Generation and transmission of inter-lineage recombinants in the SARS-CoV-2 pandemic

Ben Jackson; Maciej F. Boni; Matthew J. Bull; Amy Colleran; Rachel M. Colquhoun; Alistair C. Darby; Sam Haldenby; Verity Hill; Anita Lucaci; John T. McCrone; Samuel M. Nicholls; Áine O’toole; Nicole Pacchiarini; Radoslaw Poplawski; Emily Scher; Flora Todd; Hermione J. Webster; Mark Whitehead; Claudia Wierzbicki; The COVID-19 Genomics UK (COG-UK) Consortium; Nicholas J. Loman; Thomas R. Connor; David L. Robertson; Oliver G. Pybus; Andrew Rambaut; Matthew Bashton; Darren Smith; Andrew Nelson; Greg Young; Clare McCann

doi:10.1016/j.cell.2021.08.014

Generation and transmission of inter-lineage recombinants in the SARS-CoV-2 pandemic

Ben Jackson^*, Maciej F. Boni, Matthew J. Bull, Amy Colleran, Rachel M. Colquhoun, Alistair C. Darby, Sam Haldenby, Verity Hill, Anita Lucaci, John T. McCrone, Samuel M. Nicholls, Áine O’toole, Nicole Pacchiarini, Radoslaw Poplawski, Emily Scher, Flora Todd, Hermione J. Webster, Mark Whitehead, Claudia Wierzbicki, The COVID-19 Genomics UK (COG-UK) ConsortiumNicholas J. Loman, Thomas R. Connor, David L. Robertson, Oliver G. Pybus, Andrew Rambaut^*, Matthew Bashton, Darren Smith, Andrew Nelson, Greg Young, Clare McCann

^*Corresponding author for this work

Applied Sciences Department

Research output: Contribution to journal › Article › peer-review

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Abstract

We present evidence for multiple independent origins of recombinant SARS-CoV-2 viruses sampled from late 2020 and early 2021 in the United Kingdom. Their genomes carry single nucleotide polymorphisms and deletions that are characteristic of the B.1.1.7 variant of concern, but lack the full complement of lineage-defining mutations. Instead, the remainder of their genomes share contiguous genetic variation with non-B.1.1.7 viruses circulating in the same geographic area at the same time as the recombinants. In four instances there was evidence for onward transmission of a recombinant-origin virus, including one transmission cluster of 45 sequenced cases over the course of two months. The inferred genomic locations of recombination breakpoints suggest that every community-transmitted recombinant virus inherited its spike region from a B.1.1.7 parental virus, consistent with a transmission advantage for B.1.1.7’s set of mutations.

Original language	English
Pages (from-to)	5179-5188.e8
Number of pages	19
Journal	Cell
Volume	184
Issue number	20
Early online date	17 Aug 2021
DOIs	https://doi.org/10.1016/j.cell.2021.08.014
Publication status	Published - 30 Sept 2021

Keywords

SARS-CoV-2
evolution
recombination
genomic epidemiology
B.1.1.7
variants
genomics
Base Sequence/genetics
Genome, Viral
Pandemics
SARS-CoV-2/genetics
Gene Frequency
Humans
Genotype
Phylogeny
Computational Biology/methods
United Kingdom/epidemiology
COVID-19/epidemiology
Recombination, Genetic
Polymorphism, Single Nucleotide
Whole Genome Sequencing/methods
Mutation

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10.1016/j.cell.2021.08.014Licence: CC BY

PIIS0092867421009843Accepted author manuscript, 1.37 MBLicence: CC BY
1-s2.0-S0092867421009843-mainFinal published version, 2.65 MBLicence: CC BY

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Jackson, B., Boni, M. F., Bull, M. J., Colleran, A., Colquhoun, R. M., Darby, A. C., Haldenby, S., Hill, V., Lucaci, A., McCrone, J. T., Nicholls, S. M., O’toole, Á., Pacchiarini, N., Poplawski, R., Scher, E., Todd, F., Webster, H. J., Whitehead, M., Wierzbicki, C., ... McCann, C. (2021). Generation and transmission of inter-lineage recombinants in the SARS-CoV-2 pandemic. Cell, 184(20), 5179-5188.e8. https://doi.org/10.1016/j.cell.2021.08.014

