Untangling the Evolution of the Receptor-Binding Motif of SARS-CoV-2.
Bayes factors
Dissonance
Information content
Recombination
Viral evolution
Journal
Journal of molecular evolution
ISSN: 1432-1432
Titre abrégé: J Mol Evol
Pays: Germany
ID NLM: 0360051
Informations de publication
Date de publication:
22 May 2024
22 May 2024
Historique:
received:
17
07
2023
accepted:
04
05
2024
medline:
23
5
2024
pubmed:
23
5
2024
entrez:
22
5
2024
Statut:
aheadofprint
Résumé
The spike protein determines the host-range specificity of coronaviruses. In particular, the Receptor-Binding Motif in the spike protein from SARS-CoV-2 contains the amino acids involved in molecular recognition of the host Angiotensin Converting Enzyme 2. Therefore, to understand how SARS-CoV-2 acquired its capacity to infect humans it is necessary to reconstruct the evolution of this important motif. Early during the pandemic, it was proposed that the SARS-CoV-2 Receptor-Binding Domain was acquired via recombination with a pangolin infecting coronavirus. This proposal was challenged by an alternative explanation that suggested that the Receptor-Binding Domain from SARS-CoV-2 did not originated via recombination with a coronavirus from a pangolin. Instead, this alternative hypothesis proposed that the Receptor-Binding Motif from the bat coronavirus RaTG13, was acquired via recombination with an unidentified coronavirus. And as a consequence of this event, the Receptor-Binding Domain from the pangolin coronavirus appeared as phylogenetically closer to SARS-CoV-2. Recently, the genomes from coronaviruses from Cambodia (bat_RShST182/200) and Laos (BANAL-20-52/103/247) which are closely related to SARS-CoV-2 were reported. However, no detailed analysis of the evolution of the Receptor-Binding Motif from these coronaviruses was reported. Here we revisit the evolution of the Receptor-Binding Domain and Motif in the light of the novel coronavirus genome sequences. Specifically, we wanted to test whether the above coronaviruses from Cambodia and Laos were the source of the Receptor-Binding Domain from RaTG13. We found that the Receptor-Binding Motif from these coronaviruses is phylogenetically closer to SARS-CoV-2 than to RaTG13. Therefore, the source of the Receptor-Binding Domain from RaTG13 is still unidentified. In accordance with previous studies, our results are consistent with the hypothesis that the Receptor-Binding Motif from SARS-CoV-2 evolved by vertical inheritance from a bat-infecting population of coronaviruses.
Identifiants
pubmed: 38777906
doi: 10.1007/s00239-024-10175-y
pii: 10.1007/s00239-024-10175-y
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : CONAHCYT
ID : l1200/320/2022
Organisme : CONAHCYT
ID : l1200/224/2021
Informations de copyright
© 2024. The Author(s).
Références
Andersen KG, Rambaut A, Lipkin WI, Holmes EC, Garry RF (2020) The proximal origin of SARS-CoV-2. Nat Med 26:450–452. https://doi.org/10.1038/s41591-020-0820-9
doi: 10.1038/s41591-020-0820-9
pubmed: 32284615
pmcid: 7095063
Ashkenazy H, Erez E, Martz E, Pupko T, Ben-Ta N (2010) ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res 38:W529–W533. https://doi.org/10.1093/nar/gkq399
doi: 10.1093/nar/gkq399
pubmed: 20478830
pmcid: 2896094
Ben Chorin A, Masrati G, Kessel A, Narunsky A, Sprinzak J, Lahav S, Ashkenazy H, Ben-Tal N (2020) ConSurf-DB: an accessible repository for the evolutionary conservation patterns of the majority of PDB proteins. Protein Sci 29:258–267. https://doi.org/10.1002/pro.3779
doi: 10.1002/pro.3779
pubmed: 31702846
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. Nature Microbiol 5:1408–1417. https://doi.org/10.1038/s41564-020-0771-4
doi: 10.1038/s41564-020-0771-4
Cui J, Li F, Shi Z-L (2019) Origin and evolution of pathogenic coronaviruses. Nat Rev Microbiol 17(3):181–192. https://doi.org/10.1038/s41579-018-0118-9
doi: 10.1038/s41579-018-0118-9
pubmed: 30531947
Delaune D, Hul V, Karlsson EA, Hassanin A, Ou TP et al (2021) A novel SARS-CoV-2 related coronavirus in bats from Cambodia. Nature Commun 12(1):6563. https://doi.org/10.1038/s41467-021-26809-4
doi: 10.1038/s41467-021-26809-4
Kass RE, Raftery AE (1995) Bayes factors. J Am Stat Assoc 90:773–795. https://doi.org/10.2307/2291091
doi: 10.2307/2291091
Khare S, Gurry C, Freitas L, Schultz MB, Bach G et al (2021) GISAID’s role in pandemic response. China CDC Weekly 3(49):1049–1051. https://doi.org/10.46234/ccdcw2021.255
doi: 10.46234/ccdcw2021.255
pubmed: 34934514
pmcid: 8668406
Kishino H, Hasegawa M (1989) Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea. J Mol Evol 29:170–179. https://doi.org/10.1007/BF02100115
doi: 10.1007/BF02100115
pubmed: 2509717
Kosakovsky Pond SL, Posada D, Gravenor MB, Woelk CH, Frost SDW (2006) Automated phylogenetic detection of recombination using a genetic algorithm. Mol Biol Evol 23(10):1891–1901. https://doi.org/10.1093/molbev/msl051
