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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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Citations
Cites
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
Stamatakis, A. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btu033 · Cited by 32,291 · cited 2×
“2.8 (Stamatakis, 2014, 2006), GTR+Γ model, 100 bootstrap replicates – was inferred for each BFR longer than 500nt.”
BackgroundMethodInfluentialIQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies
Nguyen, L.-T., Schmidt, H. A., von Haeseler, A., & Minh, B. Q. (2015) · Molecular Biology and Evolution · doi:10.1093/molbev/msu300 · Cited by 26,046 · cited 1×
“The latter was reconstructed using IQTREE (Nguyen et al., 2014 ) under a General-Time Reversible (GTR) model with a discrete gamma distribution to model among-site rate variation.”
MethodA pneumonia outbreak associated with a new coronavirus of probable bat origin
Zhou, P., Yang, X.-L., Wang, X.-G., Hu, B., Zhang, L., Zhang, W., Si, H.-R., Zhu, Y., Li, B., Huang, C.-L., et al. (2020) · Nature · doi:10.1038/s41586-020-2012-7 · Cited by 21,969 · cited 11×
“…thought to be instrumental to SARS-CoV-2’s ability to infect humans – a polybasic cleavage site insertion in the Spike protein – has been seen in another close bat relative of the SARS-CoV-2 virus (Zhou et al., 2020a); however, the sequence is different and it is likely an independent event.”
BackgroundInfluentialEarly transmission dynamics in Wuhan, China, of novel coronavirus-infected pneumonia
Li, Q., Guan, X., Wu, P., Wang, X., Zhou, L., Tong, Y., Ren, R., Leung, K. S. M., Lau, E. H. Y., Wong, J. Y., et al. (2020) · New England Journal of Medicine · doi:10.1056/nejmoa2001316 · Cited by 16,575 · cited 8×
“In December 2019, a cluster of pneumonia cases epidemiologically linked to an open-air wet market in city of Wuhan (Hubei Province), China (Li et al., 2020a; Zhou et al., 2020b) led local health officials to issue an epidemiological alert to the Chinese Center for Disease Control and Prevention…”
BackgroundMethodInfluentialSelf-citationRAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models
Stamatakis, A. (2006) · Bioinformatics · doi:10.1093/bioinformatics/btl446 · Cited by 15,582 · cited 2×
“2.8 (Stamatakis, 2014, 2006), GTR+Γ model, 100 bootstrap replicates – was inferred for each BFR longer than 500nt.”
BackgroundMethodInfluentialLu, R., Zhao, X., Li, J., Niu, P., Yang, B., Wu, H., Wang, W., Song, H., Huang, B., Zhu, N., et al. (2020) · The Lancet · doi:10.1016/s0140-6736(20)30251-8 · Cited by 11,907 · cited 4×
“Across a large region of its genome, corresponding approximately to ORF1b , it did not cluster with any of the known bat coronaviruses indicating that recombination likely played a role in the evolutionary history of these viruses (Lu et al., 2020; Wu et al.”
BackgroundInfluentialA new coronavirus associated with human respiratory disease in China
Wu, F., Zhao, S., Yu, B., Chen, Y.-M., Wang, W., Song, Z.-G., Hu, Y., Tao, Z.-W., Tian, J.-H., Pei, Y.-Y., et al. (2020) · Nature · doi:10.1038/s41586-020-2008-3 · Cited by 11,688 · cited 4×
“When the first genome sequence of SARS-CoV-2, Wuhan-Hu-1, was released on January 10 2020 on Virological.org by a consortium led by Yong-Zhen Zhang (Wu et al., 2020a) it enabled the immediate analyses of its ancestry.”
BackgroundMethodInfluentialGorbalenya, A. E., Baker, S. C., Baric, R. S., de Groot, R. J., Drosten, C., Gulyaeva, A. A., Haagmans, B. L., Lauber, C., Leontovich, A. M., Neuman, B. W., et al. (2020) · Nature Microbiology · doi:10.1038/s41564-020-0695-z · Cited by 8,745 · cited 3×
“Next, we (1) collected all breakpoints into a single set, (2) complemented this set to generate a set of non-breakpoints, (3) grouped non-breakpoints into contiguous BFRs and (4) sorted these regions by length.”
BackgroundMethodThe proximal origin of SARS-CoV-2
Andersen, K. G., Rambaut, A., Lipkin, W. I., Holmes, E. C., & Garry, R. F. (2020) · Nature Medicine · doi:10.1038/s41591-020-0820-9 · Cited by 5,081 · cited 3×
“Influenza viruses reassort (Webster et al., 1992) but they do not undergo homologous recombination within RNA segments (Boni et al., 2008, 2010), meaning that ‘origins’ questions for influenza outbreaks can always be reduced to origins questions for each of influenza’s eight RNA segments.”
