Host-microbe multiomic profiling identifies distinct COVID-19 immune dysregulation in solid organ transplant recipients
Coronavirus disease 2019 (COVID-19) poses significant risks for solid organ transplant recipients, who have atypical but poorly characterized immune responses to infection. We aim to understand the host immunologic and microbial features of COVID-19 in transplant recipients by leveraging a prospective multicenter cohort of 86 transplant recipients age- and sex-matched with 172 non-transplant controls. We find that transplant recipients have higher nasal SARS-CoV-2 viral abundance and impaired viral clearance, and lower anti-spike IgG levels. In addition, transplant recipients exhibit decreased plasmablasts and transitional B cells, and increased senescent T cells. Blood and nasal transcriptional profiling demonstrate unexpected upregulation of innate immune signaling pathways and increased levels of several proinflammatory serum chemokines. Severe disease in transplant recipients, however, is characterized by a less robust induction of pro-inflammatory genes and chemokines. Together, our study reveals distinct immune features and altered viral dynamics in solid organ transplant recipients.
Authors
- Grace A. McComsey (ORCID: https://orcid.org/0000-0003-2690-8888)
- David Elashoff
- Walter L. Eckalbar (ORCID: https://orcid.org/0000-0003-2520-7852)
- Nicolas C. Issa (ORCID: https://orcid.org/0000-0002-6596-0518)
- Lekshmi Santhosh (ORCID: https://orcid.org/0000-0002-9897-3462)
- Joann Diray‐Arce (ORCID: https://orcid.org/0000-0003-2183-4269)
- Luz Torres Altamirano
- Jeremy P. Gygi (ORCID: https://orcid.org/0000-0001-8567-7472)
- Bonny D. Alvarenga (ORCID: https://orcid.org/0000-0001-7922-9454)
- Hanno Steen (ORCID: https://orcid.org/0000-0003-0179-6648)
- Lauren A. Sinko
- Charles Langelier (ORCID: https://orcid.org/0000-0002-6708-4646)
- Greg K. Tharp
- William Ruff (ORCID: https://orcid.org/0000-0001-5828-6425)
- Nataliya Melnyk
- Zain Khalil (ORCID: https://orcid.org/0009-0007-4692-1998)
- Harry Pickering (ORCID: https://orcid.org/0000-0003-2348-5410)
- Priya Prasad
- Saurabh Asthana
- Jeff Milush
- Jarrod Mosier (ORCID: https://orcid.org/0000-0002-5371-0845)
- Kerin Hurley
- Keith Farrugia
- R. Sharon Chinthrajah (ORCID: https://orcid.org/0000-0003-2467-4256)
- Amer Bechnak
- David A. Hafler (ORCID: https://orcid.org/0000-0003-4664-535X)
- Leying Guan (ORCID: https://orcid.org/0000-0003-0609-1073)
- Michael Adkisson
- Maria C. Bermúdez‐González (ORCID: https://orcid.org/0000-0002-7908-6286)
- Trina Hughes
- Subhasis Mohanty (ORCID: https://orcid.org/0000-0002-3870-2468)
- Boryana Petrova (ORCID: https://orcid.org/0000-0001-9996-9353)
- Alyssa Ward
- George A. Yendewa (ORCID: https://orcid.org/0000-0002-8474-1812)
- Jenny Brook (ORCID: https://orcid.org/0000-0001-5705-1042)
- Tatyana Vaysman
- Elsio A. Wunder (ORCID: https://orcid.org/0000-0002-5239-8511)
- Elizabeth Beagle
- Allyson Molzahn (ORCID: https://orcid.org/0000-0002-1091-7942)
- Tyson H. Holmes (ORCID: https://orcid.org/0000-0002-5512-4583)
- Debra Powell (ORCID: https://orcid.org/0000-0001-9917-3160)
- Kerry McEnaney (ORCID: https://orcid.org/0000-0002-0378-3456)
- Jessica Lasky‐Su (ORCID: https://orcid.org/0000-0001-6236-4705)
- Carolyn Leroux
- Caroline Ciric
- James A. Overton (ORCID: https://orcid.org/0000-0001-5139-5557)
- Christina Montesano
