Genomics and epidemiology of the P.1 SARS-CoV-2 lineage in Manaus, Brazil

Nuno R. Faria; Thomas A. Mellan; Charles Whittaker; Ingra M. Claro; Darlan Da S. Candido; Swapnil Mishra; Myuki A.E. Crispim; Flavia C.S. Sales; Iwona Hawryluk; John T. McCrone; Ruben J.G. Hulswit; Lucas A.M. Franco; Mariana S. Ramundo; Jaqueline G. De Jesus; Pamela S. Andrade; Thais M. Coletti; Giulia M. Ferreira; Camila A.M. Silva; Erika R. Manuli; Rafael H.M. Pereira; Pedro S. Peixoto; Moritz U.G. Kraemer; Nelson Gaburo; Cecilia Da C. Camilo; Henrique Hoeltgebaum; William M. Souza; Esmenia C. Rocha; Leandro M. De Souza; Mariana C. De Pinho; Leonardo J.T. Araujo; Frederico S.V. Malta; Aline B. De Lima; Joice Do P. Silva; Danielle A.G. Zauli; Alessandro C. Alessandro; Ricardo P. Schnekenberg; Daniel J. Laydon; Patrick G.T. Walker; Hannah M. Schlüter; Ana L.P. Dos Santos; Maria S. Vidal; Valentina S. Del Caro; Rosinaldo M.F. Filho; Helem M. Dos Santos; Renato S. Aguiar; José L. Proença-Modena; Bruce Nelson; James A. Hay; Mélodie Monod; Xenia Miscouridou; Helen Coupland; Raphael Sonabend; Michaela Vollmer; Axel Gandy; Carlos A. Prete; Vitor H. Nascimento; Marc A. Suchard; Thomas A. Bowden; Sergei L.K. Pond; Chieh Hsi Wu; Oliver Ratmann; Neil M. Ferguson; Christopher Dye; Nick J. Loman; Philippe Lemey; Andrew Rambaut; Nelson A. Fraiji; Maria Do P.S.S. Carvalho; Oliver G. Pybus; Seth Flaxman; Samir Bhatt; Ester C. Sabino

doi:10.1126/science.abh2644

Genomics and epidemiology of the P.1 SARS-CoV-2 lineage in Manaus, Brazil

Nuno R. Faria
, Thomas A. Mellan
, Charles Whittaker
, Ingra M. Claro
, Darlan Da S. Candido
, Swapnil Mishra
, Myuki A.E. Crispim
, Flavia C.S. Sales
, Iwona Hawryluk
, John T. McCrone
, Ruben J.G. Hulswit
, Lucas A.M. Franco
, Mariana S. Ramundo
, Jaqueline G. De Jesus
, Pamela S. Andrade
, Thais M. Coletti
, Giulia M. Ferreira
, Camila A.M. Silva
, Erika R. Manuli
, Rafael H.M. Pereira

Pedro S. Peixoto, Moritz U.G. Kraemer, Nelson Gaburo, Cecilia Da C. Camilo, Henrique Hoeltgebaum, William M. Souza, Esmenia C. Rocha, Leandro M. De Souza, Mariana C. De Pinho, Leonardo J.T. Araujo, Frederico S.V. Malta, Aline B. De Lima, Joice Do P. Silva, Danielle A.G. Zauli, Alessandro C. Alessandro, Ricardo P. Schnekenberg, Daniel J. Laydon, Patrick G.T. Walker, Hannah M. Schlüter, Ana L.P. Dos Santos, Maria S. Vidal, Valentina S. Del Caro, Rosinaldo M.F. Filho, Helem M. Dos Santos, Renato S. Aguiar, José L. Proença-Modena, Bruce Nelson, James A. Hay, Mélodie Monod, Xenia Miscouridou, Helen Coupland, Raphael Sonabend, Michaela Vollmer, Axel Gandy, Carlos A. Prete, Vitor H. Nascimento, Marc A. Suchard, Thomas A. Bowden, Sergei L.K. Pond, Chieh Hsi Wu, Oliver Ratmann, Neil M. Ferguson, Christopher Dye, Nick J. Loman, Philippe Lemey, Andrew Rambaut, Nelson A. Fraiji, Maria Do P.S.S. Carvalho, Oliver G. Pybus, Seth Flaxman, Samir Bhatt, Ester C. Sabino

