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Wastewater sequencing reveals early cryptic SARS-CoV-2 variant transmission

Author

Listed:
  • Smruthi Karthikeyan

    (University of California San Diego)

  • Joshua I. Levy

    (The Scripps Research Institute)

  • Peter Hoff

    (University of California San Diego
    University of California San Diego
    COVID-19 Detection, Investigation, Surveillance, Clinical, and Outbreak Response, California Department of Public Health)

  • Greg Humphrey

    (University of California San Diego)

  • Amanda Birmingham

    (University of California San Diego)

  • Kristen Jepsen

    (University of California San Diego)

  • Sawyer Farmer

    (University of California San Diego)

  • Helena M. Tubb

    (University of California San Diego)

  • Tommy Valles

    (University of California San Diego)

  • Caitlin E. Tribelhorn

    (University of California San Diego)

  • Rebecca Tsai

    (University of California San Diego)

  • Stefan Aigner

    (University of California San Diego)

  • Shashank Sathe

    (University of California San Diego)

  • Niema Moshiri

    (University of California San Diego)

  • Benjamin Henson

    (University of California San Diego)

  • Adam M. Mark

    (University of California San Diego)

  • Abbas Hakim

    (University of California San Diego
    University of California San Diego
    COVID-19 Detection, Investigation, Surveillance, Clinical, and Outbreak Response, California Department of Public Health)

  • Nathan A. Baer

    (University of California San Diego)

  • Tom Barber

    (University of California San Diego)

  • Pedro Belda-Ferre

    (University of California San Diego)

  • Marisol Chacón

    (University of California San Diego)

  • Willi Cheung

    (University of California San Diego
    University of California San Diego
    COVID-19 Detection, Investigation, Surveillance, Clinical, and Outbreak Response, California Department of Public Health)

  • Evelyn S. Cresini

    (University of California San Diego)

  • Emily R. Eisner

    (University of California San Diego)

  • Alma L. Lastrella

    (University of California San Diego)

  • Elijah S. Lawrence

    (University of California San Diego)

  • Clarisse A. Marotz

    (University of California San Diego)

  • Toan T. Ngo

    (University of California San Diego)

  • Tyler Ostrander

    (University of California San Diego)

  • Ashley Plascencia

    (University of California San Diego)

  • Rodolfo A. Salido

    (University of California San Diego)

  • Phoebe Seaver

    (University of California San Diego)

  • Elizabeth W. Smoot

    (University of California San Diego)

  • Daniel McDonald

    (University of California San Diego)

  • Robert M. Neuhard

    (University of California San Diego
    University of California San Diego)

  • Angela L. Scioscia

    (University of California San Diego
    Student Health and Well-Being, University of California San Diego)

  • Alysson M. Satterlund

    (University of California San Diego)

  • Elizabeth H. Simmons

    (University of California San Diego)

  • Dismas B. Abelman

    (University of California San Diego)

  • David Brenner

    (University of California San Diego)

  • Judith C. Bruner

    (University of California San Diego)

  • Anne Buckley

    (University of California San Diego)

  • Michael Ellison

    (University of California San Diego)

  • Jeffrey Gattas

    (University of California San Diego)

  • Steven L. Gonias

    (University of California San Diego)

  • Matt Hale

    (University of California San Diego)

  • Faith Hawkins

    (University of California San Diego)

  • Lydia Ikeda

    (University of California San Diego)

  • Hemlata Jhaveri

    (University of California San Diego)

  • Ted Johnson

    (University of California San Diego)

  • Vince Kellen

    (University of California San Diego)

  • Brendan Kremer

    (University of California San Diego)

  • Gary Matthews

    (University of California San Diego)

  • Ronald W. McLawhon

    (University of California San Diego)

  • Pierre Ouillet

    (University of California San Diego)

  • Daniel Park

    (University of California San Diego)

  • Allorah Pradenas

    (University of California San Diego)

  • Sharon Reed

    (University of California San Diego)

  • Lindsay Riggs

    (University of California San Diego)

  • Alison Sanders

    (University of California San Diego)

  • Bradley Sollenberger

    (University of California San Diego)