- Norman L. Jones (ORCID: https://orcid.org/0000-0002-8267-1419)
- Lauren I. R. Ehrlich (ORCID: https://orcid.org/0000-0002-1697-1755)
- Maimouna D. Murphy
- Akiko Iwasaki (ORCID: https://orcid.org/0000-0002-7824-9856)
- Jennifer A. Fulcher (ORCID: https://orcid.org/0000-0001-9895-8636)
- David J. Erle (ORCID: https://orcid.org/0000-0002-2171-0648)
- Nathan D. Grubaugh (ORCID: https://orcid.org/0000-0003-2031-1933)
- Chris Bime
- Alejandra Jáuregui (ORCID: https://orcid.org/0000-0001-9158-2007)
- Lauren T. Hewitt (ORCID: https://orcid.org/0000-0001-7270-7679)
- Anderson Fernandes Brito (ORCID: https://orcid.org/0000-0001-5785-7222)
- Ebony Nelson
- Albert Icksang Ko (ORCID: https://orcid.org/0000-0001-9023-2339)
- Jessica Cauley
- S. Wimalasena (ORCID: https://orcid.org/0000-0002-8248-4074)
- Heidi L. Erickson (ORCID: https://orcid.org/0000-0001-5537-8893)
- Ruth R. Montgomery (ORCID: https://orcid.org/0000-0002-8661-4454)
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- Legna Betancourt
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- Arthur Viodé (ORCID: https://orcid.org/0000-0002-3418-734X)
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- Arash Nemati Hayati
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- Renee McLin
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- Stephen R. Walsh (ORCID: https://orcid.org/0000-0002-0817-9370)
- Arjun A. Rao (ORCID: https://orcid.org/0000-0003-4480-3190)
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- Justin F. Rousseau (ORCID: https://orcid.org/0000-0002-2817-9124)
- Kieffer Hellmeister
- Patrick van Zalm (ORCID: https://orcid.org/0000-0002-0806-3685)
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- Tanzia Shaheen
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- Bethany Evans
- Sadeed Rashid
- Jacob Usher
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- Meenakshi Jha (ORCID: https://orcid.org/0000-0001-6093-871X)
- Jordan P. Metcalf (ORCID: https://orcid.org/0000-0003-4359-5270)
- Raphael Lota
- Kyra Woloszczuk
- Brent Simmons
- Janelle N. Geltman
- Jose Humberto Licona
- Kinga K. Smolen (ORCID: https://orcid.org/0000-0001-8650-3693)
- Estefania Ramires‐Sanchez
- Yael Rosenberg‐Hasson (ORCID: https://orcid.org/0000-0002-3284-5732)
- Naama Kanarek (ORCID: https://orcid.org/0000-0002-2068-3908)
- Jun Bai Park Chang (ORCID: https://orcid.org/0000-0002-3338-8043)
- Hoang Van Phan (ORCID: https://orcid.org/0000-0002-0162-4283)
- Dylan Duchen (ORCID: https://orcid.org/0000-0001-5629-2012)
- Casey P. Shannon (ORCID: https://orcid.org/0000-0002-5687-3156)
- Matthew R. Bell (ORCID: https://orcid.org/0000-0001-7246-4021)
- Michael D. Leipold (ORCID: https://orcid.org/0000-0001-5389-0906)
- Michaël Desjardins (ORCID: https://orcid.org/0000-0003-4028-8507)
- I. Michael Goonewardene
- Bali Pulendran (ORCID: https://orcid.org/0000-0001-6517-4333)
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- Scott F. Sieg (ORCID: https://orcid.org/0000-0002-1769-8682)
- Slim Fourati (ORCID: https://orcid.org/0000-0001-6609-7587)
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- Hiromitsu Asashima
- Azlann Arnett (ORCID: https://orcid.org/0000-0003-1368-4678)
- Felicity J. Coulter (ORCID: https://orcid.org/0000-0003-0485-8752)
- Miti Saksena (ORCID: https://orcid.org/0000-0002-0678-020X)
- Mitchell Cooney
- Bjoern Peters
