Multiple spillovers from humans and onward transmission of SARS-CoV-2 in white-tailed deer
Edited by Peter Palese, Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY; received November 30, 2021; accepted December 16, 2021
Significance
The results provide strong evidence of extensive SARS-CoV-2 infection of white-tailed deer, a free-living wild animal species with widespread distribution across North, Central, and South America. The analysis shows infection of deer resulted from multiple spillovers from humans, followed by efficient deer-to-deer transmission. The discovery of widespread infection of white-tailed deer indicates their establishment as potential reservoir hosts for SARS-CoV-2, a finding with important implications for the ecology, long-term persistence, and evolution of the virus, including the potential for spillback to humans.
Abstract
Many animal species are susceptible to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection and could act as reservoirs; however, transmission in free-living animals has not been documented. White-tailed deer, the predominant cervid in North America, are susceptible to SARS-CoV-2 infection, and experimentally infected fawns can transmit the virus. To test the hypothesis that SARS-CoV-2 is circulating in deer, 283 retropharyngeal lymph node (RPLN) samples collected from 151 free-living and 132 captive deer in Iowa from April 2020 through January of 2021 were assayed for the presence of SARS-CoV-2 RNA. Ninety-four of the 283 (33.2%) deer samples were positive for SARS-CoV-2 RNA as assessed by RT-PCR. Notably, following the November 2020 peak of human cases in Iowa, and coinciding with the onset of winter and the peak deer hunting season, SARS-CoV-2 RNA was detected in 80 of 97 (82.5%) RPLN samples collected over a 7-wk period. Whole genome sequencing of all 94 positive RPLN samples identified 12 SARS-CoV-2 lineages, with B.1.2 (n = 51; 54.5%) and B.1.311 (n = 19; 20%) accounting for ∼75% of all samples. The geographic distribution and nesting of clusters of deer and human lineages strongly suggest multiple human-to-deer transmission events followed by subsequent deer-to-deer spread. These discoveries have important implications for the long-term persistence of the SARS-CoV-2 pandemic. Our findings highlight an urgent need for a robust and proactive “One Health” approach to obtain enhanced understanding of the ecology, molecular evolution, and dissemination of SARS-CoV-2.
Data Availability
All SARS-CoV-2 consensus genomes are deposited in GISAID, https://www.gisaid.org/; Accession numbers EPI_ISL_5804716–EPI_ISL_5804787 and EPI_ISL_6425266–EPI_ISL_6425287, and raw reads have been submitted to NCBI’s Short Read Archive (BioProject Number: PRJNA776532).
Acknowledgments
We thank Abhinay Gontu, Shubhada Chothe, Padmaja Jakka, and Abirami Ravichnadran for help with tissue homogenization, and Vincent Nelson, Lindsey LaBella, and Corey Price for help with sample processing. We thank Matthew Ojeda Saavedra, Sindy Pena, Kristina Reppond, Madison N. Shyer, Jessica Cambric, Ryan Gadd, Rashi M. Thakur, Akanksha Batajoo, and Regan Mangham for genome sequencing. We are grateful to Drs. Suelee Robbe-Austerman, Tod Stuber, and Kristina Lantz, US Department of Agriculture (USDA) National Veterinary Services Laboratory, for invaluable assistance and wise counsel. This study was possible through the collective efforts of Iowa DNR field staff, with special thanks to Riggs Wilson for help with sample inventory. The study was funded by the Huck Institutes of the Life Sciences (S.V.K. and V.K.); USDA National Institute of Food and Agriculture Award 2020-67015-32175; US Fish and Wildlife Service Wildlife and Sport Fish Restoration Program Grant Awards FY20 F19AF00434 (19/20 samples), FY21 F20AF00309 (20/21 samples), and FY22 F21AF01914 (21/22 samples); and the Iowa DNR Fish and Game Protection Fund. This project was also funded, in part, by the Houston Methodist Academic Institute Infectious Diseases Fund (J.M.M. and R.J.O.) and supported, in part, by National Institute of Allergy and Infectious Diseases, NIH, Department of Health and Human Services, Contract 75N93019C00076 (J.J.D.). K.J.V. was partially supported by the NSF Ecology and Evolution of Infectious Diseases program (Grant 1619072).
Supporting Information
Materials/Methods, Supplementary Text, Tables, Figures, and/or References
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Copyright
Copyright © 2022 the Author(s). Published by PNAS. This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY).
Data Availability
All SARS-CoV-2 consensus genomes are deposited in GISAID, https://www.gisaid.org/; Accession numbers EPI_ISL_5804716–EPI_ISL_5804787 and EPI_ISL_6425266–EPI_ISL_6425287, and raw reads have been submitted to NCBI’s Short Read Archive (BioProject Number: PRJNA776532).
Submission history
Received: November 30, 2021
Accepted: December 16, 2021
Published online: January 25, 2022
Published in issue: February 8, 2022
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Acknowledgments
We thank Abhinay Gontu, Shubhada Chothe, Padmaja Jakka, and Abirami Ravichnadran for help with tissue homogenization, and Vincent Nelson, Lindsey LaBella, and Corey Price for help with sample processing. We thank Matthew Ojeda Saavedra, Sindy Pena, Kristina Reppond, Madison N. Shyer, Jessica Cambric, Ryan Gadd, Rashi M. Thakur, Akanksha Batajoo, and Regan Mangham for genome sequencing. We are grateful to Drs. Suelee Robbe-Austerman, Tod Stuber, and Kristina Lantz, US Department of Agriculture (USDA) National Veterinary Services Laboratory, for invaluable assistance and wise counsel. This study was possible through the collective efforts of Iowa DNR field staff, with special thanks to Riggs Wilson for help with sample inventory. The study was funded by the Huck Institutes of the Life Sciences (S.V.K. and V.K.); USDA National Institute of Food and Agriculture Award 2020-67015-32175; US Fish and Wildlife Service Wildlife and Sport Fish Restoration Program Grant Awards FY20 F19AF00434 (19/20 samples), FY21 F20AF00309 (20/21 samples), and FY22 F21AF01914 (21/22 samples); and the Iowa DNR Fish and Game Protection Fund. This project was also funded, in part, by the Houston Methodist Academic Institute Infectious Diseases Fund (J.M.M. and R.J.O.) and supported, in part, by National Institute of Allergy and Infectious Diseases, NIH, Department of Health and Human Services, Contract 75N93019C00076 (J.J.D.). K.J.V. was partially supported by the NSF Ecology and Evolution of Infectious Diseases program (Grant 1619072).
Notes
This article is a PNAS Direct Submission.
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The authors declare no competing interest.
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Multiple spillovers from humans and onward transmission of SARS-CoV-2 in white-tailed deer, Proc. Natl. Acad. Sci. U.S.A.
119 (6) e2121644119,
https://doi.org/10.1073/pnas.2121644119
(2022).
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