BackgroundMethodSelf-citationEvolution and ecology of influenza A viruses
Webster, R. G., Bean, W. J., Gorman, O. T., Chambers, T. M., & Kawaoka, Y. (1992) · Microbiological Reviews · doi:10.1128/mr.56.1.152-179.1992 · Cited by 4,739
Cited by
Sorted by citations
Items 101–200 of 997
Townsend, J. P., Hassler, H. B., Sah, P., Galvani, A. P., & Dornburg, A. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2204336119 · Cited by 85
“We also repeated these phylogenetic analyses using nonrecombining blocks of sequence (29) that were realigned and analyzed using the methods identified above.”
MethodPeacock, T. P., Goldhill, D. H., Zhou, J., Baillon, L., Frise, R., Swann, O. C., Kugathasan, R., Penn, R., Brown, J. C., Sanchez-David, R. Y., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.09.30.318311 · Cited by 88
“This polybasic CS is absent from the closest relatives of SARS-CoV-2, such as SARS-CoV, although similar polybasic CS are found in more distantly related coronaviruses (Andersen, Rambaut, Lipkin, Holmes, & Garry, 2020; Boni et al., 2020; Le Coupanec et al., 2015).”
BackgroundWrobel, A. G., Benton, D. J., Xu, P., Calder, L. J., Borg, A., Roustan, C., Martin, S. R., Rosenthal, P. B., Skehel, J. J., & Gamblin, S. J. (2021) · Nature Communications · doi:10.1038/s41467-021-21006-9 · Cited by 85
“There are conflicting reports on whether the RBD of Pangolin-CoV S, while very similar in sequence to the RBD of the current pandemic virus, is the immediate precursor to the SARS-CoV-2 RBD 18,19 .”
BackgroundAntiviral performance of graphene-based materials with emphasis on COVID-19: A review
Seifi, T., & Kamali, A. R. (2021) · Medicine in Drug Discovery · doi:10.1016/j.medidd.2021.100099 · Cited by 87
“transmembrane protein on the cell surface [24,25].”
Synonymous mutations and the molecular evolution of SARS-CoV-2 origins
Wang, H., Pipes, L., & Nielsen, R. (2020) · Virus Evolution · doi:10.1093/ve/veaa098 · Cited by 83
Coinfection by influenza A virus and respiratory syncytial virus produces hybrid virus particles
Haney, J., Víjayakríshnan, S., Streetley, J., Dee, K., Goldfarb, D. M., Clarke, M., Mullin, M., Carter, S. D., Bhella, D., & Murcia, P. R. (2022) · Nature Microbiology · doi:10.1038/s41564-022-01242-5 · Cited by 83
Halawa, S., Pullamsetti, S. S., Bangham, C. R. M., Stenmark, K. R., Dorfmüller, P., Frid, M. G., BUTROUS, G. S., Morrell, N. W., Pérez, V. D. J., Stuart, D. I., et al. (2021) · Nature Reviews Cardiology · doi:10.1038/s41569-021-00640-2 · Cited by 84
Sarbecovirus ORF6 proteins hamper induction of interferon signaling
Kimura, I., Konno, Y., Uriu, K., Hopfensperger, K., Sauter, D., Nakagawa, S., & Sato, K. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.108916 · Cited by 84
“The inconsistent phylogenetic topologies of different viral genes of sarbecoviruses (Figure 1B) are in agreement with recent studies suggesting gene recombination events among sarbecoviruses (Boni et al., 2020; Li et al., 2020b).”
Structural basis for continued antibody evasion by the SARS-CoV-2 receptor binding domain
Smith, K. N., Clark, S. A., Shankar, S., Pan, J., Clark, L. E., Yang, P., Coscia, A., McKay, L. G. A., Varnum, H., Brusic, V., et al. (2022) · Science · doi:10.1126/science.abl6251 · Cited by 77
“RaTG13 virus, which is closely related to SARS-CoV-2 phylogenetically, is one example (63).”
BackgroundRotondo, J. C., Martini, F., Maritati, M., Mazziotta, C., Mauro, G. D., Lanzillotti, C., Barp, N., Gallerani, A., Tognon, M. G., & Contini, C. (2021) · Viruses · doi:10.3390/v13091687 · Cited by 81
Unraveling the Zoonotic Origin and Transmission of SARS-CoV-2
Banerjee, A., Doxey, A. C., Mossman, K. L., & Irving, A. T. (2020) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2020.12.002 · Cited by 77
A single-dose mRNA vaccine provides a long-term protection for hACE2 transgenic mice from SARS-CoV-2
Huang, Q., Ji, K., Tian, S., Wang, F., Huang, B., Tong, Z., Tan, S., Hao, J., Wang, Q., Tan, W., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-21037-2 · Cited by 79
Maximum likelihood pandemic-scale phylogenetics
Maio, N. D., Kalaghatgi, P., Turakhia, Y., Corbett-Detig, R. B., Minh, B. Q., & Goldman, N. (2023) · Nature Genetics · doi:10.1038/s41588-023-01368-0 · Cited by 72
“Genomic data plays an essential role in the study of transmissible disease, as exemplified by its current use in identifying and tracking the spread of novel SARS-CoV-2 variants.”