@article{12152139c462488eb2489c3342e16ad3,

title = "Generation and transmission of inter-lineage recombinants in the SARS-CoV-2 pandemic",

abstract = "We present evidence for multiple independent origins of recombinant SARS-CoV-2 viruses sampled from late 2020 and early 2021 in the United Kingdom. Their genomes carry single nucleotide polymorphisms and deletions that are characteristic of the B.1.1.7 variant of concern, but lack the full complement of lineage-defining mutations. Instead, the remainder of their genomes share contiguous genetic variation with non-B.1.1.7 viruses circulating in the same geographic area at the same time as the recombinants. In four instances there was evidence for onward transmission of a recombinant-origin virus, including one transmission cluster of 45 sequenced cases over the course of two months. The inferred genomic locations of recombination breakpoints suggest that every community-transmitted recombinant virus inherited its spike region from a B.1.1.7 parental virus, consistent with a transmission advantage for B.1.1.7{\textquoteright}s set of mutations.",

keywords = "SARS-CoV-2, evolution, recombination, genomic epidemiology, B.1.1.7, variants, genomics, Base Sequence/genetics, Genome, Viral, Pandemics, SARS-CoV-2/genetics, Gene Frequency, Humans, Genotype, Phylogeny, Computational Biology/methods, United Kingdom/epidemiology, COVID-19/epidemiology, Recombination, Genetic, Polymorphism, Single Nucleotide, Whole Genome Sequencing/methods, Mutation",

author = "Ben Jackson and Boni, {Maciej F.} and Bull, {Matthew J.} and Amy Colleran and Colquhoun, {Rachel M.} and Darby, {Alistair C.} and Sam Haldenby and Verity Hill and Anita Lucaci and McCrone, {John T.} and Nicholls, {Samuel M.} and {\'A}ine O{\textquoteright}toole and Nicole Pacchiarini and Radoslaw Poplawski and Emily Scher and Flora Todd and Webster, {Hermione J.} and Mark Whitehead and Claudia Wierzbicki and {The COVID-19 Genomics UK (COG-UK) Consortium} and Loman, {Nicholas J.} and Connor, {Thomas R.} and Robertson, {David L.} and Pybus, {Oliver G.} and Andrew Rambaut and Matthew Bashton and Darren Smith and Andrew Nelson and Greg Young and Clare McCann",

note = "Matthew Bashton, Andrew Nelson, Darren Smith, Greg Young are members of the COVID-19 Genomics UK (COG-UK) consortium. Funding information: COG-UK is supported by funding from the Medical Research Council (MRC) part of UK Research & Innovation (UKRI), the National Institute of Health Research (NIHR) and Genome Research Limited, operating as the Wellcome Sanger Institute. Also MRC (MC UU 1201412), UKRI/Wellcome (COG-UK), Wellcome Trust Collaborator Award (206298/Z/17/Z – ARTIC Network; TCW Wellcome Trust Award 204802/Z/16/Z. ",

year = "2021",

month = sep,

day = "30",

doi = "10.1016/j.cell.2021.08.014",

language = "English",

volume = "184",

pages = "5179--5188.e8",

journal = "Cell",

issn = "0092-8674",

publisher = "Cell Press",

number = "20",

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Jackson, B, Boni, MF, Bull, MJ, Colleran, A, Colquhoun, RM, Darby, AC, Haldenby, S, Hill, V, Lucaci, A, McCrone, JT, Nicholls, SM, O’toole, Á, Pacchiarini, N, Poplawski, R, Scher, E, Todd, F, Webster, HJ, Whitehead, M, Wierzbicki, C, The COVID-19 Genomics UK (COG-UK) Consortium, Loman, NJ, Connor, TR, Robertson, DL, Pybus, OG, Rambaut, A, Bashton, M , Smith, D , Nelson, A, Young, G & McCann, C 2021, 'Generation and transmission of inter-lineage recombinants in the SARS-CoV-2 pandemic', Cell, vol. 184, no. 20, pp. 5179-5188.e8. https://doi.org/10.1016/j.cell.2021.08.014

TY - JOUR

T1 - Generation and transmission of inter-lineage recombinants in the SARS-CoV-2 pandemic

AU - Jackson, Ben

AU - Boni, Maciej F.

AU - Bull, Matthew J.

AU - Colleran, Amy

AU - Colquhoun, Rachel M.