  • Angela Song

    (University of California San Diego
    University of California San Diego)

  • Benjamin White

    (University of California San Diego)

  • Terri Winbush

    (University of California San Diego)

  • Christine M. Aceves

    (The Scripps Research Institute)

  • Catelyn Anderson

    (The Scripps Research Institute)

  • Karthik Gangavarapu

    (The Scripps Research Institute)

  • Emory Hufbauer

    (The Scripps Research Institute)

  • Ezra Kurzban

    (The Scripps Research Institute)

  • Justin Lee

    (The Scripps Research Institute)

  • Nathaniel L. Matteson

    (The Scripps Research Institute)

  • Edyth Parker

    (The Scripps Research Institute)

  • Sarah A. Perkins

    (The Scripps Research Institute)

  • Karthik S. Ramesh

    (The Scripps Research Institute)

  • Refugio Robles-Sikisaka

    (The Scripps Research Institute)

  • Madison A. Schwab

    (The Scripps Research Institute)

  • Emily Spencer

    (The Scripps Research Institute)

  • Shirlee Wohl

    (The Scripps Research Institute)

  • Laura Nicholson

    (Scripps Health, San Diego)

  • Ian H. McHardy

    (Scripps Health, San Diego)

  • David P. Dimmock

    (Rady Children’s Institute for Genomic Medicine)

  • Charlotte A. Hobbs

    (Rady Children’s Institute for Genomic Medicine)

  • Omid Bakhtar

    (Sharp Healthcare)

  • Aaron Harding

    (Sharp Healthcare)

  • Art Mendoza

    (Sharp Healthcare)

  • Alexandre Bolze

    (Helix)

  • David Becker

    (Helix)

  • Elizabeth T. Cirulli

    (Helix)

  • Magnus Isaksson

    (Helix)

  • Kelly M. Schiabor Barrett

    (Helix)

  • Nicole L. Washington

    (Helix)

  • John D. Malone

    (County of San Diego Health and Human Services Agency)

  • Ashleigh Murphy Schafer

    (County of San Diego Health and Human Services Agency)

  • Nikos Gurfield

    (County of San Diego Health and Human Services Agency)

  • Sarah Stous

    (County of San Diego Health and Human Services Agency)

  • Rebecca Fielding-Miller

    (University of California San Diego
    University of California San Diego)

  • Richard S. Garfein

    (University of California San Diego)

  • Tommi Gaines

    (University of California San Diego)

  • Cheryl Anderson

    (University of California San Diego)

  • Natasha K. Martin

    (University of California San Diego)

  • Robert Schooley

    (University of California San Diego)

  • Brett Austin

    (Sharp Healthcare)

  • Duncan R. MacCannell

    (Office of Advanced Molecular Detection, Centers for Disease Control and Prevention)

  • Stephen F. Kingsmore

    (Rady Children’s Institute for Genomic Medicine)

  • William Lee

    (Helix)

  • Seema Shah

    (County of San Diego Health and Human Services Agency)

  • Eric McDonald

    (County of San Diego Health and Human Services Agency)

  • Alexander T. Yu

    (COVID-19 Detection, Investigation, Surveillance, Clinical, and Outbreak Response, California Department of Public Health)

  • Mark Zeller

    (The Scripps Research Institute)

  • Kathleen M. Fisch

    (University of California San Diego
    University of California San Diego)

  • Christopher Longhurst

    (University of California San Diego
    University of California San Diego)

  • Patty Maysent

    (University of California San Diego)

  • David Pride

    (University of California San Diego
    University of California San Diego)

  • Pradeep K. Khosla

    (University of California San Diego)

  • Louise C. Laurent

    (University of California San Diego
    University of California San Diego
    University of California San Diego)

  • Gene W. Yeo

    (University of California San Diego
    University of California San Diego
    University of California San Diego)

  • Kristian G. Andersen

    (The Scripps Research Institute)

  • Rob Knight

    (University of California San Diego
    University of California San Diego
    University of California San Diego)