The coronavirus recombination pathway
Wells, H., Bonavita, C. M., Navarrete‐Macias, I., Vilchez, B., Rasmussen, A. L., & Anthony, S. J. (2023) · Cell Host & Microbe · doi:10.1016/j.chom.2023.05.003 · Cited by 75
“Given that the recombinogenicity of sarbecoviruses is already well established, 57,61,96,117,146 there is extremely strong evidence supporting that continued sarbecovirus surveillance in and around this region of Southeast Asia is critical.”
BackgroundInfluentialRole of genomics in combating COVID-19 pandemic
Saravanan, K. A., Panigrahi, M., Kumar, H., Rajawat, D., Nayak, S. S., Bhushan, B., & Dutt, T. (2022) · Gene · doi:10.1016/j.gene.2022.146387 · Cited by 81
Seasonality of endemic COVID-19
Townsend, J. P., Lamb, A. D., Hassler, H. B., Sah, P., Nishio, A. A., Nguyen, C., Tew, A. D., Galvani, A. P., & Dornburg, A. (2023) · mBio · doi:10.1128/mbio.01426-23 · Cited by 83
“Results were robust to a potential history of recombination among or within genes through phylogenetic analyses using an alignment of the putative non-recombining blocks (38).”
BackgroundKumar, S., Tao, Q., Weaver, S., Sanderford, M. D., Caraballo‐Ortiz, M. A., Sharma, S., Pond, S. L. K., & Miura, S. (2021) · Molecular Biology and Evolution · doi:10.1093/molbev/msab118 · Cited by 69
A novel SARS-CoV-2 related coronavirus in bats from CambodiaPreprint
Hul, V., Delaune, D., Karlsson, E. A., Hassanin, A., Ou, T. P., Baidaliuk, A., Gámbaro, F., Tú, V. T., Keatts, L., Mazet, J. A. K., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.01.26.428212 · Cited by 73
The Recovery, Interpretation and Use of Ancient Pathogen Genomes
Duchêne, S., Ho, S. Y. W., Carmichael, A. G., Holmes, E. C., & Poinar, H. N. (2020) · Current Biology · doi:10.1016/j.cub.2020.08.081 · Cited by 73
Phylogenetic supertree reveals detailed evolution of SARS-CoV-2
Li, T., Liu, D., Yang, Y., Guo, J., Feng, Y., Zhang, X., Cheng, S., & Feng, J. (2020) · Scientific Reports · doi:10.1038/s41598-020-79484-8 · Cited by 74
Chakraborty, C., Bhattacharya, M., Sharma, A. R., & Mallik, B. (2022) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2022.07.254 · Cited by 74
“Some studies have been performed to understand the association between the geographical location and the origin of SARS-CoV-2 variants [4-6].”
BackgroundSARS-like Coronaviruses in Horseshoe Bats (Rhinolophus spp.) in Russia, 2020
Alkhovsky, S. V., Lenshin, S. V., Romashin, A. V., Владимировна, В. Т., Vyshemirsky, O. I., Bulycheva, Y. I., Dk, L., & Gitelman, A. K. (2022) · Viruses · doi:10.3390/v14010113 · Cited by 71
Coronaviruses in humans and animals: the role of bats in viral evolution
El-Sayed, A., & Kamel, M. S. (2021) · Environmental Science and Pollution Research · doi:10.1007/s11356-021-12553-1 · Cited by 69
An ACE2-dependent Sarbecovirus in Russian bats is resistant to SARS-CoV-2 vaccines
Seifert, S. N., Bai, S., Fawcett, S., Norton, E. B., Zwezdaryk, K. J., Robinson, J. E., Gunn, B. M., & Letko, M. C. (2022) · PLoS Pathogens · doi:10.1371/journal.ppat.1010828 · Cited by 63
“However, sarbecovirus recombination in nature typically occurs via template switching resulting in acquisition of regions larger than the NTD (28).”
