vilardo, A. E., Edelstein, A., Perandones, C., et al. (2021) · Research Square · doi:10.21203/rs.3.rs-400230/v1 · Cited by 27
The first three waves of the Covid-19 pandemic hint at a limited genetic repertoire for SARS-CoV-2
Wassenaar, T. M., Wanchai, V., Buzard, G. S., & Ussery, D. W. (2022) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuac003 · Cited by 29
Fenton, M. B., Mubareka, S., Tsang, S. M., Simmons, N. B., & Becker, D. J. (2020) · FACETS · doi:10.1139/facets-2020-0028 · Cited by 26
Crippling life support for SARS-CoV-2 and other viruses through synthetic lethality
Mast, F. D., Navare, A., van der Sloot, A. M., Coulombe‐Huntington, J., Rout, M. P., Baliga, N. S., Kaushansky, A., Chait, B. T., Aderem, A. A., Rice, C. M., et al. (2020) · The Journal of Cell Biology · doi:10.1083/jcb.202006159 · Cited by 25
Metadata
- Authors
- Boni, M. F., Lemey, P., Jiang, X., Lam, T. T.-Y., Perry, B. W., Castoe, T. A., Rambaut, A., & Robertson, D. L.
- Affiliations
- Pennsylvania State University (US)
- KU Leuven (BE)
- Xi’an Jiaotong-Liverpool University (CN)
- University of Hong Kong (HK)
- The University of Texas at Arlington (US)
- University of Edinburgh (GB)
- MRC University of Glasgow Centre for Virus Research (GB)
- Corresponding author
- Boni, Maciej F.
- Lemey, Philippe
- Rambaut, Andrew
- Robertson, David L.
- ORCID
- Venue
- Nature Microbiology
- Published
- 2020-07-28
- Volume
- 5
- Issue
- 11
- Pages
- 1408-1417
- ISSN
- 2058-5276 (ISSN-L)
- OpenAlex
- W3046218112
- Cited by
- 1,014
- References
- 69
- Citations by year
- 2026: 23 · 2025: 46 · 2024: 79 · 2023: 118 · 2022: 240 · 2021: 327 · 2020: 178
- FWCI
- 28.54
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Nature Microbiology (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc)
- PubMed (publishedVersion)
- ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (submittedVersion, cc-by-sa)
- Lirias (KU Leuven) (submittedVersion)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, other-oa)
- Funders
- Fonds Wetenschappelijk Onderzoek (G0D5117N, G0B9317N)
- Wellcome Trust (206298/Z/17/Z)
- RCUK | Medical Research Council (MC_UU_1201412)
- Topics
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Virus Infections Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Keywords
- SARS-CoV-2, sarbecoviruses, COVID-19 pandemic, viral recombination, bat reservoirs, pangolins, divergence time estimation, receptor-binding motif, ACE2 receptor, phylogenetic dating, viral emergence, genetic diversity, SARS-CoV
- MeSH terms
- Betacoronavirus, Angiotensin-Converting Enzyme 2, COVID-19, SARS-CoV-2, Animals, Bayes Theorem, China, Chiroptera, Humans, Peptidyl-Dipeptidase A, Phylogeny, Pneumonia, Viral, Recombination, Genetic, Genetic Variation, Genome, Viral, Coronavirus Infections, Evolution, Molecular, Pandemics
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