Microbiology, Immunology, and Molecular Genetics

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

1062 Scopus citations

Abstract

Cases of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection in Manaus, Brazil, resurged in late 2020 despite previously high levels of infection. Genome sequencing of viruses sampled in Manaus between November 2020 and January 2021 revealed the emergence and circulation of a novel SARS-CoV-2 variant of concern. Lineage P.1 acquired 17 mutations, including a trio in the spike protein (K417T, E484K, and N501Y) associated with increased binding to the human ACE2 (angiotensin-converting enzyme 2) receptor. Molecular clock analysis shows that P.1 emergence occurred around mid-November 2020 and was preceded by a period of faster molecular evolution. Using a two-category dynamical model that integrates genomic and mortality data, we estimate that P.1 may be 1.7- to 2.4-fold more transmissible and that previous (non-P.1) infection provides 54 to 79% of the protection against infection with P.1 that it provides against non-P.1 lineages. Enhanced global genomic surveillance of variants of concern, which may exhibit increased transmissibility and/or immune evasion, is critical to accelerate pandemic responsiveness.

Original language	English
Article number	6544
Journal	Science
Volume	372
Issue number	6544
DOIs	https://doi.org/10.1126/science.abh2644
State	Published - May 21 2021

Bibliographical note

Publisher Copyright:
Copyright © 2021 The Authors, some rights reserved.

Funding

This work was supported by a Medical Research Council-São Paulo Research Foundation (FAPESP) CADDE partnership award (MR/S0195/1 and FAPESP 18/14389-0) (https://caddecentre.org); FAPESP (E.C.S.: 18/ 14389-0; I.M.C: 2018/17176-8 and 2019/12000-1, F.C.S.S.: 2018/ 25468-9; J.G.d.J.: 2018/17176-8, 2019/12000-1, 18/14389-0; T.M.C.: 2019/07544-2; C.A.M.S.: 2019/21301-5; W.M.S.: 2017/ 13981-0, 2019/24251-9; L.M.d.S.: 2020/04272-9; M.C.d.P.: 2019/ 21568-1; V.H.N.: 2018/12579-7; C.A.P.: 2019/21858-0; and P.S.P.: 16/18445-7; J.L.P.-M.: 2020/04558-0); Wellcome Trust and Royal Society (N.R.F.: Sir Henry Dale Fellowship: 204311/Z/16/Z); Wellcome Trust (Wellcome Centre for Human Genetics: 203141/Z/ 16/Z); Clarendon Fund and Department of Zoology, University of Oxford (D.d.S.C.); Medical Research Council (T.A.B and R.J.G.H: MR/S007555/1); European Molecular Biology Organisation (R.J.G.H.: ALTF 869-2019); CNPq (R.S.A.: 312688/2017-2, 439119/ 2018-9; W.M.S.: 408338/2018-0, 304714/2018-6; V.H.N.: 304714/ 2018-6); FAPERJ (R.S.A.: 202.922/2018); FFMUSP (M.S.R.: 206.706; C.A.P.); Imperial College COVID-19 Research Fund (H.M.S. and S.F.); CAPES (G.M.F. and C.A.P., Code 001); Wellcome Trust Collaborator Award (P.L., A.R., and N.J.L.: 206298/Z/17/Z); European Research Council (P.L and A.R.: 725422-ReservoirDOCS); European Union's Horizon 2020 project MOOD (P.L. and M.U.G.K.: 874850); U.S. National Institutes of Health (M.A.S.: U19 AI135995); Oxford Martin School (O.G.P.); Branco Weiss Fellowship (M.U.G.K); Covid-19 Research Fund (S.F.); EPSRC (S.F.: EP/V002910/1; M.M. through the EPSRC Centre for Doctoral Training in Modern Statistics and Statistical Machine Learning); BMGF (S.B.); UKRI (S.B.); Novo Nordisk Foundation (S.B.); Academy of Medical Sciences (S.B.); BRC (S.B.); MRC (S.B.); and Bill & Melinda Gates Foundation (O.R.: OPP1175094). We acknowledge support from the Rede Corona-ômica BR MCTI/ FINEP affiliated to RedeVírus/MCTI (FINEP 01.20.0029.000462/ 20, CNPq 404096/2020-4), FAPESP project 2018/12579-7 CNPq project 304714/2018-6 (V.H.N.), EPSRC Centre for Doctoral Training in Modern Statistics and Statistical Machine Learning at Imperial and Oxford (M.M.), and the Bill & Melinda Gates Foundation (OPP1175094) (O.R.). This work received funding from the UK Medical Research Council under a concordat with the UK Department for International Development. We additionally acknowledge support from Community Jameel and the NIHR Health Protection Research Unit in Modelling Methodology. Last, we also gratefully acknowledge support from Oxford Nanopore Technologies for a donation of sequencing reagents and NVIDIA Corporation and Advanced Micro Devices for a donation of parallel computing resources.

