Genetic tracing of market wildlife and viruses at the epicenter of the COVID-19 pandemic

Alexander Crits-Christoph; Joshua I. Levy; Jonathan E. Pekar; Stephen A. Goldstein; Reema Singh; Zach Hensel; Karthik Gangavarapu; Matthew B. Rogers; Niema Moshiri; Robert F. Garry; Edward C. Holmes; Marion P.G. Koopmans; Philippe Lemey; Thomas P. Peacock; Saskia Popescu; Andrew Rambaut; David L. Robertson; Marc A. Suchard; Joel O. Wertheim; Angela L. Rasmussen; Kristian G. Andersen; Michael Worobey; Florence Débarre

doi:10.1016/j.cell.2024.08.010

Genetic tracing of market wildlife and viruses at the epicenter of the COVID-19 pandemic

Alexander Crits-Christoph, Joshua I. Levy, Jonathan E. Pekar, Stephen A. Goldstein, Reema Singh, Zach Hensel, Karthik Gangavarapu, Matthew B. Rogers, Niema Moshiri, Robert F. Garry, Edward C. Holmes, Marion P.G. Koopmans, Philippe Lemey, Thomas P. Peacock, Saskia Popescu, Andrew Rambaut, David L. Robertson, Marc A. Suchard, Joel O. Wertheim, Angela L. RasmussenKristian G. Andersen, Michael Worobey, Florence Débarre

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

8 Scopus citations

Abstract

Zoonotic spillovers of viruses have occurred through the animal trade worldwide. The start of the COVID-19 pandemic was traced epidemiologically to the Huanan Seafood Wholesale Market. Here, we analyze environmental qPCR and sequencing data collected in the Huanan market in early 2020. We demonstrate that market-linked severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) genetic diversity is consistent with market emergence and find increased SARS-CoV-2 positivity near and within a wildlife stall. We identify wildlife DNA in all SARS-CoV-2-positive samples from this stall, including species such as civets, bamboo rats, and raccoon dogs, previously identified as possible intermediate hosts. We also detect animal viruses that infect raccoon dogs, civets, and bamboo rats. Combining metagenomic and phylogenetic approaches, we recover genotypes of market animals and compare them with those from farms and other markets. This analysis provides the genetic basis for a shortlist of potential intermediate hosts of SARS-CoV-2 to prioritize for serological and viral sampling.

Original language	English (US)
Pages (from-to)	5468-5482.e11
Journal	Cell
Volume	187
Issue number	19
DOIs	https://doi.org/10.1016/j.cell.2024.08.010
State	Published - Sep 19 2024
Externally published	Yes

Keywords

SARS-CoV-2
forensic genomics
metatranscriptomics
phylodynamics
phylogenetics
viral emergence
virus evolution
wildlife trade

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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10.1016/j.cell.2024.08.010

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Crits-Christoph, A., Levy, J. I., Pekar, J. E., Goldstein, S. A., Singh, R., Hensel, Z., Gangavarapu, K., Rogers, M. B., Moshiri, N., Garry, R. F., Holmes, E. C., Koopmans, M. P. G., Lemey, P., Peacock, T. P., Popescu, S., Rambaut, A., Robertson, D. L., Suchard, M. A., Wertheim, J. O., ... Débarre, F. (2024). Genetic tracing of market wildlife and viruses at the epicenter of the COVID-19 pandemic. Cell, 187(19), 5468-5482.e11. https://doi.org/10.1016/j.cell.2024.08.010

Crits-Christoph, A, Levy, JI, Pekar, JE, Goldstein, SA, Singh, R, Hensel, Z, Gangavarapu, K, Rogers, MB, Moshiri, N, Garry, RF, Holmes, EC, Koopmans, MPG, Lemey, P, Peacock, TP, Popescu, S, Rambaut, A, Robertson, DL, Suchard, MA, Wertheim, JO, Rasmussen, AL, Andersen, KG, Worobey, M & Débarre, F 2024, 'Genetic tracing of market wildlife and viruses at the epicenter of the COVID-19 pandemic', Cell, vol. 187, no. 19, pp. 5468-5482.e11. https://doi.org/10.1016/j.cell.2024.08.010

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abstract = "Zoonotic spillovers of viruses have occurred through the animal trade worldwide. The start of the COVID-19 pandemic was traced epidemiologically to the Huanan Seafood Wholesale Market. Here, we analyze environmental qPCR and sequencing data collected in the Huanan market in early 2020. We demonstrate that market-linked severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) genetic diversity is consistent with market emergence and find increased SARS-CoV-2 positivity near and within a wildlife stall. We identify wildlife DNA in all SARS-CoV-2-positive samples from this stall, including species such as civets, bamboo rats, and raccoon dogs, previously identified as possible intermediate hosts. We also detect animal viruses that infect raccoon dogs, civets, and bamboo rats. Combining metagenomic and phylogenetic approaches, we recover genotypes of market animals and compare them with those from farms and other markets. This analysis provides the genetic basis for a shortlist of potential intermediate hosts of SARS-CoV-2 to prioritize for serological and viral sampling.",

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AU - Singh, Reema

AU - Hensel, Zach

AU - Gangavarapu, Karthik

AU - Rogers, Matthew B.

AU - Moshiri, Niema

AU - Garry, Robert F.

AU - Holmes, Edward C.

AU - Koopmans, Marion P.G.

AU - Lemey, Philippe

AU - Peacock, Thomas P.

AU - Popescu, Saskia

AU - Rambaut, Andrew

AU - Robertson, David L.

AU - Suchard, Marc A.

AU - Wertheim, Joel O.

AU - Rasmussen, Angela L.

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AU - Worobey, Michael

AU - Débarre, Florence

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AB - Zoonotic spillovers of viruses have occurred through the animal trade worldwide. The start of the COVID-19 pandemic was traced epidemiologically to the Huanan Seafood Wholesale Market. Here, we analyze environmental qPCR and sequencing data collected in the Huanan market in early 2020. We demonstrate that market-linked severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) genetic diversity is consistent with market emergence and find increased SARS-CoV-2 positivity near and within a wildlife stall. We identify wildlife DNA in all SARS-CoV-2-positive samples from this stall, including species such as civets, bamboo rats, and raccoon dogs, previously identified as possible intermediate hosts. We also detect animal viruses that infect raccoon dogs, civets, and bamboo rats. Combining metagenomic and phylogenetic approaches, we recover genotypes of market animals and compare them with those from farms and other markets. This analysis provides the genetic basis for a shortlist of potential intermediate hosts of SARS-CoV-2 to prioritize for serological and viral sampling.

KW - SARS-CoV-2

KW - forensic genomics

KW - metatranscriptomics

KW - phylodynamics

KW - phylogenetics

KW - viral emergence

KW - virus evolution

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ER -

Genetic tracing of market wildlife and viruses at the epicenter of the COVID-19 pandemic

Abstract

Keywords

ASJC Scopus subject areas

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