Divergent SARS-CoV-2 variant emerges in white-tailed deer with deer-to-human transmission

Bradley Pickering; Oliver Lung; Finlay Maguire; Peter Kruczkiewicz; Jonathon D. Kotwa; Tore Buchanan; Marianne Gagnier; Jennifer L. Guthrie; Claire M. Jardine; Alex Marchand-Austin; Ariane Massé; Heather McClinchey; Kuganya Nirmalarajah; Patryk Aftanas; Juliette Blais-Savoie; Hsien Yao Chee; Emily Chien; Winfield Yim; Andra Banete; Bryan D. Griffin; Lily Yip; Melissa Goolia; Matthew Suderman; Mathieu Pinette; Greg Smith; Daniel Sullivan; Josip Rudar; Oksana Vernygora; Elizabeth Adey; Michelle Nebroski; Guillaume Goyette; Andrés Finzi; Geneviève Laroche; Ardeshir Ariana; Brett Vahkal; Marceline Côté; Allison J. McGeer; Larissa Nituch; Samira Mubareka; Jeff Bowman

doi:10.1038/s41564-022-01268-9

Divergent SARS-CoV-2 variant emerges in white-tailed deer with deer-to-human transmission

Bradley Pickering, Oliver Lung, Finlay Maguire, Peter Kruczkiewicz, Jonathon D. Kotwa, Tore Buchanan, Marianne Gagnier, Jennifer L. Guthrie, Claire M. Jardine, Alex Marchand-Austin, Ariane Massé, Heather McClinchey, Kuganya Nirmalarajah, Patryk Aftanas, Juliette Blais-Savoie, Hsien Yao Chee, Emily Chien, Winfield Yim, Andra Banete, Bryan D. GriffinLily Yip, Melissa Goolia, Matthew Suderman, Mathieu Pinette, Greg Smith, Daniel Sullivan, Josip Rudar, Oksana Vernygora, Elizabeth Adey, Michelle Nebroski, Guillaume Goyette, Andrés Finzi, Geneviève Laroche, Ardeshir Ariana, Brett Vahkal, Marceline Côté, Allison J. McGeer, Larissa Nituch, Samira Mubareka, Jeff Bowman

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119 Citas (Scopus)

Resumen

Wildlife reservoirs of broad-host-range viruses have the potential to enable evolution of viral variants that can emerge to infect humans. In North America, there is phylogenomic evidence of continual transmission of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) from humans to white-tailed deer (Odocoileus virginianus) through unknown means, but no evidence of transmission from deer to humans. We carried out an observational surveillance study in Ontario, Canada during November and December 2021 (n = 300 deer) and identified a highly divergent lineage of SARS-CoV-2 in white-tailed deer (B.1.641). This lineage is one of the most divergent SARS-CoV-2 lineages identified so far, with 76 mutations (including 37 previously associated with non-human mammalian hosts). From a set of five complete and two partial deer-derived viral genomes we applied phylogenomic, recombination, selection and mutation spectrum analyses, which provided evidence for evolution and transmission in deer and a shared ancestry with mink-derived virus. Our analysis also revealed an epidemiologically linked human infection. Taken together, our findings provide evidence for sustained evolution of SARS-CoV-2 in white-tailed deer and of deer-to-human transmission.

Idioma original	English
Publicación	Nature Microbiology
DOI	https://doi.org/10.1038/s41564-022-01268-9
Estado	Accepted/In press - 2022

