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Host-microbe multiomic profiling identifies distinct COVID-19 immune dysregulation in solid organ transplant recipients

Nature Communications, 2025

Pickering H., Schaenman J., Phan H., Maguire C., Tsitsiklis A., Rouphael N., Higuita N., Atkinson M., Brakenridge S., Fung M., Messer W., Reed E., Rivera A., Pickering H., Sen S., Elashoff D., Ward D., Brook J., Ramires-Sanchez E., Llamas M., Perdomo C., Magyar C., Fulcher J., Erle D., Calfee C., Hendrickson C., Kangelaris K., Nguyen V., Lee D., Chak S., Ghale R., Gonzalez A., Jauregui A., Leroux C., Altamirano L., Rashid A., Willmore A., Woodruff P., Krummel M., Carrillo S., Ward A., Patel R., Wilson M., Dandekar R., Alvarenga B., Rajan J., Schroeder A., Fragiadakis G., Mick E., Guerrero Y., Love C., Maliskova L., Adkisson M., Leligdowicz A., Beagle A., Rao A., Sigman A., Samad B., Curiel C., Shaw C., Tietje-Ulrich G., Milush J., Singer J., Vasquez J., Tang K., Betancourt L., Santhosh L., Pierce L., Paz M., Matthay M., Thakur N., Rodriguez N., Sutter N., Jones N., Sinha P., Prasad P., Lota R., Rashid S., Asthana S., Bhide S., Lea T., Abe-Jones Y., Ehrlich L., Melamed E., Maguire C., Wylie D., Rousseau J., Hurley K., Geltman J., Siles N., Rogers J., Tipan P., Boddapati A., Tharp G., Pellegrini K., Johnson B., Panganiban B., Huerta C., Anderson E., Samaha H., Sevransky J., Bristow L., Beagle E., Cowan D., Hamilton S., Hodder T., Bechnak A., Cheng A., Mehta A., Ciric C., Spainhour C., Carter E., Scherer E., Usher J., Hellmeister K., Hussaini L., Hewitt L., Mcnair N., Ribeiro S., Wimalasena S., Metcalf J., Agudelo Higuita N., Sinko L., Booth J., Drevets D., Brown B., Brakenridge S., Ungaro R., Manning B., Moldawer L., Messer W., Hough C., Siegel S., Sullivan P., Lu Z., Brunton A., Strand M., Lyski Z., Coulter F., Micheletti C., Jayavelu N., Presnell S., Kohr B., Jancsyk T., Arnett A., Augustine A., Holland S., Rosen L., Lee S., Vaysman T., Ozonoff A., Chen J., Kho A., Milliren C., Chang A., McEnaney K., Syphurs C., Barton B., Lentucci C., Murphy M., Saluvan M., Shaheen T., Liu S., Albert M., Hayati A., Bryant R., Abraham J., Cooney M., Karoly M., Steen H., van Zalm P., Fatou B., Smolen K., Viode A., van Haren S., Jha M., Stevenson D., Thomas S., Petrova B., Kanarek N., Fernandez-Sesma A., Simon V., Van Bakel H., Gonzalez-Reiche A., Qi J., Lee B., Carreño J., Singh G., Raskin A., Tcheou J., Khalil Z., van de Guchte A., Farrugia K., Khan Z., Kelly G., Srivastava K., Eaker L., Bermúdez-González M., Mulder L., Beach K., Saksena M., Altman D., Kojic E., Sominsky L., Azad A., Bielak D., Kawabata H., Yellin T., Fried M., Sullivan L., Morris S., Kleiner G., Stadlbauer D., Dutta J., Xie H., Patel M., Nie K., Monahan B., Hafler D., Montgomery R., Shaw A., Gygi J., Duchen D., Pawar S., Konstorum A., Chen E., Cotsapas C., Wang X., Dela Cruz C., Iwasaki A., Mohanty S., Nelson A., Zhao Y., Farhadian S., Asashima H., Chaudhary O., Coppi A., Fournier J., Muenker M., Raddassi K., Rainone M., Ruff W., Salahuddin S., Shulz W., Vijayakumar P., Wang H., Wunder E., Young H., Ko A., Gabernet G., Esserman D., Guan L., Brito A., Rothman J., Grubaugh N., Wang K., Xu L., Maecker H., Pulendran B., Nadeau K., Rosenberg-Hasson Y., Leipold M., Sigal N., Rogers A., Fernandes A., Manohar M., Do E., Chang I., Lee A., Blish C., Din H., Roque J., Geng L., Artandi M., Davis M., Ahuja N., Yang S., Chinthrajah S., Hagan T., Holmes T., Abe K., Baden L., Mendez K., Lasky-Su J., Tong A., Rooks R., Desjardins M., Sherman A., Walsh S., Mitre X., Cauley J., Li X., Evans B., Montesano C., Licona J., Krauss J., Issa N., Chang J., Izaguirre N., Corry D., Kheradmand F., Song L., Nelson E., Kraft M., Bime C., Mosier J., Erickson H., Schunk R., Kimura H., Conway M., Francisco D., Molzahn A., Wilson C., Hughes T., Sierra B., Oberhaus J., Guirgis F., Borresen B., Anderson M., Peters B., Overton J., Vita R., Westendorf K., Tebbutt S., Shannon C., Sekaly R., Fourati S., McComsey G., Harris P., Sieg S., Yendewa G., Consolo M., Tribout H., Ribeiro S., Cairns C., Haddad E., Kutzler M., Bernui M., Cusimano G., Connors J., Woloszczuk K., Joyner D., Edwards C., Lee E., Lin E., Melnyk N., Powell D., Kim J., Goonewardene I., Simmons B., Smith C., Martens M., Croen B., Semenza N., Bell M., Furukawa S., McLin R., Tegos G., Rogowski B., Mege N., Ulring K., Schearer P., Sheidy J., Nagle C., Overton J., Hutton S., Michelotti G., Wong K., Rahman A., Seyfert-Margolis V., Salehi-rad R., Altman M., Becker P., Bosinger S., Eckalbar W., Hoch A., Doni Jayavelu N., Kim-Schulze S., Jenkins M., Kleinstein S., Krammer F., Maecker H., Ozonoff A., Diray-Arce J., Shaw A., Baden L., Levy O., Reed E., Langelier C.

Disease areaApplication areaSample typeProducts
Immunological & Inflammatory Diseases
Infectious Diseases
Pathophysiology
Serum
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Abstract

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.

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