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. PereiraPedro 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

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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 (US)
Article number	6544
Journal	Science
Volume	372
Issue number	6544
DOIs	https://doi.org/10.1126/science.abh2644
State	Published - May 21 2021
Externally published	Yes

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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

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

@article{f6b45f35269c423183f20baefe074e8a,

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 (US)",

volume = "372",

journal = "Science",

issn = "0036-8075",

publisher = "American Association for the Advancement of Science",

number = "6544",

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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.

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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

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