BackgroundMakarenkov, V., Mazoure, B., Rabusseau, G., & Legendre, P. (2021) · BMC Ecology and Evolution · doi:10.1186/s12862-020-01732-2 · Cited by 67
Yi, C., Sun, X., Lin, Y., Gu, C., Ding, L., Lü, X., Yang, Z., Zhang, Y., Ma, L., Gu, W., et al. (2021) · Genome Medicine · doi:10.1186/s13073-021-00985-w · Cited by 74
Can, H., Köseoğlu, A. E., Alak, S. E., Güvendi, M., Döşkaya, M., Karakavuk, M., Gürüz, A. Y., & Ün, C. (2020) · Scientific Reports · doi:10.1038/s41598-020-79645-9 · Cited by 66
Ijaz, M. K., Nims, R. W., Zhou, S. S., Whitehead, K., Srinivasan, V., Kapes, T., Fanuel, S., Epstein, J. H., Daszak, P., Rubino, J. R., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-84842-1 · Cited by 67
One year into the pandemic: Short-term evolution of SARS-CoV-2 and emergence of new lineages
Gónzález‐Candelas, F., Shaw, M., Phan, T. G., Kulkarni‐Kale, U., Paraskevis, D. N., Luciani, F., Kimura, H., & Sironi, M. (2021) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2021.104869 · Cited by 65
Elrashdy, F., Redwan, E. M. M. M., & Uversky, V. N. (2020) · Biomolecules · doi:10.3390/biom10091312 · Cited by 64
“It was also pointed out that not all pets are equally susceptible to SARS-CoV-2, with chimpanzees and monkeys being the most sensitive to this infection, and with mice being shown to be the least susceptible to SARS-CoV-2 [178,191].”
Characterizing Transcriptional Regulatory Sequences in Coronaviruses and Their Role in Recombination
Yang, Y., Yan, W., Hall, A. B., & Jiang, X. (2020) · Molecular Biology and Evolution · doi:10.1093/molbev/msaa281 · Cited by 64
Self-citationHall, J. S., Knowles, S., Nashold, S. W., Ip, H. S., Leon, A. E., Rocke, T. E., Keller, S., Carossino, M., Balasuriya, U. B. R., & Hofmeister, E. K. (2020) · Transboundary and Emerging Diseases · doi:10.1111/tbed.13949 · Cited by 64
Retrieval and Investigation of Data on SARS-CoV-2 and COVID-19 Using Bioinformatics Approach
Fahmi, M., Kharisma, V. D., Ansori, A. N. M., & Ito, M. (2021) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-63761-3_47 · Cited by 65
Ghafari, M., Peter Simmonds, K., Pybus, O. G., & Katzourakis, A. (2021) · Current Biology · doi:10.1016/j.cub.2021.08.020 · Cited by 64
The Ecology of Viral Emergence
Holmes, E. C. (2022) · Annual Review of Virology · doi:10.1146/annurev-virology-100120-015057 · Cited by 65
Wú, Z., Han, Y., Wang, Y., Liu, B., Zhao, L., Zhang, J., Su, H., Zhao, W., Liu, L., Bai, S., et al. (2022) · National Science Review · doi:10.1093/nsr/nwac213 · Cited by 64
“However, whether these bat and pangolin species could serve as the direct natural reservoirs and intermediate hosts for SARSCoV-2, respectively, remains elusive because of remaining genome differences [24].”
BackgroundZoonotic and Reverse Zoonotic Transmissibility of SARS-CoV-2
Goraichuk, I. V., Arefiev, V. L., Stegniy, B. Т., & Gerilovych, A. (2021) · Virus Research · doi:10.1016/j.virusres.2021.198473 · Cited by 66
A Bayesian approach to infer recombination patterns in coronaviruses
Müller, N. F., Kistler, K. E., & Bedford, T. (2022) · Nature Communications · doi:10.1038/s41467-022-31749-8 · Cited by 63
Recombination events are concentrated in the spike protein region of Betacoronaviruses
Bobay, L., O’Donnell, A. C., & Ochman, H. (2020) · PLoS Genetics · doi:10.1371/journal.pgen.1009272 · Cited by 60
“A more probable scenario is that it resulted from a combination of earlier recombination events and accumulated mutations [8,9,35,37].”
BackgroundResultUnlocking capacities of genomics for the COVID-19 response and future pandemics
Knyazev, S., Chhugani, K., Sarwal, V., Ayyala, R., Singh, H., Karthikeyan, S., Deshpande, D., Baykal, P. I., Comarova, Z., Lu, A., et al. (2022) · Nature Methods · doi:10.1038/s41592-022-01444-z · Cited by 61
Self-citationRecombination in Positive-Strand RNA Viruses
Wang, H., Cui, X., Cai, X., & An, T. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.870759 · Cited by 70
Choosing a cellular model to study SARS-CoV-2
de Souza, G. A. P., Bideau, M. L., Boschi, C., Wurtz, N., Colson, P., Aherfi, S., Devaux, C. A., & Scola, B. L. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.1003608 · Cited by 63
“Although much could be inferred from what had been discovered for SARS-CoV and MERS-CoV (Boni et al., 2020; Zhou et al., 2021b), significant doubts remained about the particularities of SARS-CoV-2, including the most suitable cellular models for studying the new coronavirus.”