Funders	Funder number
NIHR Imperial Biomedical Research Centre
Oxford Martin School, University of Oxford
Branco Weiss Fellowship
National Institute for Health and Care Research
National Institutes of Health (NIH)
Medical Research Council-São Paulo Research Foundation
European Commission
Department of Zoology, University of Oxford
Imperial College COVID-19 Research Fund
Department for International Development, UK Government
Oxford Nanopore Technologies
Rede Corona-ômica BR MCTI
Chinese Academy of Medical Sciences Innovation Fund for Medical Sciences
H2020 European Research Council
Novo Nordisk Fonden
Nvidia
Clarendon Fund
UK Industrial Decarbonization Research and Innovation Centre
UK Medical Research Council, Engineering and Physical Sciences Research Council	MR/V038109/1, MR/S007555/1, MR/S019510/1, EP/V002910/1
Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro	202.922/2018
FFMUSP	206.706
Conselho Nacional de Desenvolvimento Científico e Tecnológico	408338/2018-0, 439119/ 2018-9, 312688/2017-2, 304714/2018-6
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior	206298/Z/17/Z
Horizon 2020 Framework Programme	874850, 725422
Wellcome Trust	203141, 206298
National Institute of Allergy and Infectious F32-AI286447 Cydney N. Johnson Diseases National Institute of Allergy and Infectious R01AI168214 Jason W. Rosch Diseases National Institute of Allergy and Infectious P30 Cydney N. Johnson Diseases National Institute of Allergy and Infectious R00-AI166116 Christopher D. Radka Diseases National Institute of Allergy and Infectious T32-AI106700 Cydney N. Johnson Diseases National Institute of Allergy and Infectious R01AI192221 Jason W. Rosch Diseases National Inst...	U19AI135995
European Molecular Biology Organization	ALTF 869-2019
Fundação de Amparo à Pesquisa do Estado de São Paulo	2018/17176-8, 2017/ 13981-0, 2019/21301-5, 16/18445-7, 2020/04558-0, 2019/24251-9, 2018/12579-7, 2019/21858-0, 2019/ 21568-1, 2019/07544-2, 2018/ 25468-9, 18/14389-0, 2020/04272-9, MR/S0195/1, 2019/12000-1
Ministério da Ciência, Tecnologia e Inovação	404096/2020-4
Bill and Melinda Gates Foundation	OPP1175094
Royal Society of Medicine	204311/Z/16/Z, 203141/Z/ 16/Z

