Recombination events are concentrated in the spike protein region of Betacoronaviruses

The Betacoronaviruses comprise multiple subgenera whose members have been implicated in human disease. As with SARS, MERS and now SARS-CoV-2, the origin and emergence of new variants are often attributed to events of recombination that alter host tropism or disease severity. In most cases, recombina...

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Published inPLoS genetics Vol. 16; no. 12; p. e1009272
Main Authors Bobay, Louis-Marie, O’Donnell, Angela C., Ochman, Howard
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 17.12.2020
Public Library of Science (PLoS)
Subjects
ACE2
Angiotensin-converting enzyme 2
Betacoronavirus - classification
Betacoronavirus - genetics
Biology and Life Sciences
Coronaviruses
Crossing Over, Genetic - genetics
Divergence
Evolution
Genes, Viral - genetics
Genetic aspects
Genetic recombination
Genome, Viral - genetics
Genomes
Host Specificity - genetics
Medicine and health sciences
Models, Genetic
Mutation
Nucleotide sequence
Physiological aspects
Polymorphism, Genetic
Population structure
Proteins
Recombination
Recombination, Genetic - genetics
SARS-CoV-2 - classification
SARS-CoV-2 - genetics
Severe acute respiratory syndrome coronavirus 2
Spike Glycoprotein, Coronavirus - genetics
Spike protein
Standard deviation
Transversion
Viral proteins
Viral Tropism - genetics
United States
Online AccessGet full text
ISSN1553-7404
1553-7390
1553-7404
DOI10.1371/journal.pgen.1009272

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Abstract The Betacoronaviruses comprise multiple subgenera whose members have been implicated in human disease. As with SARS, MERS and now SARS-CoV-2, the origin and emergence of new variants are often attributed to events of recombination that alter host tropism or disease severity. In most cases, recombination has been detected by searches for excessively similar genomic regions in divergent strains; however, such analyses are complicated by the high mutation rates of RNA viruses, which can produce sequence similarities in distant strains by convergent mutations. By applying a genome-wide approach that examines the source of individual polymorphisms and that can be tested against null models in which recombination is absent and homoplasies can arise only by convergent mutations, we examine the extent and limits of recombination in Betacoronaviruses . We find that recombination accounts for nearly 40% of the polymorphisms circulating in populations and that gene exchange occurs almost exclusively among strains belonging to the same subgenus. Although experimental studies have shown that recombinational exchanges occur at random along the coronaviral genome, in nature, they are vastly overrepresented in regions controlling viral interaction with host cells.
AbstractList The Betacoronaviruses comprise multiple subgenera whose members have been implicated in human disease. As with SARS, MERS and now SARS-CoV-2, the origin and emergence of new variants are often attributed to events of recombination that alter host tropism or disease severity. In most cases, recombination has been detected by searches for excessively similar genomic regions in divergent strains; however, such analyses are complicated by the high mutation rates of RNA viruses, which can produce sequence similarities in distant strains by convergent mutations. By applying a genome-wide approach that examines the source of individual polymorphisms and that can be tested against null models in which recombination is absent and homoplasies can arise only by convergent mutations, we examine the extent and limits of recombination in Betacoronaviruses. We find that recombination accounts for nearly 40% of the polymorphisms circulating in populations and that gene exchange occurs almost exclusively among strains belonging to the same subgenus. Although experimental studies have shown that recombinational exchanges occur at random along the coronaviral genome, in nature, they are vastly overrepresented in regions controlling viral interaction with host cells.
The Betacoronaviruses comprise multiple subgenera whose members have been implicated in human disease. As with SARS, MERS and now SARS-CoV-2, the origin and emergence of new variants are often attributed to events of recombination that alter host tropism or disease severity. In most cases, recombination has been detected by searches for excessively similar genomic regions in divergent strains; however, such analyses are complicated by the high mutation rates of RNA viruses, which can produce sequence similarities in distant strains by convergent mutations. By applying a genome-wide approach that examines the source of individual polymorphisms and that can be tested against null models in which recombination is absent and homoplasies can arise only by convergent mutations, we examine the extent and limits of recombination in Betacoronaviruses . We find that recombination accounts for nearly 40% of the polymorphisms circulating in populations and that gene exchange occurs almost exclusively among strains belonging to the same subgenus. Although experimental studies have shown that recombinational exchanges occur at random along the coronaviral genome, in nature, they are vastly overrepresented in regions controlling viral interaction with host cells.