BackgroundInfluentialHalabowski, D., & Rzymski, P. (2020) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2020.143723 · Cited by 66
Secretory Vesicles Are the Principal Means of SARS-CoV-2 Egress
Eymieux, S., Uzbekov, R. E., Rouillé, Y., Blanchard, E., Hourioux, C., Dubuisson, J., Belouzard, S., & Roingeard, P. (2021) · Cells · doi:10.3390/cells10082047 · Cited by 61
Wahba, L., Jain, N., Fire, A. Z., Shoura, M. J., Artiles, K. L., McCoy, M. J., & Jeong, D. (2020) · mSphere · doi:10.1128/msphere.00160-20 · Cited by 86
COVID-19 Lung Pathogenesis in SARS-CoV-2 Autopsy Cases
Valdebenito, S., Bessis, S., Annane, D., de la Grandmaison, G. L., Cramer, E. M., Prideaux, B., Eugenín, E. A., & Bomsel, M. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.735922 · Cited by 61
Transmission of SARS-CoV-2 from humans to animals and potential host adaptationPreprint
Tan, C. C. S., Lam, S. D., Richard, D., Owen, C. J., Berchtold, D., Orengo, C. A., Nair, M. S., Kuchipudi, S. V., Kapur, V., van Dorp, L., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.11.16.384743 · Cited by 62
Interferon induction, evasion, and paradoxical roles during SARS‐CoV‐2 infection*
Chiale, C., Greene, T. T., & Zúñiga, E. I. (2022) · Immunological Reviews · doi:10.1111/imr.13113 · Cited by 66
Nikolaidis, M., Papakyriakou, A., Chlichlia, K., Markoulatos, P., Oliver, S. G., & Amoutzias, G. D. (2022) · Viruses · doi:10.3390/v14040707 · Cited by 57
“Within the first year of the pandemic, SARS-CoV-2 displayed a slightly higher mutation rate than SARS-CoV-1, MERS-CoV (a beta-genus Merbecovirus) or HCoV-OC43 (a betagenus Embecovirus); however, it did not undergo phenotypically significant mutational changes [20,21].”
BackgroundResultInfluentialFeng, Y., Yuan, M., Powers, J. M., Hu, M., Munt, J. E., Arunachalam, P. S., Leist, S. R., Bellusci, L., Kim, J., Sprouse, K. R., et al. (2023) · Science Translational Medicine · doi:10.1126/scitranslmed.adg7404 · Cited by 58
“…and the potential for zoonotic coronaviruses such as SARS-CoV and MERS-CoV, as well as bat coronaviruses like WIV-1, RaTG13, and SHC014 (2, 3, 33, 50-54), to spill-over into humans, considerable effort is focused on identifying broadly neutralizing antibodies able to cross-neutralize various…”
BackgroundTo stop the next pandemic, we need to unravel the origins of COVID-19
Relman, D. A. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2021133117 · Cited by 56
Contribution of Syndecans to the Cellular Entry of SARS-CoV-2
Hudák, A., Letoha, A., Szilák, L., & Letoha, T. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22105336 · Cited by 56
“Endocytic uptake of monomeric amyloid- beta peptides is clathrin- and dynamin-independent and results in selective accumulation of Abeta(1-42) compared to Abeta(1-40).”
BackgroundThe evolutionary dynamics of endemic human coronaviruses
Jo, W. K., Drosten, C., & Drexler, J. F. (2021) · Virus Evolution · doi:10.1093/ve/veab020 · Cited by 60
SARS-CoV-2 and influenza: a comparative overview and treatment implications
Manzanares, L. D., & Contreras, O. M. (2020) · Boletín Médico del Hospital Infantil de México · doi:10.24875/bmhim.20000183 · Cited by 64
Tomaszewski, T., DeVries, R. S., Dong, M., Bhatia, G., Norsworthy, M. D., Zheng, X., & Caetano‐Anollés, G. (2020) · Evolutionary Bioinformatics · doi:10.1177/1176934320965149 · Cited by 57
Understanding the Origin of COVID-19 Requires to Change the Paradigm on Zoonotic Emergence
Frutos, R., Gavotte, L., & Devaux, C. A. (2020) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2021.104812 · Cited by 61
Behl, A., Nair, A., Mohagaonkar, S., Yadav, P., Gambhir, K., Tyagi, N., Sharma, R. K., Butola, B. S., & Sharma, N. (2022) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2022.105217 · Cited by 58
Assessing Uncertainty in the Rooting of the SARS-CoV-2 Phylogeny
Pipes, L., Wang, H., Huelsenbeck, J. P., & Nielsen, R. (2020) · Molecular Biology and Evolution · doi:10.1093/molbev/msaa316 · Cited by 55
Hoque, M. N., Chaudhury, A., Akanda, M. A. M., Hossain, M. A., & Islam, T. (2020) · PeerJ · doi:10.7717/peerj.9689 · Cited by 53
Gallaher, W. R. (2020) · Archives of Virology · doi:10.1007/s00705-020-04750-z · Cited by 58
“[25] identify as a breakpointfree region.”