Nota bibliográfica

Funding Information:
We acknowledge the contributions of the Virus Detection, Molecular Diagnostics, DNA Core sections and the Biocomputing Centre of Public Health Ontario, and in particular S. Teatero for leading the genome sequencing efforts. We gratefully acknowledge contributions of SARS-CoV-2 genome sequences from other laboratories through GISAID (Supplementary Table ). We thank the licensed Ontario deer hunters who submitted samples for wildlife disease surveillance, the staff of MNRF’s CWD surveillance programme for their assistance with sample collection, and S. Hagey for GIS support. We also acknowledge the contributions of CFIA NCFAD’s Genomics Unit for their assistance with additional laboratory support and sequencing. S.M. and B.P. are members of the Canada and the Canadian Institutes for Health Research Coronavirus Variants Rapid Response Network (CoVaRR-Net). We are grateful to D. Bulir from McMaster University for providing the primer and probe sequences for the 5′ UTR RT–PCR SARS-CoV-2 PCR assay, and to M. Taipale for cathepsin L knock-out TMPRSS2-overexpressing Vero cells. We appreciate the Public Health Agency of Canada for uploading the raw sequencing data for the Public Health Ontario human sequence to the Short Read Archive. The CV3-25 antibody was produced using the pTT vector kindly provided by the Canada Research Council. We also thank D. Leclair, J. Provencher, C. Soos and A. Wilcox (Environment and Climate Change Canada) for comments on an earlier draft of the manuscript. Ethical approvals for this work were provided by Sinai Health System Research Ethics Board (#22-0030-E), Sunnybrook HSC Research Ethics Board (#SUN-2218) and University of Ottawa Research Ethics Board (#H-01-22-7842). Funding to S.M. was provided by the Public Health Agency of Canada and the Canadian Institutes for Health Research Operating grant: Emerging COVID-19 Research Gaps and Priorities #466984. J.D.K. was supported by the Association of Medical Microbiology and Infectious Diseases (AMMI) Canada 2020 AMMI Canada/Biomérieux Post Residency Fellowship in Microbial Diagnostics (unrestricted). Funding and computing resources for F.M. were provided by the Shared Hospital Laboratory, Dalhousie University and the Donald Hill Family. Funding for B.P. was provided by the Canadian Food Inspection Agency and the Canadian Safety and Security Program. Funding to J.B., T.B. and L.N. was provided by MNRF and the Public Health Agency of Canada. Funding for O.L. was from the Canadian Safety and Security Program, Laboratories Canada and CFIA. A.F. is the recipient of Canada Research Chair on Retroviral Entry no. RCHS0235 950-232424. M.C. is a Canada Research Chair in Molecular Virology and Antiviral Therapeutics (950-232840) and a recipient of an Ontario Ministry of Research, Innovation and Science Early Researcher Award (ER18-14-09). Funding to M.C. was provided by a COVID-19 Rapid Research grant from the Canadian Institutes for Health Research (CIHR, OV3 170632), CIHR stream 1 for SARS-CoV-2 Variant Research. Work from M.C. and A.F. is also supported by the Sentinelle COVID Quebec network led by the Laboratoire de Santé Publique du Québec (LSPQ) in collaboration with Fonds de Recherche du Québec-Santé (FRQS) and Genome Canada—Génome Québec, and by the Ministère de la Santé et des Services Sociaux (MSSS) and the Ministère de l’Économie et Innovation (MEI).

Publisher Copyright:
© 2022, The Author(s).

ASJC Scopus Subject Areas

Microbiology
Immunology
Applied Microbiology and Biotechnology
Genetics
Microbiology (medical)
Cell Biology

PubMed: MeSH publication types

Journal Article

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10.1038/s41564-022-01268-9

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Pickering, B., Lung, O., Maguire, F., Kruczkiewicz, P., Kotwa, J. D., Buchanan, T., Gagnier, M., Guthrie, J. L., Jardine, C. M., Marchand-Austin, A., Massé, A., McClinchey, H., Nirmalarajah, K., Aftanas, P., Blais-Savoie, J., Chee, H. Y., Chien, E., Yim, W., Banete, A., ... Bowman, J. (Aceptado/En prensa). Divergent SARS-CoV-2 variant emerges in white-tailed deer with deer-to-human transmission. Nature Microbiology. https://doi.org/10.1038/s41564-022-01268-9

Pickering, B, Lung, O, Maguire, F, Kruczkiewicz, P, Kotwa, JD, Buchanan, T, Gagnier, M, Guthrie, JL, Jardine, CM, Marchand-Austin, A, Massé, A, McClinchey, H, Nirmalarajah, K, Aftanas, P, Blais-Savoie, J, Chee, HY, Chien, E, Yim, W, Banete, A, Griffin, BD, Yip, L, Goolia, M, Suderman, M, Pinette, M, Smith, G, Sullivan, D, Rudar, J, Vernygora, O, Adey, E, Nebroski, M, Goyette, G, Finzi, A, Laroche, G, Ariana, A, Vahkal, B, Côté, M, McGeer, AJ, Nituch, L, Mubareka, S & Bowman, J 2022, 'Divergent SARS-CoV-2 variant emerges in white-tailed deer with deer-to-human transmission', Nature Microbiology. https://doi.org/10.1038/s41564-022-01268-9

