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The emergence of highly fit SARS-CoV-2 variants accelerated by recombination

Michael R. Garvin, Erica T. Prates, Jonathon Romero, Ashley Cliff, Joao Gabriel Felipe Machado Gazolla, Monica Pickholz, Mirko Pavicic, View ORCID ProfileDaniel Jacobson
doi: https://doi.org/10.1101/2021.08.03.454981
Michael R. Garvin
1Oak Ridge National Laboratory, Computational Systems Biology, Biosciences, Oak Ridge, TN
2National Virtual Biotechnology Laboratory, US Department of Energy
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  • For correspondence: garvinmr@ornl.gov jacobsonda@ornl.gov
Erica T. Prates
1Oak Ridge National Laboratory, Computational Systems Biology, Biosciences, Oak Ridge, TN
2National Virtual Biotechnology Laboratory, US Department of Energy
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Jonathon Romero
3The Bredesen Center for Interdisciplinary Research and Graduate Education, University of Tennessee Knoxville, Knoxville, TN
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Ashley Cliff
3The Bredesen Center for Interdisciplinary Research and Graduate Education, University of Tennessee Knoxville, Knoxville, TN
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Joao Gabriel Felipe Machado Gazolla
1Oak Ridge National Laboratory, Computational Systems Biology, Biosciences, Oak Ridge, TN
2National Virtual Biotechnology Laboratory, US Department of Energy
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Monica Pickholz
4Departamento de Física, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
5Instituto de Física de Buenos Aires (IFIBA), CONICET-Universidad de Buenos Aires, Buenos Aires, Argentina
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Mirko Pavicic
1Oak Ridge National Laboratory, Computational Systems Biology, Biosciences, Oak Ridge, TN
2National Virtual Biotechnology Laboratory, US Department of Energy
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Daniel Jacobson
1Oak Ridge National Laboratory, Computational Systems Biology, Biosciences, Oak Ridge, TN
2National Virtual Biotechnology Laboratory, US Department of Energy
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  • ORCID record for Daniel Jacobson
  • For correspondence: garvinmr@ornl.gov jacobsonda@ornl.gov
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Abstract

The SARS-CoV-2 pandemic has entered an alarming new phase with the emergence of the variants of concern (VOC), P.1, B.1.351, and B.1.1.7, in late 2020, and B.1.427, B.1.429, and B.1.617, in 2021. Substitutions in the spike glycoprotein (S), such as Asn501Tyr and Glu484Lys, are likely key in several VOC. However, Asn501Tyr had been circulating for months in earlier strains and Glu484Lys is not found in B.1.1.7, indicating that they do not fully explain those fast-spreading variants. Here we use a computational systems biology approach to process more than 900,000 SARS-CoV-2 genomes and map spatiotemporal relationships, revealing other critical attributes of these variants. Comparisons to earlier dominant mutations and protein structural analyses indicate that the increased transmission is promoted by the combination of functionally complementary mutations in S and in other regions of the SARS-CoV-2 proteome. We report that the VOC have in common mutations in non-S proteins involved in immune-antagonism and replication performance, such as the nonstructural proteins 6 and 13, suggesting a convergent evolution of the virus. Critically, we propose that recombination events among divergent coinfecting haplotypes greatly accelerates the emergence of VOC by bringing together cooperative mutations and explaining the remarkably high mutation load of B.1.1.7. Therefore, extensive community distribution of SARS-CoV-2 increases the probability of future recombination events, further accelerating the evolution of the virus. This study reinforces the need for a global response to stop COVID-19 and future pandemics.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Notice: This manuscript has been authored by UT-Battelle, LLC, under contract DE-AC05-00OR22725 with the US Department of Energy (DOE). The US government retains and the publisher, by accepting the article for publication, acknowledges that the US government retains a nonexclusive, paid-up, irrevocable, worldwide license to publish or reproduce the published form of this manuscript, or allow others to do so, for US government purposes. DOE will provide public access to these results of federally sponsored research in accordance with the DOE Public Access Plan (http://energy.gov/downloads/doe-public-access-plan).

    ”Nothing in Biology Makes Sense Except in the Light of Evolution” -Theodosius Dobzhansky

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted August 08, 2021.
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The emergence of highly fit SARS-CoV-2 variants accelerated by recombination
Michael R. Garvin, Erica T. Prates, Jonathon Romero, Ashley Cliff, Joao Gabriel Felipe Machado Gazolla, Monica Pickholz, Mirko Pavicic, Daniel Jacobson
bioRxiv 2021.08.03.454981; doi: https://doi.org/10.1101/2021.08.03.454981
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The emergence of highly fit SARS-CoV-2 variants accelerated by recombination
Michael R. Garvin, Erica T. Prates, Jonathon Romero, Ashley Cliff, Joao Gabriel Felipe Machado Gazolla, Monica Pickholz, Mirko Pavicic, Daniel Jacobson
bioRxiv 2021.08.03.454981; doi: https://doi.org/10.1101/2021.08.03.454981

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