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SARS-CoV-2 variant evolution in the United States: High accumulation of viral mutations over time likely through serial Founder Events and mutational bursts

Since the first case of COVID-19 in December 2019 in Wuhan, China, SARS-CoV-2 has spread worldwide and within a year and a half has caused 3.56 million deaths globally. With dramatically increasing infection numbers, and the arrival of new variants with increased infectivity, tracking the evolution...

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Autores principales: Tasakis, Rafail Nikolaos, Samaras, Georgios, Jamison, Anna, Lee, Michelle, Paulus, Alexandra, Whitehouse, Gabrielle, Verkoczy, Laurent, Papavasiliou, F. Nina, Diaz, Marilyn
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8301627/
https://www.ncbi.nlm.nih.gov/pubmed/34297786
http://dx.doi.org/10.1371/journal.pone.0255169
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author Tasakis, Rafail Nikolaos
Samaras, Georgios
Jamison, Anna
Lee, Michelle
Paulus, Alexandra
Whitehouse, Gabrielle
Verkoczy, Laurent
Papavasiliou, F. Nina
Diaz, Marilyn
author_facet Tasakis, Rafail Nikolaos
Samaras, Georgios
Jamison, Anna
Lee, Michelle
Paulus, Alexandra
Whitehouse, Gabrielle
Verkoczy, Laurent
Papavasiliou, F. Nina
Diaz, Marilyn
author_sort Tasakis, Rafail Nikolaos
collection PubMed
description Since the first case of COVID-19 in December 2019 in Wuhan, China, SARS-CoV-2 has spread worldwide and within a year and a half has caused 3.56 million deaths globally. With dramatically increasing infection numbers, and the arrival of new variants with increased infectivity, tracking the evolution of its genome is crucial for effectively controlling the pandemic and informing vaccine platform development. Our study explores evolution of SARS-CoV-2 in a representative cohort of sequences covering the entire genome in the United States, through all of 2020 and early 2021. Strikingly, we detected many accumulating Single Nucleotide Variations (SNVs) encoding amino acid changes in the SARS-CoV-2 genome, with a pattern indicative of RNA editing enzymes as major mutators of SARS-CoV-2 genomes. We report three major variants through October of 2020. These revealed 14 key mutations that were found in various combinations among 14 distinct predominant signatures. These signatures likely represent evolutionary lineages of SARS-CoV-2 in the U.S. and reveal clues to its evolution such as a mutational burst in the summer of 2020 likely leading to a homegrown new variant, and a trend towards higher mutational load among viral isolates, but with occasional mutation loss. The last quartile of 2020 revealed a concerning accumulation of mostly novel low frequency replacement mutations in the Spike protein, and a hypermutable glutamine residue near the putative furin cleavage site. Finally, end of the year data and 2021 revealed the gradual increase to prevalence of known variants of concern, particularly B.1.1.7, that have acquired additional Spike mutations. Overall, our results suggest that predominant viral genomes are dynamically evolving over time, with periods of mutational bursts and unabated mutation accumulation. This high level of existing variation, even at low frequencies and especially in the Spike-encoding region may become problematic when super-spreader events, akin to serial Founder Events in evolution, drive these rare mutations to prominence.
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spelling pubmed-83016272021-07-31 SARS-CoV-2 variant evolution in the United States: High accumulation of viral mutations over time likely through serial Founder Events and mutational bursts Tasakis, Rafail Nikolaos Samaras, Georgios Jamison, Anna Lee, Michelle Paulus, Alexandra Whitehouse, Gabrielle Verkoczy, Laurent Papavasiliou, F. Nina Diaz, Marilyn PLoS One Research Article Since the first case of COVID-19 in December 2019 in Wuhan, China, SARS-CoV-2 has spread worldwide and within a year and a half has caused 3.56 million deaths globally. With dramatically increasing infection numbers, and the arrival of new variants with increased infectivity, tracking the evolution of its genome is crucial for effectively controlling the pandemic and informing vaccine platform development. Our study explores evolution of SARS-CoV-2 in a representative cohort of sequences covering the entire genome in the United States, through all of 2020 and early 2021. Strikingly, we detected many accumulating Single Nucleotide Variations (SNVs) encoding amino acid changes in the SARS-CoV-2 genome, with a pattern indicative of RNA editing enzymes as major mutators of SARS-CoV-2 genomes. We report three major variants through October of 2020. These revealed 14 key mutations that were found in various combinations among 14 distinct predominant signatures. These signatures likely represent evolutionary lineages of SARS-CoV-2 in the U.S. and reveal clues to its evolution such as a mutational burst in the summer of 2020 likely leading to a homegrown new variant, and a trend towards higher mutational load among viral isolates, but with occasional mutation loss. The last quartile of 2020 revealed a concerning accumulation of mostly novel low frequency replacement mutations in the Spike protein, and a hypermutable glutamine residue near the putative furin cleavage site. Finally, end of the year data and 2021 revealed the gradual increase to prevalence of known variants of concern, particularly B.1.1.7, that have acquired additional Spike mutations. Overall, our results suggest that predominant viral genomes are dynamically evolving over time, with periods of mutational bursts and unabated mutation accumulation. This high level of existing variation, even at low frequencies and especially in the Spike-encoding region may become problematic when super-spreader events, akin to serial Founder Events in evolution, drive these rare mutations to prominence. Public Library of Science 2021-07-23 /pmc/articles/PMC8301627/ /pubmed/34297786 http://dx.doi.org/10.1371/journal.pone.0255169 Text en © 2021 Tasakis et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Tasakis, Rafail Nikolaos
Samaras, Georgios
Jamison, Anna
Lee, Michelle
Paulus, Alexandra
Whitehouse, Gabrielle
Verkoczy, Laurent
Papavasiliou, F. Nina
Diaz, Marilyn
SARS-CoV-2 variant evolution in the United States: High accumulation of viral mutations over time likely through serial Founder Events and mutational bursts
title SARS-CoV-2 variant evolution in the United States: High accumulation of viral mutations over time likely through serial Founder Events and mutational bursts
title_full SARS-CoV-2 variant evolution in the United States: High accumulation of viral mutations over time likely through serial Founder Events and mutational bursts
title_fullStr SARS-CoV-2 variant evolution in the United States: High accumulation of viral mutations over time likely through serial Founder Events and mutational bursts
title_full_unstemmed SARS-CoV-2 variant evolution in the United States: High accumulation of viral mutations over time likely through serial Founder Events and mutational bursts
title_short SARS-CoV-2 variant evolution in the United States: High accumulation of viral mutations over time likely through serial Founder Events and mutational bursts
title_sort sars-cov-2 variant evolution in the united states: high accumulation of viral mutations over time likely through serial founder events and mutational bursts
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8301627/
https://www.ncbi.nlm.nih.gov/pubmed/34297786
http://dx.doi.org/10.1371/journal.pone.0255169
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