- Peter E. Sullivan (ORCID: https://orcid.org/0000-0001-8982-0643)
- Mehmet Saluvan (ORCID: https://orcid.org/0000-0002-7670-2450)
- Hady Samaha (ORCID: https://orcid.org/0000-0002-9124-7820)
- Evan Do
- Cole Maguire (ORCID: https://orcid.org/0000-0001-8986-9762)
- Sidney Carrillo (ORCID: https://orcid.org/0000-0002-6043-2468)
- Erin M. Scherer (ORCID: https://orcid.org/0000-0002-8794-1932)
- Mary Consolo (ORCID: https://orcid.org/0000-0002-9095-5913)
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- Farrah Kheradmand (ORCID: https://orcid.org/0000-0001-5343-103X)
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- Ron Schunk
- Scott Presnell (ORCID: https://orcid.org/0000-0001-9203-6403)
- Pablo Guaman Tipan (ORCID: https://orcid.org/0009-0007-3127-7095)
- Kathryn L. Pellegrini (ORCID: https://orcid.org/0000-0002-5089-5477)
- Faheem W. Guirgis (ORCID: https://orcid.org/0000-0002-4445-3939)
- Cole Shaw
- Nicholas C. Semenza (ORCID: https://orcid.org/0000-0002-4989-0847)
- Ramin Salehi‐Rad (ORCID: https://orcid.org/0000-0003-1543-5421)
- Natalie Izaguirre (ORCID: https://orcid.org/0000-0002-1778-4708)
- Matthew C. Altman (ORCID: https://orcid.org/0000-0002-1784-8505)
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- Catherine L. Hough (ORCID: https://orcid.org/0000-0001-6425-0867)
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- Pratik Sinha (ORCID: https://orcid.org/0000-0003-3751-9079)
- Yujiao Zhao (ORCID: https://orcid.org/0000-0001-9142-4332)
- Jonathan Krauß (ORCID: https://orcid.org/0000-0002-9126-1315)
- Laila Hussaini
- Christina Love
- Jennifer Connors (ORCID: https://orcid.org/0000-0001-9137-0717)
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- Erna Milunka Kojic
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- Alvin T. Kho (ORCID: https://orcid.org/0000-0002-9887-312X)
- Deanna Lee
- Cindy Curiel
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- Gisela Gabernet (ORCID: https://orcid.org/0000-0001-7049-9474)
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- John Fournier (ORCID: https://orcid.org/0000-0001-8320-4268)
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- Dawn C. Ward (ORCID: https://orcid.org/0000-0003-1672-740X)
- Rebecca Rooks (ORCID: https://orcid.org/0009-0007-1137-6707)
- Aleksandra Leligdowicz (ORCID: https://orcid.org/0000-0001-6055-4644)
- Kristen Ulring
- David Francisco (ORCID: https://orcid.org/0000-0003-1206-7424)
- Sara Morris (ORCID: https://orcid.org/0000-0002-7701-334X)
- Monali Manohar (ORCID: https://orcid.org/0000-0002-1869-2645)
- Johnstone Tcheou (ORCID: https://orcid.org/0000-0003-2733-4687)
- Monica Kraft (ORCID: https://orcid.org/0009-0002-6965-1090)
- Steven H. Kleinstein (ORCID: https://orcid.org/0000-0003-4957-1544)
- Christine Spainhour
- Kevin Tang (ORCID: https://orcid.org/0000-0002-2908-1954)
- Monica Fung (ORCID: https://orcid.org/0000-0002-1725-5259)
- Matthew Strand (ORCID: https://orcid.org/0000-0002-9083-5989)
- Ernie Chen (ORCID: https://orcid.org/0000-0003-1573-7577)
- Ofer Levy (ORCID: https://orcid.org/0000-0002-5859-1945)
- Prescott G. Woodruff (ORCID: https://orcid.org/0000-0003-3176-0603)
- Holden T. Maecker (ORCID: https://orcid.org/0000-0003-0795-9946)
- Randi Vita (ORCID: https://orcid.org/0000-0001-8957-7612)
- Alexandra Tong (ORCID: https://orcid.org/0009-0002-7361-1809)
- Naresh Doni Jayavelu (ORCID: https://orcid.org/0000-0001-5613-0830)