BackgroundInfluentialBioinformatics resources for SARS-CoV-2 discovery and surveillance
Hu, T., Li, J., Zhou, H., Li, C., Holmes, E. C., & Shi, W. (2020) · Briefings in Bioinformatics · doi:10.1093/bib/bbaa386 · Cited by 57
Bats, pangolins, minks and other animals - villains or victims of SARS-CoV-2?
do Vale, B., Lopes, A. P., Fontes, M. D. C., Silvestre, A. M., Cardoso, L., & Coelho, A. C. (2021) · Veterinary Research Communications · doi:10.1007/s11259-021-09787-2 · Cited by 55
Berrío, A., Gartner, V., & Wray, G. A. (2020) · PeerJ · doi:10.7717/peerj.10234 · Cited by 51
From quantum‐derived principles underlying cysteine reactivity to combating the COVID ‐19 pandemic
Mazmanian, K., Chen, T., Sargsyan, K., & Lim, C. (2022) · Wiley Interdisciplinary Reviews Computational Molecular Science · doi:10.1002/wcms.1607 · Cited by 53
“SARS-CoV-2 shows the highest conservation in regions encoding the viral targets revealed herein.(131) This suggests the possibility of targeting the multiple conserved reactive free/Zn-bound Cys in emergent coronavirus pathogens indispensable for the coronavirus replication using a cocktail of Zn-ejecting drugs and ot…”
BackgroundA review on favipiravir: the properties, function, and usefulness to treat COVID-19
Hashemian, S. M. R., Farhadi, T., & Velayati, A. A. (2020) · Expert Review of Anti-infective Therapy · doi:10.1080/14787210.2021.1866545 · Cited by 53
Development of a large volume concentration method for recovery of coronavirus from wastewater
McMinn, B. R., Korajkic, A., Kelleher, J., Herrmann, M. P., Pemberton, A. C., Ahmed, W., Villegas, E. N., & Oshima, K. H. (2021) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2021.145727 · Cited by 52
Emergence and widespread circulation of a recombinant SARS-CoV-2 lineage in North America
Gutiérrez, B., Castelán-Sánchez, H. G., Cândido, D. D. S., Jackson, B., Fleishon, S., Houzet, R., Ruis, C., Delaye, L., Faria, N. R., Rambaut, A., et al. (2022) · Cell Host & Microbe · doi:10.1016/j.chom.2022.06.010 · Cited by 55
Self-citationDharmarajan, G., Li, R., Chanda, E., Dean, K. R., Dirzo, R., Jakobsen, K. S., Khan, I., Leirs, H., Shi, Z., WOLFE, N. D., et al. (2022) · Zoonoses · doi:10.15212/zoonoses-2021-0028 · Cited by 57
“Although SARS-CoV-2 itself does not appear to be a recombinant of any currently known sarbecoviruses [98], coronaviruses generally do show high recombination rates [99], and such viral recombination can increase the risk of emergence of novel zoonotic pathogens.”
BackgroundSARS-CoV-2 evolution influences GBP and IFITM sensitivity
Mesner, D., Reuschl, A., Whelan, M. V. X., Bronzovich, T., Haider, T., Thorne, L., Ragazzini, R., Bonfanti, P., Towers, G. J., & Jolly, C. L. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2212577120 · Cited by 54
“The polybasic furin cleavage site (FCS) Arg–Arg–Ala–Arg (or RRAR) motif that is targeted by furin is absent in closely related coronaviruses, including the closest relatives of SARS-CoV-2, bat RaTG13 and pangolin CoV (2, 4, 5).”
Tan, C. C. S., Owen, C. J., Tham, C. Y. L., Bertoletti, A., van Dorp, L., & Balloux, F. (2021) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2021.105075 · Cited by 54
An antibody class with a common CDRH3 motif broadly neutralizes sarbecoviruses
Liu, L., Iketani, S., Guo, Y., Reddem, E. R., Casner, R. G., Nair, M. S., Yu, J., Chan, J. F., Wang, M., Cerutti, G., et al. (2022) · Science Translational Medicine · doi:10.1126/scitranslmed.abn6859 · Cited by 51
Spratt, A. N., Gallazzi, F., Quinn, T. P., Lorson, C. L., Sönnerborg, A. B., & Singh, K. D. (2021) · Expert Opinion on Therapeutic Patents · doi:10.1080/13543776.2021.1884224 · Cited by 50
Goldstein, S. A., Brown, J., Pedersen, B. S., Quinlan, A. R., & Elde, N. C. (2022) · Genome Biology and Evolution · doi:10.1093/gbe/evac161 · Cited by 53
Ferri, M., & Lloyd-Evans, M. (2021) · One Health · doi:10.1016/j.onehlt.2021.100230 · Cited by 52
“The 4% genetic differences between RaTG13 and SARS-CoV-2 represent 40 – 70 years of mutation, at the rate generally found in coronaviruses, suggesting that the common ancestor dates back to about 1948 – 1982 [39].”