doi: 10.1093/molbev/msl051
pubmed: 16818476
Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R et al (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19(9):1639–1645. https://doi.org/10.1101/gr.092759.109
doi: 10.1101/gr.092759.109
pubmed: 19541911
pmcid: 2752132
Lam TTY, Jia N, Zhang YW, Shum MH-H, Jiang J-F et al (2020) Identifying SARS-CoV-2-related coronaviruses in Malayan pangolins. Nature 583:282–285. https://doi.org/10.1038/s41586-020-2169-0
doi: 10.1038/s41586-020-2169-0
pubmed: 32218527
Lan J, Ge J, Yu J, Shan S, Zhou H et al (2020) Structure of the SARS-CoV-2 spike receptor-binding domain bound to the ACE2 receptor. Nature 581:215–220. https://doi.org/10.1038/s41586-020-2180-5
doi: 10.1038/s41586-020-2180-5
pubmed: 32225176
Lewis PO, Chen M-H, Kuo L, Lewis LA, Fučíková K et al (2016) Estimating Bayesian phylogenetic information content. Syst Biol 65(6):1009–1023. https://doi.org/10.1093/sysbio/syw042
doi: 10.1093/sysbio/syw042
pubmed: 27155008
pmcid: 5066063
Li X, Giorgi EE, Marichannegowda MH, Foley B, Xiao Ch et al (2020) Emergence of SARS-CoV-2 through recombination and strong purifying selection. Sci Adv. https://doi.org/10.1126/sciadv.abb9153
doi: 10.1126/sciadv.abb9153
pubmed: 33355146
pmcid: 10764100
Li M, Du J, Liu W, Li Z, Lv F et al (2023) Comparative susceptibility of SARS-CoV-2, SARS-CoV, and MERS-CoV across mammals. ISME J 17:549–560. https://doi.org/10.1038/s41396-023-01368-2
doi: 10.1038/s41396-023-01368-2
pubmed: 36690780
pmcid: 9869846
Lytras S, Hughes J, Martin D, Swanepoel P et al (2022) Exploring the natural origins of SARS-CoV-2 in the light of recombination. Genome Biol Evol 14(2):evac018. https://doi.org/10.1093/gbe/evac018
doi: 10.1093/gbe/evac018
pubmed: 35137080
pmcid: 8882382
Makarenkov V, Mazoure B, Rabusseau G, Legrendre P (2021) Horizontal gene transfer and recombination analysis of SARS-CoV-2 genes helps discover its close relatives and shed light on its origin. BMC Ecol Evol 1:5. https://doi.org/10.1186/s12862-020-01732-2
doi: 10.1186/s12862-020-01732-2
Martin DP, Varsani A, Roumagnac P, Botha G, Maslamoney S, Schwab T, Kelz Z, Kumar V, Murrell B (2020) RDP5: a computer program for analyzing recombination in, and removing signals of recombination from, nucleotide sequence datasets. Virus Evol 7(1):veaa087. https://doi.org/10.1093/ve/veaa087
doi: 10.1093/ve/veaa087
pubmed: 33936774
pmcid: 8062008
Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD et al (2020) IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol and Evol 37(5):1530–1534. https://doi.org/10.1093/molbev/msaa015
doi: 10.1093/molbev/msaa015
Neupane S et al (2019) Assessing combinability of phylogenomic data using Bayes factors. Syst Biol 68(5):744–754. https://doi.org/10.1093/sysbio/syz007
doi: 10.1093/sysbio/syz007
pubmed: 30726954
pmcid: 7967903
Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM et al (2004) UCSF chimera—a visualization system for exploratory research and analysis. J Comput Chem 25(13):1605–1612. https://doi.org/10.1002/jcc.20084
doi: 10.1002/jcc.20084
pubmed: 15264254
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A et al (2012) MRBAYES 3.2: efficient Bayesian phylogenetic inference and model selection across a large model space. Syst Biol 61(3):539–542
doi: 10.1093/sysbio/sys029
pubmed: 22357727
pmcid: 3329765
Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38(7):3022–3027. https://doi.org/10.1093/molbev/msab120
doi: 10.1093/molbev/msab120
pubmed: 33892491
pmcid: 8233496
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 604:330–336. https://doi.org/10.1038/s41586-022-04532-4
doi: 10.1038/s41586-022-04532-4
pubmed: 35172323
Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ (2009) Jalview version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189–1191. https://doi.org/10.1093/bioinformatics/btp033
doi: 10.1093/bioinformatics/btp033
pubmed: 19151095
pmcid: 2672624
Weaver S, Shank SD, Spielman SJ, Li M, Muse SV, Pond SLK (2018) Datamonkey 2.0: a modern web application for characterizing selective and other evolutionary processes. Mol Biol Evol 35(3):773–777. https://doi.org/10.1093/molbev/msx335
doi: 10.1093/molbev/msx335
pubmed: 29301006
pmcid: 5850112
Xia X (2021) Domains and functions of spike protein in SARS-Cov-2 in the context of vaccine design. Viruses 13(1):109. https://doi.org/10.3390/v13010109
doi: 10.3390/v13010109
pubmed: 33466921
pmcid: 7829931
Zhang T, Wu Q, Zhang Z (2020) Probable pangolin origin of SARS-CoV-2 associated with the COVID-19 outbreak. Curr Biol 30(7):1346-1351.e2. https://doi.org/10.1016/j.cub.2020.03.022
doi: 10.1016/j.cub.2020.03.022
pubmed: 32197085
pmcid: 7156161
Zhou P, Yang X-L, Wang X-G, Hu B, Zhang L et al (2020) A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature 579:270–273. https://doi.org/10.1038/s41586-020-2012-7
doi: 10.1038/s41586-020-2012-7
pubmed: 32015507
pmcid: 7095418