The receptor-binding domain (RBD) of the SARS-CoV-2 spike protein, a crucial component that enables target cell entry via ACE2 receptor binding, is more similar to the RBD of the strain isolated from pangolins, with 97% sequence identity at the amino-acid level [3,5–7]. The greater similarity of the RBD region to a more distantly related strain raises questions about whether the spike protein of SARS-CoV-2 evolved through a recombination event or, alternatively, by multiple independent mutations followed by selection, causing convergence to the more pangolin-derived sequence. Since recombination events typically span hundreds of nucleotides, it is usually possible to discriminate between gene exchange and convergent evolution by assessing whether the polymorphisms shared by divergent strains are clumped. Despite very high rates of mutation that has led to polymorphisms shared among strains from the same or different subgenera, we find that over a third of the standing variation within Betacoronaviruses can be ascribed to recombination. [...]recombination in the Sarbecovirus subgenus, of which SARS-CoV-2 is a member, is concentrated in genes encoding the spike protein. In parallel, we estimated the number of homoplasies expected to result from convergent mutations by simulating genome evolution with mutations and without recombination, while conserving population structure, numbers of polymorphisms, transition/transversion ratio and relative substitution rates across codon positions.
The Betacoronaviruses comprise multiple subgenera whose members have been implicated in human disease. As with SARS, MERS and now SARS-CoV-2, the origin and emergence of new variants are often attributed to events of recombination that alter host tropism or disease severity. In most cases, recombination has been detected by searches for excessively similar genomic regions in divergent strains; however, such analyses are complicated by the high mutation rates of RNA viruses, which can produce sequence similarities in distant strains by convergent mutations. By applying a genome-wide approach that examines the source of individual polymorphisms and that can be tested against null models in which recombination is absent and homoplasies can arise only by convergent mutations, we examine the extent and limits of recombination in Betacoronaviruses. We find that recombination accounts for nearly 40% of the polymorphisms circulating in populations and that gene exchange occurs almost exclusively among strains belonging to the same subgenus. Although experimental studies have shown that recombinational exchanges occur at random along the coronaviral genome, in nature, they are vastly overrepresented in regions controlling viral interaction with host cells.The Betacoronaviruses comprise multiple subgenera whose members have been implicated in human disease. As with SARS, MERS and now SARS-CoV-2, the origin and emergence of new variants are often attributed to events of recombination that alter host tropism or disease severity. In most cases, recombination has been detected by searches for excessively similar genomic regions in divergent strains; however, such analyses are complicated by the high mutation rates of RNA viruses, which can produce sequence similarities in distant strains by convergent mutations. By applying a genome-wide approach that examines the source of individual polymorphisms and that can be tested against null models in which recombination is absent and homoplasies can arise only by convergent mutations, we examine the extent and limits of recombination in Betacoronaviruses. We find that recombination accounts for nearly 40% of the polymorphisms circulating in populations and that gene exchange occurs almost exclusively among strains belonging to the same subgenus. Although experimental studies have shown that recombinational exchanges occur at random along the coronaviral genome, in nature, they are vastly overrepresented in regions controlling viral interaction with host cells.
The receptor-binding domain (RBD) of the SARS-CoV-2 spike protein, a crucial component that enables target cell entry via ACE2 receptor binding, is more similar to the RBD of the strain isolated from pangolins, with 97% sequence identity at the amino-acid level [3,5–7]. The greater similarity of the RBD region to a more distantly related strain raises questions about whether the spike protein of SARS-CoV-2 evolved through a recombination event or, alternatively, by multiple independent mutations followed by selection, causing convergence to the more pangolin-derived sequence. Since recombination events typically span hundreds of nucleotides, it is usually possible to discriminate between gene exchange and convergent evolution by assessing whether the polymorphisms shared by divergent strains are clumped. Despite very high rates of mutation that has led to polymorphisms shared among strains from the same or different subgenera, we find that over a third of the standing variation within Betacoronaviruses can be ascribed to recombination. [...]recombination in the Sarbecovirus subgenus, of which SARS-CoV-2 is a member, is concentrated in genes encoding the spike protein. In parallel, we estimated the number of homoplasies expected to result from convergent mutations by simulating genome evolution with mutations and without recombination, while conserving population structure, numbers of polymorphisms, transition/transversion ratio and relative substitution rates across codon positions.
