Generation and transmission of interlineage 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

doi:10.1016/j.cell.2021.08.014

Generation and transmission of interlineage 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

School of Nursing, Midwifery and Health

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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 2 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
Article number	e8
Pages (from-to)	5179-5188
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

Bibliographical note

This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/)

Funder

The COG-UK Consortium is supported by funding from the Medical Research Council (MRC) part of UK Research & Innovation (UKRI), the National Institute of Health Research (NIHR) (MC_PC_19027), and Genome Research Limited , operating as the Wellcome Sanger Institute . O.G.P. was supported by the Oxford Martin School . J.T.M., R.M.C., N.J.L., and A.R. acknowledge the support of the Wellcome Trust (Collaborators Award 206298/Z/17/Z – ARTIC network ). D.L.R. acknowledges the support of the MRC ( MC_UU_12014/12 ) and the Wellcome Trust ( 220977/Z/20/Z ). E.S. and A.R. are supported by the European Research Council (grant agreement no. 725422 – ReservoirDOCS ). T.R.C. and N.J.L. acknowledge the support of the MRC , which provided the funding for the MRC CLIMB infrastructure used to analyze, store, and share the UK sequencing dataset ( MR/L015080/1 and MR/T030062/1 ). The samples sequenced in Wales were sequenced partly using funding provided by the Welsh Government .

Funding

The COG-UK Consortium is supported by funding from the Medical Research Council (MRC) part of UK Research & Innovation (UKRI), the National Institute of Health Research (NIHR) (MC_PC_19027), and Genome Research Limited , operating as the Wellcome Sanger Institute . O.G.P. was supported by the Oxford Martin School . J.T.M., R.M.C., N.J.L., and A.R. acknowledge the support of the Wellcome Trust (Collaborators Award 206298/Z/17/Z – ARTIC network ). D.L.R. acknowledges the support of the MRC ( MC_UU_12014/12 ) and the Wellcome Trust ( 220977/Z/20/Z ). E.S. and A.R. are supported by the European Research Council (grant agreement no. 725422 – ReservoirDOCS ). T.R.C. and N.J.L. acknowledge the support of the MRC , which provided the funding for the MRC CLIMB infrastructure used to analyze, store, and share the UK sequencing dataset ( MR/L015080/1 and MR/T030062/1 ). The samples sequenced in Wales were sequenced partly using funding provided by the Welsh Government .

Funders	Funder number
Medical Research Council
UK Research and Innovation
National Institute for Health and Care Research	MC_PC_19027
Wellcome Trust Sanger Institute
University of Oxford
Wellcome Trust	206298/Z/17/Z
European Research Council	725422 – ReservoirDOCS
Welsh Government

Keywords

SARS-CoV-2
genomics
evolution
recombination
genomic epidemiology
B.1.1.7
variants

ASJC Scopus subject areas

General Biochemistry,Genetics and Molecular Biology

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10.1016/j.cell.2021.08.014Licence: CC BY

Bridgewater2021VoRFinal published version, 2.99 MBLicence: CC BY

Cite this

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., ... Rambaut, A. (2021). Generation and transmission of interlineage recombinants in the SARS-CoV-2 pandemic. Cell, 184(20), 5179-5188. Article e8. https://doi.org/10.1016/j.cell.2021.08.014

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 2021, 'Generation and transmission of interlineage recombinants in the SARS-CoV-2 pandemic', Cell, vol. 184, no. 20, e8, pp. 5179-5188. https://doi.org/10.1016/j.cell.2021.08.014

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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 2 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.",

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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 - Davies, Robert

AU - Bridgewater, Hannah E.

N1 - This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/)

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 2 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 2 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.

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KW - evolution

KW - recombination

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SP - 5179

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JO - Cell

JF - Cell

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ER -

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

Abstract

Bibliographical note

Funder

Funding

Keywords

ASJC Scopus subject areas

Access to Document

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