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title = "Divergent SARS-CoV-2 variant emerges in white-tailed deer with deer-to-human transmission",

abstract = "Wildlife reservoirs of broad-host-range viruses have the potential to enable evolution of viral variants that can emerge to infect humans. In North America, there is phylogenomic evidence of continual transmission of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) from humans to white-tailed deer (Odocoileus virginianus) through unknown means, but no evidence of transmission from deer to humans. We carried out an observational surveillance study in Ontario, Canada during November and December 2021 (n = 300 deer) and identified a highly divergent lineage of SARS-CoV-2 in white-tailed deer (B.1.641). This lineage is one of the most divergent SARS-CoV-2 lineages identified so far, with 76 mutations (including 37 previously associated with non-human mammalian hosts). From a set of five complete and two partial deer-derived viral genomes we applied phylogenomic, recombination, selection and mutation spectrum analyses, which provided evidence for evolution and transmission in deer and a shared ancestry with mink-derived virus. Our analysis also revealed an epidemiologically linked human infection. Taken together, our findings provide evidence for sustained evolution of SARS-CoV-2 in white-tailed deer and of deer-to-human transmission.",

author = "Bradley Pickering and Oliver Lung and Finlay Maguire and Peter Kruczkiewicz and Kotwa, {Jonathon D.} and Tore Buchanan and Marianne Gagnier and Guthrie, {Jennifer L.} and Jardine, {Claire M.} and Alex Marchand-Austin and Ariane Mass{\'e} and Heather McClinchey and Kuganya Nirmalarajah and Patryk Aftanas and Juliette Blais-Savoie and Chee, {Hsien Yao} and Emily Chien and Winfield Yim and Andra Banete and Griffin, {Bryan D.} and Lily Yip and Melissa Goolia and Matthew Suderman and Mathieu Pinette and Greg Smith and Daniel Sullivan and Josip Rudar and Oksana Vernygora and Elizabeth Adey and Michelle Nebroski and Guillaume Goyette and Andr{\'e}s Finzi and Genevi{\`e}ve Laroche and Ardeshir Ariana and Brett Vahkal and Marceline C{\^o}t{\'e} and McGeer, {Allison J.} and Larissa Nituch and Samira Mubareka and Jeff Bowman",

note = "Funding Information: We acknowledge the contributions of the Virus Detection, Molecular Diagnostics, DNA Core sections and the Biocomputing Centre of Public Health Ontario, and in particular S. Teatero for leading the genome sequencing efforts. We gratefully acknowledge contributions of SARS-CoV-2 genome sequences from other laboratories through GISAID (Supplementary Table ). We thank the licensed Ontario deer hunters who submitted samples for wildlife disease surveillance, the staff of MNRF{\textquoteright}s CWD surveillance programme for their assistance with sample collection, and S. Hagey for GIS support. We also acknowledge the contributions of CFIA NCFAD{\textquoteright}s Genomics Unit for their assistance with additional laboratory support and sequencing. S.M. and B.P. are members of the Canada and the Canadian Institutes for Health Research Coronavirus Variants Rapid Response Network (CoVaRR-Net). We are grateful to D. Bulir from McMaster University for providing the primer and probe sequences for the 5′ UTR RT–PCR SARS-CoV-2 PCR assay, and to M. Taipale for cathepsin L knock-out TMPRSS2-overexpressing Vero cells. We appreciate the Public Health Agency of Canada for uploading the raw sequencing data for the Public Health Ontario human sequence to the Short Read Archive. The CV3-25 antibody was produced using the pTT vector kindly provided by the Canada Research Council. We also thank D. Leclair, J. Provencher, C. Soos and A. Wilcox (Environment and Climate Change Canada) for comments on an earlier draft of the manuscript. Ethical approvals for this work were provided by Sinai Health System Research Ethics Board (#22-0030-E), Sunnybrook HSC Research Ethics Board (#SUN-2218) and University of Ottawa Research Ethics Board (#H-01-22-7842). Funding to S.M. was provided by the Public Health Agency of Canada and the Canadian Institutes for Health Research Operating grant: Emerging COVID-19 Research Gaps and Priorities #466984. J.D.K. was supported by the Association of Medical Microbiology and Infectious Diseases (AMMI) Canada 2020 AMMI Canada/Biom{\'e}rieux Post Residency Fellowship in Microbial Diagnostics (unrestricted). Funding and computing resources for F.M. were provided by the Shared Hospital Laboratory, Dalhousie University and the Donald Hill Family. Funding for B.P. was provided by the Canadian Food Inspection Agency and the Canadian Safety and Security Program. Funding to J.B., T.B. and L.N. was provided by MNRF and the Public Health Agency of Canada. Funding for O.L. was from the Canadian Safety and Security Program, Laboratories Canada and CFIA. A.F. is the recipient of Canada Research Chair on Retroviral Entry no. RCHS0235 950-232424. M.C. is a Canada Research Chair in Molecular Virology and Antiviral Therapeutics (950-232840) and a recipient of an Ontario Ministry of Research, Innovation and Science Early Researcher Award (ER18-14-09). Funding to M.C. was provided by a COVID-19 Rapid Research grant from the Canadian Institutes for Health Research (CIHR, OV3 170632), CIHR stream 1 for SARS-CoV-2 Variant Research. Work from M.C. and A.F. is also supported by the Sentinelle COVID Quebec network led by the Laboratoire de Sant{\'e} Publique du Qu{\'e}bec (LSPQ) in collaboration with Fonds de Recherche du Qu{\'e}bec-Sant{\'e} (FRQS) and Genome Canada—G{\'e}nome Qu{\'e}bec, and by the Minist{\`e}re de la Sant{\'e} et des Services Sociaux (MSSS) and the Minist{\`e}re de l{\textquoteright}{\'E}conomie et Innovation (MEI). Publisher Copyright: {\textcopyright} 2022, The Author(s).",