- Megan Llamas (ORCID: https://orcid.org/0000-0001-7612-4913)
- Levy A. Sominsky (ORCID: https://orcid.org/0000-0001-8084-3187)
- Angela J. Rogers (ORCID: https://orcid.org/0000-0001-6969-6200)
- Gayelan Tietje-Ulrich
- Sharvari Bhide
- Florian Krammer (ORCID: https://orcid.org/0000-0003-4121-776X)
- Dominika Bielak
- Bianca Sierra
- Denise Esserman
- Andreas Coppi (ORCID: https://orcid.org/0000-0002-5243-552X)
- Arun K. Boddapati (ORCID: https://orcid.org/0000-0002-7661-8443)
- Alexandra Tsitsiklis (ORCID: https://orcid.org/0000-0003-3467-1171)
- Robert W. Bryant
- Alexandra S. Lee (ORCID: https://orcid.org/0000-0003-4526-3800)
- James N. Kim
- Cecilia M. Smith
- Patrice M. Becker (ORCID: https://orcid.org/0000-0002-1170-8587)
- Mariana Bernui
- Geoffrey Kelly
- Gina Cusimano (ORCID: https://orcid.org/0000-0002-1393-9485)
- Linda N. Geng (ORCID: https://orcid.org/0000-0002-9891-5705)
- Andrew Cheng (ORCID: https://orcid.org/0000-0003-2201-8052)
- Bernadine Panganiban
- Maja Artandi (ORCID: https://orcid.org/0000-0003-2342-6277)
- Dennis Wylie (ORCID: https://orcid.org/0000-0003-0380-3549)
- Syim Salahuddin
- Yumiko Abe‐Jones
- David B. Corry (ORCID: https://orcid.org/0000-0001-9729-1016)
- Ana Fernández-Sesma (ORCID: https://orcid.org/0000-0002-3405-6702)
- Sarah Siegel (ORCID: https://orcid.org/0000-0001-8249-2632)
- Nelson Iván Agudelo Higuita (ORCID: https://orcid.org/0000-0002-9363-6280)
- James Abraham (ORCID: https://orcid.org/0000-0002-3742-4179)
- Iris Chang (ORCID: https://orcid.org/0009-0007-1971-8513)
- Rajani Ghale
- Joshua Vasquez (ORCID: https://orcid.org/0000-0002-7165-5739)
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- Elias K. Haddad (ORCID: https://orcid.org/0000-0001-6924-4300)
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- Maria Paz (ORCID: https://orcid.org/0000-0002-1236-5571)
- Shrikant Pawar
- Thomas Hagan (ORCID: https://orcid.org/0000-0002-5254-5251)
- Claudia Lentucci
- Catherine A. Blish (ORCID: https://orcid.org/0000-0001-6946-7627)
- Lyle L. Moldawer (ORCID: https://orcid.org/0000-0002-9041-9838)
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- Tasha Lea
- Brenda Barton
- Khadir Raddassi (ORCID: https://orcid.org/0000-0002-2383-9744)
- Al Ozonoff (ORCID: https://orcid.org/0000-0003-4233-5899)
- Pavithra Vijayakumar (ORCID: https://orcid.org/0000-0001-9191-7671)
- Sydney Hamilton
- Kirsten N. Kangelaris (ORCID: https://orcid.org/0000-0001-8152-994X)
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- Gagandeep Singh (ORCID: https://orcid.org/0000-0003-3260-2631)
- Jordan Oberhaus
- Suzanna Chak
- Andrea Fernandes (ORCID: https://orcid.org/0000-0002-2855-4262)
- Ricardo Ungaro
- Gabriela K. Fragiadakis (ORCID: https://orcid.org/0000-0001-9703-2591)
- Leqi Xu (ORCID: https://orcid.org/0000-0001-6789-4959)
- Ravi Dandekar (ORCID: https://orcid.org/0000-0002-2930-3043)
- Neeta Thakur (ORCID: https://orcid.org/0000-0001-6126-6601)
- Erin Carter (ORCID: https://orcid.org/0000-0002-2744-5312)
- Michael Rainone
- Scott C. Brakenridge (ORCID: https://orcid.org/0000-0002-7327-3718)
- Lubbertus C. F. Mulder
- Alison D. Augustine (ORCID: https://orcid.org/0000-0003-0064-9785)
- Lindsey Robert Baden (ORCID: https://orcid.org/0009-0004-1752-1926)
- Meagan M. Jenkins (ORCID: https://orcid.org/0000-0003-1379-9176)
- Connie Cathleen Wilson
- Xiaomei Wang
- Caitlin Syphurs (ORCID: https://orcid.org/0009-0004-5066-3985)