AU - Darby, Alistair C.

AU - Haldenby, Sam

AU - Hill, Verity

AU - Lucaci, Anita

AU - McCrone, John T.

AU - Nicholls, Samuel M.

AU - O’toole, Áine

AU - Pacchiarini, Nicole

AU - Poplawski, Radoslaw

AU - Scher, Emily

AU - Todd, Flora

AU - Webster, Hermione J.

AU - Whitehead, Mark

AU - Wierzbicki, Claudia

AU - The COVID-19 Genomics UK (COG-UK) Consortium

AU - Loman, Nicholas J.

AU - Connor, Thomas R.

AU - Robertson, David L.

AU - Pybus, Oliver G.

AU - Rambaut, Andrew

AU - Bashton, Matthew

AU - Smith, Darren

AU - Nelson, Andrew

AU - Young, Greg

AU - McCann, Clare

N1 - Matthew Bashton, Andrew Nelson, Darren Smith, Greg Young are members of the COVID-19 Genomics UK (COG-UK) consortium. Funding information: COG-UK is supported by funding from the Medical Research Council (MRC) part of UK Research & Innovation (UKRI), the National Institute of Health Research (NIHR) and Genome Research Limited, operating as the Wellcome Sanger Institute. Also MRC (MC UU 1201412), UKRI/Wellcome (COG-UK), Wellcome Trust Collaborator Award (206298/Z/17/Z – ARTIC Network; TCW Wellcome Trust Award 204802/Z/16/Z.

PY - 2021/9/30

Y1 - 2021/9/30

N2 - We present evidence for multiple independent origins of recombinant SARS-CoV-2 viruses sampled from late 2020 and early 2021 in the United Kingdom. Their genomes carry single nucleotide polymorphisms and deletions that are characteristic of the B.1.1.7 variant of concern, but lack the full complement of lineage-defining mutations. Instead, the remainder of their genomes share contiguous genetic variation with non-B.1.1.7 viruses circulating in the same geographic area at the same time as the recombinants. In four instances there was evidence for onward transmission of a recombinant-origin virus, including one transmission cluster of 45 sequenced cases over the course of two months. The inferred genomic locations of recombination breakpoints suggest that every community-transmitted recombinant virus inherited its spike region from a B.1.1.7 parental virus, consistent with a transmission advantage for B.1.1.7’s set of mutations.

AB - We present evidence for multiple independent origins of recombinant SARS-CoV-2 viruses sampled from late 2020 and early 2021 in the United Kingdom. Their genomes carry single nucleotide polymorphisms and deletions that are characteristic of the B.1.1.7 variant of concern, but lack the full complement of lineage-defining mutations. Instead, the remainder of their genomes share contiguous genetic variation with non-B.1.1.7 viruses circulating in the same geographic area at the same time as the recombinants. In four instances there was evidence for onward transmission of a recombinant-origin virus, including one transmission cluster of 45 sequenced cases over the course of two months. The inferred genomic locations of recombination breakpoints suggest that every community-transmitted recombinant virus inherited its spike region from a B.1.1.7 parental virus, consistent with a transmission advantage for B.1.1.7’s set of mutations.

KW - SARS-CoV-2

KW - evolution

KW - recombination

KW - genomic epidemiology

KW - B.1.1.7

KW - variants

KW - genomics

KW - Base Sequence/genetics

KW - Genome, Viral

KW - Pandemics

KW - SARS-CoV-2/genetics

KW - Gene Frequency

KW - Humans

KW - Genotype

KW - Phylogeny

KW - Computational Biology/methods

KW - United Kingdom/epidemiology

KW - COVID-19/epidemiology

KW - Recombination, Genetic

KW - Polymorphism, Single Nucleotide

KW - Whole Genome Sequencing/methods

KW - Mutation

UR - http://www.scopus.com/inward/record.url?scp=85114700839&partnerID=8YFLogxK

U2 - 10.1016/j.cell.2021.08.014

DO - 10.1016/j.cell.2021.08.014

M3 - Article

C2 - 34499854

SN - 0092-8674

VL - 184

SP - 5179-5188.e8

JO - Cell

JF - Cell

IS - 20

ER -

Generation and transmission of inter-lineage recombinants in the SARS-CoV-2 pandemic

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Keywords

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