year = "2022",

doi = "10.1038/s41564-022-01268-9",

language = "English",

journal = "Nature Microbiology",

issn = "2058-5276",

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TY - JOUR

T1 - Divergent SARS-CoV-2 variant emerges in white-tailed deer with deer-to-human transmission

AU - Pickering, Bradley

AU - Lung, Oliver

AU - Maguire, Finlay

AU - Kruczkiewicz, Peter

AU - Kotwa, Jonathon D.

AU - Buchanan, Tore

AU - Gagnier, Marianne

AU - Guthrie, Jennifer L.

AU - Jardine, Claire M.

AU - Marchand-Austin, Alex

AU - Massé, Ariane

AU - McClinchey, Heather

AU - Nirmalarajah, Kuganya

AU - Aftanas, Patryk

AU - Blais-Savoie, Juliette

AU - Chee, Hsien Yao

AU - Chien, Emily

AU - Yim, Winfield

AU - Banete, Andra

AU - Griffin, Bryan D.

AU - Yip, Lily

AU - Goolia, Melissa

AU - Suderman, Matthew

AU - Pinette, Mathieu

AU - Smith, Greg

AU - Sullivan, Daniel

AU - Rudar, Josip

AU - Vernygora, Oksana

AU - Adey, Elizabeth

AU - Nebroski, Michelle

AU - Goyette, Guillaume

AU - Finzi, Andrés

AU - Laroche, Geneviève

AU - Ariana, Ardeshir

AU - Vahkal, Brett

AU - Côté, Marceline

AU - McGeer, Allison J.

