Rapid spread of the SARS-CoV-2 Omicron XDR lineage derived from recombination between XBB and BA.2.86 subvariants circulating in Brazil in late 2023

ABSTRACT Recombination plays a crucial role in the evolution of SARS-CoV-2. The Omicron XBB* recombinant lineages are a noteworthy example, as they have been the dominant SARS-CoV-2 variant worldwide in the first half of 2023. Since November 2023, a new recombinant lineage between Omicron subvariant...

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Main Authors: Ighor Arantes, Kimihito Ito, Marcelo Gomes, Felipe Cotrim de Carvalho, Walquiria Aparecida Ferreira de Almeida, Ricardo Khouri, Fabio Miyajima, Gabriel Luz Wallau, Felipe Gomes Naveca, Elisa Cavalcante Pereira, Marilda Mendonça Siqueira, Paola Cristina Resende, Gonzalo Bello
Format: Article
Language:English
Published: American Society for Microbiology 2025-01-01
Series:Microbiology Spectrum
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Online Access:https://journals.asm.org/doi/10.1128/spectrum.01193-24
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author Ighor Arantes
Kimihito Ito
Marcelo Gomes
Felipe Cotrim de Carvalho
Walquiria Aparecida Ferreira de Almeida
Ricardo Khouri
Fabio Miyajima
Gabriel Luz Wallau
Felipe Gomes Naveca
Elisa Cavalcante Pereira
Marilda Mendonça Siqueira
Paola Cristina Resende
Gonzalo Bello
author_facet Ighor Arantes
Kimihito Ito
Marcelo Gomes
Felipe Cotrim de Carvalho
Walquiria Aparecida Ferreira de Almeida
Ricardo Khouri
Fabio Miyajima
Gabriel Luz Wallau
Felipe Gomes Naveca
Elisa Cavalcante Pereira
Marilda Mendonça Siqueira
Paola Cristina Resende
Gonzalo Bello
author_sort Ighor Arantes
collection DOAJ
description ABSTRACT Recombination plays a crucial role in the evolution of SARS-CoV-2. The Omicron XBB* recombinant lineages are a noteworthy example, as they have been the dominant SARS-CoV-2 variant worldwide in the first half of 2023. Since November 2023, a new recombinant lineage between Omicron subvariants XBB and BA.2.86, designated XDR, has been detected mainly in Brazil. In this study, we reconstructed the spatiotemporal dynamics and estimated the absolute and relative transmissibility of the XDR lineage. The XDR lineage displayed a recombination breakpoint in the ORF1a-coding region, and the most closely related sequences to the 5′ and 3′ ends of the recombinant correspond to JD.1.1 and JN.1.1 lineages, respectively. The first XDR sequences were detected in November 2023 in the Northeastern Brazilian region, and their prevalence rapidly surged from <1% to 25% by February 2024. The Bayesian phylogeographic analysis supports that the XDR lineage likely emerged in the Northeastern Brazilian region around late October 2023 and rapidly disseminated within and outside Brazilian borders from mid-November onward. The median effective reproductive number of the XDR lineage in Brazil during the initial expansion phase was estimated to be around 1.5, and the average relative instantaneous reproduction numbers of XDR and JN* lineages were estimated to be 1.37 and 1.29 higher than that of co-circulating XBB* lineages. In summary, these findings support that the recombinant lineage XDR arose in the Northeastern Brazilian region in October 2023, shortly after the first detection of JN.1 sequences in the country. In Brazil, the XDR lineage exhibited a higher transmissibility level than its parental XBB.* lineages and is spreading at a rate similar to or slightly faster than the JN.1* lineages.IMPORTANCEThis study highlights the emergence and rapid dissemination of the recombinant SARS-CoV-2 XDR lineage, derived from the Omicron lineages JD.1.1 and JN.1.1. The XDR lineage exhibited equivalent transmissibility to its JN.1* parental lineages and quickly spread across Brazil in late 2023. The findings underscore the critical role of real-time genomic surveillance in detecting novel variants with higher transmission potential. By utilizing phylogenetic and epidemiological methods, this research provides important insights into the molecular dynamics of XDR, which could inform public health responses and vaccine composition updates. The study’s significance lies in its ability to document the impact of recombination on viral evolution, offering valuable information to the field of virology and pandemic preparedness.