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being

ASJC Scopus subject areas

General

Access to Document

10.1126/science.abh2644

Cite this

Faria, N. R., Mellan, T. A., Whittaker, C., Claro, I. M., Candido, D. D. S., Mishra, S., Crispim, M. A. E., Sales, F. C. S., Hawryluk, I., McCrone, J. T., Hulswit, R. J. G., Franco, L. A. M., Ramundo, M. S., De Jesus, J. G., Andrade, P. S., Coletti, T. M., Ferreira, G. M., Silva, C. A. M., Manuli, E. R., ... Sabino, E. C. (2021). Genomics and epidemiology of the P.1 SARS-CoV-2 lineage in Manaus, Brazil. Science, 372(6544), Article 6544. https://doi.org/10.1126/science.abh2644

@article{3cf2db8d56a8420094ccb786b0b9353d,

title = "Genomics and epidemiology of the P.1 SARS-CoV-2 lineage in Manaus, Brazil",

abstract = "Cases of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection in Manaus, Brazil, resurged in late 2020 despite previously high levels of infection. Genome sequencing of viruses sampled in Manaus between November 2020 and January 2021 revealed the emergence and circulation of a novel SARS-CoV-2 variant of concern. Lineage P.1 acquired 17 mutations, including a trio in the spike protein (K417T, E484K, and N501Y) associated with increased binding to the human ACE2 (angiotensin-converting enzyme 2) receptor. Molecular clock analysis shows that P.1 emergence occurred around mid-November 2020 and was preceded by a period of faster molecular evolution. Using a two-category dynamical model that integrates genomic and mortality data, we estimate that P.1 may be 1.7- to 2.4-fold more transmissible and that previous (non-P.1) infection provides 54 to 79\% of the protection against infection with P.1 that it provides against non-P.1 lineages. Enhanced global genomic surveillance of variants of concern, which may exhibit increased transmissibility and/or immune evasion, is critical to accelerate pandemic responsiveness.",

author = "Faria, \{Nuno R.\} and Mellan, \{Thomas A.\} and Charles Whittaker and Claro, \{Ingra M.\} and Candido, \{Darlan Da S.\} and Swapnil Mishra and Crispim, \{Myuki A.E.\} and Sales, \{Flavia C.S.\} and Iwona Hawryluk and McCrone, \{John T.\} and Hulswit, \{Ruben J.G.\} and Franco, \{Lucas A.M.\} and Ramundo, \{Mariana S.\} and \{De Jesus\}, \{Jaqueline G.\} and Andrade, \{Pamela S.\} and Coletti, \{Thais M.\} and Ferreira, \{Giulia M.\} and Silva, \{Camila A.M.\} and Manuli, \{Erika R.\} and Pereira, \{Rafael H.M.\} and Peixoto, \{Pedro S.\} and Kraemer, \{Moritz U.G.\} and Nelson Gaburo and Camilo, \{Cecilia Da C.\} and Henrique Hoeltgebaum and Souza, \{William M.\} and Rocha, \{Esmenia C.\} and \{De Souza\}, \{Leandro M.\} and \{De Pinho\}, \{Mariana C.\} and Araujo, \{Leonardo J.T.\} and Malta, \{Frederico S.V.\} and \{De Lima\}, \{Aline B.\} and Silva, \{Joice Do P.\} and Zauli, \{Danielle A.G.\} and Alessandro, \{Alessandro C.\} and Schnekenberg, \{Ricardo P.\} and Laydon, \{Daniel J.\} and Walker, \{Patrick G.T.\} and Schl{\"u}ter, \{Hannah M.\} and \{Dos Santos\}, \{Ana L.P.\} and Vidal, \{Maria S.\} and \{Del Caro\}, \{Valentina S.\} and Filho, \{Rosinaldo M.F.\} and \{Dos Santos\}, \{Helem M.\} and Aguiar, \{Renato S.\} and Proen{\c c}a-Modena, \{Jos{\'e} L.\} and Bruce Nelson and Hay, \{James A.\} and M{\'e}lodie Monod and Xenia Miscouridou and Helen Coupland and Raphael Sonabend and Michaela Vollmer and Axel Gandy and Prete, \{Carlos A.\} and Nascimento, \{Vitor H.\} and Suchard, \{Marc A.\} and Bowden, \{Thomas A.\} and Pond, \{Sergei L.K.\} and Wu, \{Chieh Hsi\} and Oliver Ratmann and Ferguson, \{Neil M.\} and Christopher Dye and Loman, \{Nick J.\} and Philippe Lemey and Andrew Rambaut and Fraiji, \{Nelson A.\} and Carvalho, \{Maria Do P.S.S.\} and Pybus, \{Oliver G.\} and Seth Flaxman and Samir Bhatt and Sabino, \{Ester C.\}",