AU - Nituch, Larissa

AU - Mubareka, Samira

AU - Bowman, Jeff

N1 - Funding Information: We acknowledge the contributions of the Virus Detection, Molecular Diagnostics, DNA Core sections and the Biocomputing Centre of Public Health Ontario, and in particular S. Teatero for leading the genome sequencing efforts. We gratefully acknowledge contributions of SARS-CoV-2 genome sequences from other laboratories through GISAID (Supplementary Table ). We thank the licensed Ontario deer hunters who submitted samples for wildlife disease surveillance, the staff of MNRF’s CWD surveillance programme for their assistance with sample collection, and S. Hagey for GIS support. We also acknowledge the contributions of CFIA NCFAD’s Genomics Unit for their assistance with additional laboratory support and sequencing. S.M. and B.P. are members of the Canada and the Canadian Institutes for Health Research Coronavirus Variants Rapid Response Network (CoVaRR-Net). We are grateful to D. Bulir from McMaster University for providing the primer and probe sequences for the 5′ UTR RT–PCR SARS-CoV-2 PCR assay, and to M. Taipale for cathepsin L knock-out TMPRSS2-overexpressing Vero cells. We appreciate the Public Health Agency of Canada for uploading the raw sequencing data for the Public Health Ontario human sequence to the Short Read Archive. The CV3-25 antibody was produced using the pTT vector kindly provided by the Canada Research Council. We also thank D. Leclair, J. Provencher, C. Soos and A. Wilcox (Environment and Climate Change Canada) for comments on an earlier draft of the manuscript. Ethical approvals for this work were provided by Sinai Health System Research Ethics Board (#22-0030-E), Sunnybrook HSC Research Ethics Board (#SUN-2218) and University of Ottawa Research Ethics Board (#H-01-22-7842). Funding to S.M. was provided by the Public Health Agency of Canada and the Canadian Institutes for Health Research Operating grant: Emerging COVID-19 Research Gaps and Priorities #466984. J.D.K. was supported by the Association of Medical Microbiology and Infectious Diseases (AMMI) Canada 2020 AMMI Canada/Biomérieux Post Residency Fellowship in Microbial Diagnostics (unrestricted). Funding and computing resources for F.M. were provided by the Shared Hospital Laboratory, Dalhousie University and the Donald Hill Family. Funding for B.P. was provided by the Canadian Food Inspection Agency and the Canadian Safety and Security Program. Funding to J.B., T.B. and L.N. was provided by MNRF and the Public Health Agency of Canada. Funding for O.L. was from the Canadian Safety and Security Program, Laboratories Canada and CFIA. A.F. is the recipient of Canada Research Chair on Retroviral Entry no. RCHS0235 950-232424. M.C. is a Canada Research Chair in Molecular Virology and Antiviral Therapeutics (950-232840) and a recipient of an Ontario Ministry of Research, Innovation and Science Early Researcher Award (ER18-14-09). Funding to M.C. was provided by a COVID-19 Rapid Research grant from the Canadian Institutes for Health Research (CIHR, OV3 170632), CIHR stream 1 for SARS-CoV-2 Variant Research. Work from M.C. and A.F. is also supported by the Sentinelle COVID Quebec network led by the Laboratoire de Santé Publique du Québec (LSPQ) in collaboration with Fonds de Recherche du Québec-Santé (FRQS) and Genome Canada—Génome Québec, and by the Ministère de la Santé et des Services Sociaux (MSSS) and the Ministère de l’Économie et Innovation (MEI). Publisher Copyright: © 2022, The Author(s).

PY - 2022

Y1 - 2022

N2 - Wildlife reservoirs of broad-host-range viruses have the potential to enable evolution of viral variants that can emerge to infect humans. In North America, there is phylogenomic evidence of continual transmission of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) from humans to white-tailed deer (Odocoileus virginianus) through unknown means, but no evidence of transmission from deer to humans. We carried out an observational surveillance study in Ontario, Canada during November and December 2021 (n = 300 deer) and identified a highly divergent lineage of SARS-CoV-2 in white-tailed deer (B.1.641). This lineage is one of the most divergent SARS-CoV-2 lineages identified so far, with 76 mutations (including 37 previously associated with non-human mammalian hosts). From a set of five complete and two partial deer-derived viral genomes we applied phylogenomic, recombination, selection and mutation spectrum analyses, which provided evidence for evolution and transmission in deer and a shared ancestry with mink-derived virus. Our analysis also revealed an epidemiologically linked human infection. Taken together, our findings provide evidence for sustained evolution of SARS-CoV-2 in white-tailed deer and of deer-to-human transmission.

AB - Wildlife reservoirs of broad-host-range viruses have the potential to enable evolution of viral variants that can emerge to infect humans. In North America, there is phylogenomic evidence of continual transmission of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) from humans to white-tailed deer (Odocoileus virginianus) through unknown means, but no evidence of transmission from deer to humans. We carried out an observational surveillance study in Ontario, Canada during November and December 2021 (n = 300 deer) and identified a highly divergent lineage of SARS-CoV-2 in white-tailed deer (B.1.641). This lineage is one of the most divergent SARS-CoV-2 lineages identified so far, with 76 mutations (including 37 previously associated with non-human mammalian hosts). From a set of five complete and two partial deer-derived viral genomes we applied phylogenomic, recombination, selection and mutation spectrum analyses, which provided evidence for evolution and transmission in deer and a shared ancestry with mink-derived virus. Our analysis also revealed an epidemiologically linked human infection. Taken together, our findings provide evidence for sustained evolution of SARS-CoV-2 in white-tailed deer and of deer-to-human transmission.

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Divergent SARS-CoV-2 variant emerges in white-tailed deer with deer-to-human transmission

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