SARS-CoV-2 accessory protein ORF8 is secreted extracellularly as a glycoprotein homodimer
Matsuoka, K., Imahashi, N., Ohno, M., Ode, H., Nakata, Y., Kubota, M., Sugimoto, A., Imahashi, M., Yokomaku, Y., & Iwatani, Y. (2022) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2022.101724 · Cited by 49
“The followings are limitations of our study regarding the validation of the ORF8 protein we used: (1) the mycFLAG added to the C-terminus may have affected the bioactivity, and (2) the induction time may have been insufficient.”
Marcotte, H., Cao, Y., Zuo, F., Simonelli, L., Sammartino, J. C., Pedotti, M., Sun, R., Cassaniti, I., Hagbom, M., Piralla, A., et al. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2315354120 · Cited by 53
“…in a S - pseudotype vesicular stomatitis virus neutralization assay showing its potent neutralizing (IC 50 : 0.01 to 1.6 nM) effect against 15 known SARS - CoV - 2 variants and other clade 1b sarbecoviruses circulating among other species, including RaTG13 and Pangolin - GD (37) ( SI Appendix, Fig.”
InfluentialXiang, Y., Xu, J., McGovern, B. L., Ranzenigo, A., Huang, W., Sang, Z., Shen, J., Diaz-Tapia, R., Pham, N. D., Teunissen, A. J. P., et al. (2024) · Cell · doi:10.1016/j.cell.2024.09.043 · Cited by 48
Beyond Infection: Integrating Competence into Reservoir Host Prediction
Becker, D. J., Seifert, S. N., & Carlson, C. J. (2020) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2020.08.014 · Cited by 49
The tyrosine kinase inhibitor nilotinib inhibits SARS‐CoV‐2 in vitro
Cagno, V., Magliocco, G., Tapparel, C., & Daali, Y. (2020) · Basic & Clinical Pharmacology & Toxicology · doi:10.1111/bcpt.13537 · Cited by 49
Sparrer, M. N., Hodges, N. F., Sherman, T. J., VandeWoude, S., Bosco‐Lauth, A. M., & Mayo, C. E. (2023) · Journal of Clinical Microbiology · doi:10.1128/jcm.01610-22 · Cited by 58
“The two lineages remained genetically similar; however, human ACE2 binding affinity was maintained in the SARS-CoV-2 progenitor and not in RaTG13 (20).”
BackgroundInfluentialMetagenomic identification of a new sarbecovirus from horseshoe bats in Europe
Crook, J. M., Murphy, I., Carter, D., Pullan, S. T., Carroll, M. W., Vipond, R., Cunningham, A. A., & Bell, D. (2021) · Scientific Reports · doi:10.1038/s41598-021-94011-z · Cited by 47
SARS‐CoV‐2 virulence evolution: Avirulence theory, immunity and trade‐offs
Alizon, S., & Sofonea, M. T. (2021) · Journal of Evolutionary Biology · doi:10.1111/jeb.13896 · Cited by 53
“Many reviews have been written on the evolutionary origin of the virus (Andersen et al., 2020; Boni et al. 2020) and on its genetic evolution since then (van Dorp, Acman, et al., 2020; Worobey et al., 2020).”
BackgroundAndrade, A. C. D. S. P., Campolina-Silva, G. H., Queiroz‐Junior, C. M., de Oliveira, L. C., Lacerda, L. D. S. B., Pimenta, J. C., Resende, F., Chaves, I. D. M., Passos, I. B. S., Teixeira, D. C., et al. (2021) · Journal of Virology · doi:10.1128/jvi.01276-21 · Cited by 50
Host ecology regulates interspecies recombination in bacteria of the genus Campylobacter
Mourkas, E., Yahara, K., Bayliss, S., Calland, J., Johansson, H., Mageiros, L., Muñoz-Ramírez, Z. Y., Futcher, G., Méric, G., Hitchings, M. D., et al. (2022) · eLife · doi:10.7554/elife.73552 · Cited by 45
Hunting Wildlife in the Tropics and Subtropics
Fa, J. E., Funk, S. M., & Nasi, R. (2022) · Cambridge University Press eBooks · doi:10.1017/9781316338704 · Cited by 56
Llanes, A., Restrepo, C. M., Zuleima Caballero, E., Rajeev, S., Kennedy, M. A., & Lleonart, R. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21124546 · Cited by 52
“A preliminary study has estimated that the group containing SARS-CoV-2 and its closest bat coronavirus, RaTG13, may have diverged between 40–70 years ago [91].”
BackgroundHost Diversity and Potential Transmission Pathways of SARS-CoV-2 at the Human-Animal Interface
Hedman, H. D., Krawczyk, E., Helmy, Y. A., Zhang, L., & Varga, C. (2021) · Pathogens · doi:10.3390/pathogens10020180 · Cited by 45
“SARS-CoV and SARS-CoV-2 belong to the subgenus Sarbecoviruses, characterized by frequent recombination events [25,26].”