note = "Publisher Copyright: Copyright {\textcopyright} 2021 The Authors, some rights reserved.",

year = "2021",

month = may,

day = "21",

doi = "10.1126/science.abh2644",

language = "English",

volume = "372",

number = "6544",

}

Faria, NR, Mellan, TA, Whittaker, C, Claro, IM, Candido, DDS, Mishra, S, Crispim, MAE, Sales, FCS, Hawryluk, I, McCrone, JT, Hulswit, RJG, Franco, LAM, Ramundo, MS, De Jesus, JG, Andrade, PS, Coletti, TM, Ferreira, GM, Silva, CAM, Manuli, ER, Pereira, RHM, Peixoto, PS, Kraemer, MUG, Gaburo, N, Camilo, CDC, Hoeltgebaum, H, Souza, WM, Rocha, EC, De Souza, LM, De Pinho, MC, Araujo, LJT, Malta, FSV, De Lima, AB, Silva, JDP, Zauli, DAG, Alessandro, AC, Schnekenberg, RP, Laydon, DJ, Walker, PGT, Schlüter, HM, Dos Santos, ALP, Vidal, MS, Del Caro, VS, Filho, RMF, Dos Santos, HM, Aguiar, RS, Proença-Modena, JL, Nelson, B, Hay, JA, Monod, M, Miscouridou, X, Coupland, H, Sonabend, R, Vollmer, M, Gandy, A, Prete, CA, Nascimento, VH, Suchard, MA, Bowden, TA, Pond, SLK, Wu, CH, Ratmann, O, Ferguson, NM, Dye, C, Loman, NJ, Lemey, P, Rambaut, A, Fraiji, NA, Carvalho, MDPSS, Pybus, OG, Flaxman, S, Bhatt, S & Sabino, EC 2021, 'Genomics and epidemiology of the P.1 SARS-CoV-2 lineage in Manaus, Brazil', Science, vol. 372, no. 6544, 6544. https://doi.org/10.1126/science.abh2644

TY - JOUR

T1 - Genomics and epidemiology of the P.1 SARS-CoV-2 lineage in Manaus, Brazil

AU - Faria, Nuno R.

AU - Mellan, Thomas A.

AU - Whittaker, Charles

AU - Claro, Ingra M.

AU - Candido, Darlan Da S.

AU - Mishra, Swapnil

AU - Crispim, Myuki A.E.

AU - Sales, Flavia C.S.

AU - Hawryluk, Iwona

AU - McCrone, John T.

AU - Hulswit, Ruben J.G.

AU - Franco, Lucas A.M.

AU - Ramundo, Mariana S.

AU - De Jesus, Jaqueline G.

AU - Andrade, Pamela S.

AU - Coletti, Thais M.

AU - Ferreira, Giulia M.

AU - Silva, Camila A.M.

AU - Manuli, Erika R.

AU - Pereira, Rafael H.M.

AU - Peixoto, Pedro S.

AU - Kraemer, Moritz U.G.

AU - Gaburo, Nelson

AU - Camilo, Cecilia Da C.

AU - Hoeltgebaum, Henrique

AU - Souza, William M.

AU - Rocha, Esmenia C.

AU - De Souza, Leandro M.

AU - De Pinho, Mariana C.

AU - Araujo, Leonardo J.T.

AU - Malta, Frederico S.V.

AU - De Lima, Aline B.

AU - Silva, Joice Do P.

AU - Zauli, Danielle A.G.