- Thomas Hodder
- Tomasz Jancsyk
- Bernard Kohr
- Brittney Borresen
- Xiaofang Li (ORCID: https://orcid.org/0000-0002-4210-7952)
- Haowei Wang (ORCID: https://orcid.org/0000-0002-5420-1153)
- Brian Lee (ORCID: https://orcid.org/0000-0002-1337-1105)
- Jing Chen (ORCID: https://orcid.org/0000-0002-7611-4173)
- Kexin Wang (ORCID: https://orcid.org/0000-0001-9184-3967)
- Shanshan Liu (ORCID: https://orcid.org/0009-0007-0775-5616)
- Chris Cotsapas (ORCID: https://orcid.org/0000-0002-7772-5910)
- Edward Lee (ORCID: https://orcid.org/0000-0003-0418-1454)
- Li-Zhen Song (ORCID: https://orcid.org/0000-0003-0955-3261)
- Hiroki Kimura (ORCID: https://orcid.org/0000-0001-9419-9855)
- Nguyễn Hoàng Việt (ORCID: https://orcid.org/0009-0002-5216-2282)
- David K. Stevenson (ORCID: https://orcid.org/0000-0002-7127-0281)
- Viviana Simon (ORCID: https://orcid.org/0000-0002-6416-5096)
- Andrew Schroeder (ORCID: https://orcid.org/0000-0002-8232-7837)
- Brent R. Brown (ORCID: https://orcid.org/0000-0003-3742-3763)
- Jacob E. Rogers
- Leeba Sullivan
- Koji Abe
- Lindsey B. Rosen
- Allison Nelson
- Paul Harris (ORCID: https://orcid.org/0000-0002-4758-0685)
- Gregory A. Michelotti (ORCID: https://orcid.org/0000-0002-7908-1979)
- Zenab Khan
- Jayant V. Rajan
- Nicklaus Rodriguez
- Kari E. Wong
- Ana Gonzalez
- M. Fried
- Adreanne M. Rivera
- J. Leland Booth
- Lindsey R. Baden
- Vicki Seyfert‐Margolis
- Christopher Huerta
- Omkar Chaudhary
- Brittany Roth Manning
- Edward H. Lin
- Subha Sen
- Kai Nie (ORCID: https://orcid.org/0000-0002-7963-8431)
- Jonathan Sevransky
- Bushra Samad
- Albert Marisa
- Yanedth Sanchez Guerrero
- Serena Lee
- Michael M. Matthay
- Michelle Conway
- Nicole Sutter
- Meagan Karoly
- Courtney Micheletti
- Wade L. Shulz
- Henna Naz Din
- Pam Schearer
- Judie Sheidy
Institutions
- Broad Institute (US)
- Brigham and Women's Hospital (US)
- Boston Children's Hospital (US)
- National Institutes of Health (US)
- La Jolla Institute for Immunology (US)
- Harvard University (US)
- University of Arizona (US)
- University of British Columbia (CA)
- Emory University (US)
- University of California, Los Angeles (US)
- Oregon Health & Science University (US)
- Palo Alto University (US)
- University of California, San Francisco (US)
- Baylor College of Medicine (US)
- University of Washington (US)
- University of South Florida (US)
- University Hospitals of Cleveland (US)
- Yale University (US)
- University of Florida (US)
- Immunai (United States) (US)
- Chan Zuckerberg Initiative (United States) (US)
- Metabolon (United States) (US)
- Prevention of Organ Failure (CA)
- National Institute of Allergy and Infectious Diseases (US)
- OU Health
- University of Oklahoma Health Sciences Center (US)
- Case Western Reserve University (US)
- Drexel University (US)
- The University of Texas at Austin (US)
- Stanford University (US)
- Icahn School of Medicine at Mount Sinai (US)
Publication Details
- Journal
- Nature Communications
- Published
- 2025-01-10
- DOI
- https://doi.org/10.1038/s41467-025-55823-z
- Citations
- 5
- Primary Topic
- COVID-19 Clinical Research Studies
- Type
- article
- Field-Weighted Citation Impact
- 6.98
Funders
- Yale University
- National Institutes of Health
- University of California, Los Angeles
- National Heart, Lung, and Blood Institute
- National Institute of Allergy and Infectious Diseases