BackgroundMethodInfluentialGarushyants, S. K., Rogozin, I. B., & Koonin, E. V. (2021) · Communications Biology · doi:10.1038/s42003-021-02858-9 · Cited by 46
Biological Properties of SARS-CoV-2 Variants: Epidemiological Impact and Clinical Consequences
Hoteit, R., & Yassine, H. M. (2022) · Vaccines · doi:10.3390/vaccines10060919 · Cited by 47
Morais-da-Silva, R. L., Reis, G. G., Sanctorum, H., & Molento, C. F. M. (2022) · Food Policy · doi:10.1016/j.foodpol.2022.102337 · Cited by 52
“There are also indications of an association of meat production and consumption with the introduction of infectious diseases (Espinosa et al., 2020), as probably occurred for the emergence of Covid-19 (Boni et al., 2020).”
Fc-mediated pan-sarbecovirus protection after alphavirus vector vaccination
Adams, L. E., Leist, S. R., Dinnon, K. H., West, A., Gully, K. L., Anderson, E. J., Loome, J. F., Madden, E. A., Powers, J. M., Schäfer, A., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112326 · Cited by 46
“In contrast, mice vaccinated with the homologous spike demonstrated significant protection from SARS-CoV-2-induced lung pathology, with baseline-equivalent DAD and ALI scores (41) (Figures 2G– 2I).”
Lauber, C., Zhang, X., Vaas, J., Klingler, F., Mutz, P., Dubin, A., Pietschmann, T., Roth, O., Neuman, B. W., Gorbalenya, A. E., et al. (2024) · PLoS Pathogens · doi:10.1371/journal.ppat.1012163 · Cited by 42
Burnett, D. L., Jackson, K., Langley, D. B., Aggarwal, A., Stella, A. O., Johansen, M. D., Balachandran, H., Lenthall, H., Rouet, R., Walker, G. J., et al. (2021) · Immunity · doi:10.1016/j.immuni.2021.10.019 · Cited by 45
“K417N/T, E484K, and N501Y mutations in the RBS epitope have independently arisen in rapidly spreading CoV2 variants of concern in South Africa (B.1.351/beta) and Brazil/Japan (P.1/gamma) (Greaney et al., 2021; Starr et al., 2021).”
BackgroundInfluentialEmergence of a recurrent insertion in the N-terminal domain of the SARS-CoV-2 spike glycoprotein
Gerdol, M., Dishnica, K., & Giorgetti, A. (2022) · Virus Research · doi:10.1016/j.virusres.2022.198674 · Cited by 47
Ahmad, S. U., Kiani, B. H., Abrar, M., Jan, Z., Zafar, I., Ali, Y., Alanazi, A. M., Malik, A., Rather, M. A., Ahmad, A., et al. (2022) · Journal of Infection and Public Health · doi:10.1016/j.jiph.2022.07.002 · Cited by 45
“The COVID-19 outbreak has enabled ongoing research engagement and data exchange, allowing scientists to examine SARS-CoV-2 recombination and propagation activities in real-time [53].”
Land Use Change and Infectious Disease Emergence
Rulli, M. C., D’Odorico, P., Galli, N., John, R. S., Muylaert, R. L., Santini, M., & Hayman, D. T. S. (2025) · Reviews of Geophysics · doi:10.1029/2022rg000785 · Cited by 57
Brierley, L., & Fowler, A. (2021) · PLoS Pathogens · doi:10.1371/journal.ppat.1009149 · Cited by 44
“Machine learning analysis To quantify the potential for genome composition biases to predict coronavirus host category, we used random forests, an ensemble machine learning approach that aggregates over a large number of individual classification tree models (Breiman, 2001).”
MethodSuperimmunity by pan-sarbecovirus nanobodies
Xiang, Y., Huang, W., Liu, H., Sang, Z., Nambulli, S., Tubiana, J., Williams, K. L., Duprex, W. P., Schneidman‐Duhovny, D., Wilson, I. A., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111004 · Cited by 43
“The high genetic diversity, frequent recombination, large natural reservoirs, and proximity to heavily populated areas across continents, underlie the recurrent zoonotic risks of sarbecoviruses and other circulating coronaviruses (Boni et al., 2020; Meganck and Baric, 2021).”
BackgroundDiagnosing the novel SARS-CoV-2 by quantitative RT-PCR: variations and opportunities
Barreto, H. G., Milagres, F. A. D. P., de Araújo, G. C., Daúde, M. M., & Benedito, V. A. (2020) · Journal of Molecular Medicine · doi:10.1007/s00109-020-01992-x · Cited by 43
Nikolaidis, M., Markoulatos, P., de Peer, Y. V., Oliver, S. G., & Amoutzias, G. D. (2021) · Molecular Biology and Evolution · doi:10.1093/molbev/msab292 · Cited by 42
“Fortunately, genomics is a valuable new tool for monitoring the emergence, spread, and ongoing adaptations of SARS-CoV-2 (Boni et al. 2020; Neches et al. 2020; Worobey et al. 2020; Kemp et al. 2021; Volz et al. 2021).”
BackgroundMethodResultInfluential
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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