AU - Alessandro, Alessandro C.

AU - Schnekenberg, Ricardo P.

AU - Laydon, Daniel J.

AU - Walker, Patrick G.T.

AU - Schlüter, Hannah M.

AU - Dos Santos, Ana L.P.

AU - Vidal, Maria S.

AU - Del Caro, Valentina S.

AU - Filho, Rosinaldo M.F.

AU - Dos Santos, Helem M.

AU - Aguiar, Renato S.

AU - Proença-Modena, José L.

AU - Nelson, Bruce

AU - Hay, James A.

AU - Monod, Mélodie

AU - Miscouridou, Xenia

AU - Coupland, Helen

AU - Sonabend, Raphael

AU - Vollmer, Michaela

AU - Gandy, Axel

AU - Prete, Carlos A.

AU - Nascimento, Vitor H.

AU - Suchard, Marc A.

AU - Bowden, Thomas A.

AU - Pond, Sergei L.K.

AU - Wu, Chieh Hsi

AU - Ratmann, Oliver

AU - Ferguson, Neil M.

AU - Dye, Christopher

AU - Loman, Nick J.

AU - Lemey, Philippe

AU - Rambaut, Andrew

AU - Fraiji, Nelson A.

AU - Carvalho, Maria Do P.S.S.

AU - Pybus, Oliver G.

AU - Flaxman, Seth

AU - Bhatt, Samir

AU - Sabino, Ester C.

PY - 2021/5/21

Y1 - 2021/5/21

N2 - Cases of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection in Manaus, Brazil, resurged in late 2020 despite previously high levels of infection. Genome sequencing of viruses sampled in Manaus between November 2020 and January 2021 revealed the emergence and circulation of a novel SARS-CoV-2 variant of concern. Lineage P.1 acquired 17 mutations, including a trio in the spike protein (K417T, E484K, and N501Y) associated with increased binding to the human ACE2 (angiotensin-converting enzyme 2) receptor. Molecular clock analysis shows that P.1 emergence occurred around mid-November 2020 and was preceded by a period of faster molecular evolution. Using a two-category dynamical model that integrates genomic and mortality data, we estimate that P.1 may be 1.7- to 2.4-fold more transmissible and that previous (non-P.1) infection provides 54 to 79% of the protection against infection with P.1 that it provides against non-P.1 lineages. Enhanced global genomic surveillance of variants of concern, which may exhibit increased transmissibility and/or immune evasion, is critical to accelerate pandemic responsiveness.

AB - Cases of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection in Manaus, Brazil, resurged in late 2020 despite previously high levels of infection. Genome sequencing of viruses sampled in Manaus between November 2020 and January 2021 revealed the emergence and circulation of a novel SARS-CoV-2 variant of concern. Lineage P.1 acquired 17 mutations, including a trio in the spike protein (K417T, E484K, and N501Y) associated with increased binding to the human ACE2 (angiotensin-converting enzyme 2) receptor. Molecular clock analysis shows that P.1 emergence occurred around mid-November 2020 and was preceded by a period of faster molecular evolution. Using a two-category dynamical model that integrates genomic and mortality data, we estimate that P.1 may be 1.7- to 2.4-fold more transmissible and that previous (non-P.1) infection provides 54 to 79% of the protection against infection with P.1 that it provides against non-P.1 lineages. Enhanced global genomic surveillance of variants of concern, which may exhibit increased transmissibility and/or immune evasion, is critical to accelerate pandemic responsiveness.

UR - https://www.scopus.com/pages/publications/85105876512

UR - https://www.scopus.com/pages/publications/85105876512#tab=citedBy

U2 - 10.1126/science.abh2644

DO - 10.1126/science.abh2644

M3 - Article

C2 - 33853970

AN - SCOPUS:85105876512

SN - 0036-8075

VL - 372

JO - Science

JF - Science

IS - 6544

M1 - 6544

ER -

Genomics and epidemiology of the P.1 SARS-CoV-2 lineage in Manaus, Brazil

Abstract

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