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spelling doaj-art-84758870fbfd4229aa134e362c95e7922025-01-07T14:05:19ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972025-01-0113110.1128/spectrum.01193-24Rapid spread of the SARS-CoV-2 Omicron XDR lineage derived from recombination between XBB and BA.2.86 subvariants circulating in Brazil in late 2023Ighor Arantes0Kimihito Ito1Marcelo Gomes2Felipe Cotrim de Carvalho3Walquiria Aparecida Ferreira de Almeida4Ricardo Khouri5Fabio Miyajima6Gabriel Luz Wallau7Felipe Gomes Naveca8Elisa Cavalcante Pereira9Marilda Mendonça Siqueira10Paola Cristina Resende11Gonzalo Bello12Laboratório de Arbovírus e Vírus Hemorrágicos, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, BrazilInternational Institute for Zoonosis Control, Hokkaido University, Hokkaido, JapanGrupo de Métodos Analíticos em Vigilância Epidemiológica, Fiocruz, Rio de Janeiro, BrazilDepartamento do Programa Nacional de Imunizações, Coordenação-Geral de Vigilância das doenças imunopreveníveis, Secretaria de Vigilância em saúde e ambiente, Brasília, BrazilDepartamento do Programa Nacional de Imunizações, Coordenação-Geral de Vigilância das doenças imunopreveníveis, Secretaria de Vigilância em saúde e ambiente, Brasília, BrazilInstituto Gonçalo Moniz, Fiocruz, Salvador, BrazilFiocruz Ceará, Fortaleza, Brazil7Department of Arbovirology, Bernhard Nocht Institute for Tropical Medicine, WHO Collaborating Center for Arbovirus and Hemorrhagic Fever Reference and Research, National Reference Center for Tropical Infectious Diseases, Hamburg, GermanyLaboratório de Arbovírus e Vírus Hemorrágicos, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, BrazilLaboratório de Vírus Respiratórios, Exantemáticos, Enterovírus e Emergências Virais, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, BrazilLaboratório de Vírus Respiratórios, Exantemáticos, Enterovírus e Emergências Virais, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, BrazilLaboratório de Vírus Respiratórios, Exantemáticos, Enterovírus e Emergências Virais, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, BrazilLaboratório de Arbovírus e Vírus Hemorrágicos, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, BrazilABSTRACT Recombination plays a crucial role in the evolution of SARS-CoV-2. The Omicron XBB* recombinant lineages are a noteworthy example, as they have been the dominant SARS-CoV-2 variant worldwide in the first half of 2023. Since November 2023, a new recombinant lineage between Omicron subvariants XBB and BA.2.86, designated XDR, has been detected mainly in Brazil. In this study, we reconstructed the spatiotemporal dynamics and estimated the absolute and relative transmissibility of the XDR lineage. The XDR lineage displayed a recombination breakpoint in the ORF1a-coding region, and the most closely related sequences to the 5′ and 3′ ends of the recombinant correspond to JD.1.1 and JN.1.1 lineages, respectively. The first XDR sequences were detected in November 2023 in the Northeastern Brazilian region, and their prevalence rapidly surged from <1% to 25% by February 2024. The Bayesian phylogeographic analysis supports that the XDR lineage likely emerged in the Northeastern Brazilian region around late October 2023 and rapidly disseminated within and outside Brazilian borders from mid-November onward. The median effective reproductive number of the XDR lineage in Brazil during the initial expansion phase was estimated to be around 1.5, and the average relative instantaneous reproduction numbers of XDR and JN* lineages were estimated to be 1.37 and 1.29 higher than that of co-circulating XBB* lineages. In summary, these findings support that the recombinant lineage XDR arose in the Northeastern Brazilian region in October 2023, shortly after the first detection of JN.1 sequences in the country. In Brazil, the XDR lineage exhibited a higher transmissibility level than its parental XBB.* lineages and is spreading at a rate similar to or slightly faster than the JN.1* lineages.IMPORTANCEThis study highlights the emergence and rapid dissemination of the recombinant SARS-CoV-2 XDR lineage, derived from the Omicron lineages JD.1.1 and JN.1.1. The XDR lineage exhibited equivalent transmissibility to its JN.1* parental lineages and quickly spread across Brazil in late 2023. The findings underscore the critical role of real-time genomic surveillance in detecting novel variants with higher transmission potential. By utilizing phylogenetic and epidemiological methods, this research provides important insights into the molecular dynamics of XDR, which could inform public health responses and vaccine composition updates. The study’s significance lies in its ability to document the impact of recombination on viral evolution, offering valuable information to the field of virology and pandemic preparedness.https://journals.asm.org/doi/10.1128/spectrum.01193-24SARS-CoV-2XDRBrazilrecombinationphylogeography
spellingShingle Ighor Arantes
Kimihito Ito
Marcelo Gomes
Felipe Cotrim de Carvalho
Walquiria Aparecida Ferreira de Almeida
Ricardo Khouri
Fabio Miyajima
Gabriel Luz Wallau
Felipe Gomes Naveca
Elisa Cavalcante Pereira
Marilda Mendonça Siqueira
Paola Cristina Resende
Gonzalo Bello
Rapid spread of the SARS-CoV-2 Omicron XDR lineage derived from recombination between XBB and BA.2.86 subvariants circulating in Brazil in late 2023
Microbiology Spectrum
SARS-CoV-2
XDR
Brazil
recombination
phylogeography
title Rapid spread of the SARS-CoV-2 Omicron XDR lineage derived from recombination between XBB and BA.2.86 subvariants circulating in Brazil in late 2023
title_full Rapid spread of the SARS-CoV-2 Omicron XDR lineage derived from recombination between XBB and BA.2.86 subvariants circulating in Brazil in late 2023
title_fullStr Rapid spread of the SARS-CoV-2 Omicron XDR lineage derived from recombination between XBB and BA.2.86 subvariants circulating in Brazil in late 2023
title_full_unstemmed Rapid spread of the SARS-CoV-2 Omicron XDR lineage derived from recombination between XBB and BA.2.86 subvariants circulating in Brazil in late 2023
title_short Rapid spread of the SARS-CoV-2 Omicron XDR lineage derived from recombination between XBB and BA.2.86 subvariants circulating in Brazil in late 2023
title_sort rapid spread of the sars cov 2 omicron xdr lineage derived from recombination between xbb and ba 2 86 subvariants circulating in brazil in late 2023
topic SARS-CoV-2
XDR
Brazil
recombination
phylogeography
url https://journals.asm.org/doi/10.1128/spectrum.01193-24
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