The Betacoronaviruses comprise multiple subgenera whose members have been implicated in human disease. As with SARS, MERS and now SARS-CoV-2, the origin and emergence of new variants are often attributed to events of recombination that alter host tropism or disease severity. In most cases, recombination has been detected by searches for excessively similar genomic regions in divergent strains; however, such analyses are complicated by the high mutation rates of RNA viruses, which can produce sequence similarities in distant strains by convergent mutations. By applying a genome-wide approach that examines the source of individual polymorphisms and that can be tested against null models in which recombination is absent and homoplasies can arise only by convergent mutations, we examine the extent and limits of recombination in Betacoronaviruses . We find that recombination accounts for nearly 40% of the polymorphisms circulating in populations and that gene exchange occurs almost exclusively among strains belonging to the same subgenus. Although experimental studies have shown that recombinational exchanges occur at random along the coronaviral genome, in nature, they are vastly overrepresented in regions controlling viral interaction with host cells. The high mutation rate of RNA viruses makes it problematic to understand and resolve the role of recombination in generating genomic variation. Frequent mutations will (1) increase the likelihood of convergent mutations, particularly in regions subject to strong positive selection, causing sequence similarities that can be mistaken for recombination events, and (2) introduce new changes that accumulate and obscure recognition of past recombination events. We analyzed the patterns of recombination across Betacoronaviruses using a dedicated approach to distinguish true recombination from convergent mutations. The Betacoronaviruses comprise several populations that could be considered distinct biological species in that they do not engage in gene flow with one another. Moreover, recombination events within the Sarbecovirus subgenus, which includes SARS-CoV-2, are highly biased and predominate in the spike protein region, implicating recombination as having a substantial role in host tropism and viral ecology.
Audience Academic
Author Bobay, Louis-Marie
O’Donnell, Angela C.
Ochman, Howard
AuthorAffiliation 1 Department of Biology, University of North Carolina at Greensboro, Greensboro, North Carolina, United States of America
Stanford University, UNITED STATES
2 Department of Integrative Biology, University of Texas at Austin, Austin, Texas, United States of America
AuthorAffiliation_xml – name: 2 Department of Integrative Biology, University of Texas at Austin, Austin, Texas, United States of America
– name: 1 Department of Biology, University of North Carolina at Greensboro, Greensboro, North Carolina, United States of America
– name: Stanford University, UNITED STATES
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  givenname: Angela C.
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  surname: O’Donnell
  fullname: O’Donnell, Angela C.
– sequence: 3
  givenname: Howard
  orcidid: 0000-0003-1688-7059
  surname: Ochman
  fullname: Ochman, Howard
BackLink https://www.ncbi.nlm.nih.gov/pubmed/33332358$$D View this record in MEDLINE/PubMed
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Snippet The Betacoronaviruses comprise multiple subgenera whose members have been implicated in human disease. As with SARS, MERS and now SARS-CoV-2, the origin and...
The Betacoronaviruses comprise multiple subgenera whose members have been implicated in human disease. As with SARS, MERS and now SARS-CoV-2, the origin and...
The receptor-binding domain (RBD) of the SARS-CoV-2 spike protein, a crucial component that enables target cell entry via ACE2 receptor binding, is more...
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StartPage e1009272
SubjectTerms ACE2
Angiotensin-converting enzyme 2
Betacoronavirus - classification
Betacoronavirus - genetics
Biology and Life Sciences
Coronaviruses
Crossing Over, Genetic - genetics
Divergence
Evolution
Genes, Viral - genetics
Genetic aspects
Genetic recombination
Genome, Viral - genetics
Genomes
Host Specificity - genetics
Medicine and health sciences
Models, Genetic
Mutation
Nucleotide sequence
Physiological aspects
Polymorphism, Genetic
Population structure
Proteins
Recombination
Recombination, Genetic - genetics
SARS-CoV-2 - classification
SARS-CoV-2 - genetics
Severe acute respiratory syndrome coronavirus 2
Spike Glycoprotein, Coronavirus - genetics
Spike protein
Standard deviation
Transversion
Viral proteins
Viral Tropism - genetics
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Title Recombination events are concentrated in the spike protein region of Betacoronaviruses
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http://dx.doi.org/10.1371/journal.pgen.1009272
Volume 16
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