Abstract

As SARS-CoV-2 continues to spread and evolve, detecting emerging variants early is critical for public health interventions. Inferring lineage prevalence by clinical testing is infeasible at scale, especially in areas with limited resources, participation, or testing and/or sequencing capacity, which can also introduce biases1–3. SARS-CoV-2 RNA concentration in wastewater successfully tracks regional infection dynamics and provides less biased abundance estimates than clinical testing4,5. Tracking virus genomic sequences in wastewater would improve community prevalence estimates and detect emerging variants. However, two factors limit wastewater-based genomic surveillance: low-quality sequence data and inability to estimate relative lineage abundance in mixed samples. Here we resolve these critical issues to perform a high-resolution, 295-day wastewater and clinical sequencing effort, in the controlled environment of a large university campus and the broader context of the surrounding county. We developed and deployed improved virus concentration protocols and deconvolution software that fully resolve multiple virus strains from wastewater. We detected emerging variants of concern up to 14 days earlier in wastewater samples, and identified multiple instances of virus spread not captured by clinical genomic surveillance. Our study provides a scalable solution for wastewater genomic surveillance that allows early detection of SARS-CoV-2 variants and identification of cryptic transmission.

Suggested Citation

  • Smruthi Karthikeyan & Joshua I. Levy & Peter Hoff & Greg Humphrey & Amanda Birmingham & Kristen Jepsen & Sawyer Farmer & Helena M. Tubb & Tommy Valles & Caitlin E. Tribelhorn & Rebecca Tsai & Stefan A, 2022. "Wastewater sequencing reveals early cryptic SARS-CoV-2 variant transmission," Nature, Nature, vol. 609(7925), pages 101-108, September.
    • Handle: RePEc:nat:nature:v:609:y:2022:i:7925:d:10.1038_s41586-022-05049-6
    DOI: 10.1038/s41586-022-05049-6
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    Citations

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    Cited by:

    1. Braden T. Tierney & Jonathan Foox & Krista A. Ryon & Daniel Butler & Namita Damle & Benjamin G. Young & Christopher Mozsary & Kristina M. Babler & Xue Yin & Yamina Carattini & David Andrews & Alexande, 2024. "Towards geospatially-resolved public-health surveillance via wastewater sequencing," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    2. Michael Tisza & Sara Javornik Cregeen & Vasanthi Avadhanula & Ping Zhang & Tulin Ayvaz & Karen Feliz & Kristi L. Hoffman & Justin R. Clark & Austen Terwilliger & Matthew C. Ross & Juwan Cormier & Hann, 2023. "Wastewater sequencing reveals community and variant dynamics of the collective human virome," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    3. Yunxi Liu & Nicolae Sapoval & Pilar Gallego-García & Laura Tomás & David Posada & Todd J. Treangen & Lauren B. Stadler, 2024. "Crykey: Rapid identification of SARS-CoV-2 cryptic mutations in wastewater," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    4. Mukhlid Yousif & Said Rachida & Setshaba Taukobong & Nkosenhle Ndlovu & Chinwe Iwu-Jaja & Wayne Howard & Shelina Moonsamy & Nompilo Mhlambi & Sipho Gwala & Joshua I. Levy & Kristian G. Andersen & Cath, 2023. "SARS-CoV-2 genomic surveillance in wastewater as a model for monitoring evolution of endemic viruses," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    5. Sung Hee Ko & Pierce Radecki & Frida Belinky & Jinal N. Bhiman & Susan Meiring & Jackie Kleynhans & Daniel Amoako & Vanessa Guerra Canedo & Margaret Lucas & Dikeledi Kekana & Neil Martinson & Limakats, 2024. "Rapid intra-host diversification and evolution of SARS-CoV-2 in advanced HIV infection," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    6. Kayla G. Barnes & Joshua I. Levy & Jillian Gauld & Jonathan Rigby & Oscar Kanjerwa & Christopher B. Uzzell & Chisomo Chilupsya & Catherine Anscombe & Christopher Tomkins-Tinch & Omar Mbeti & Edward Ca, 2023. "Utilizing river and wastewater as a SARS-CoV-2 surveillance tool in settings with limited formal sewage systems," Nature Communications, Nature, vol. 14(1), pages 1-11, December.

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