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SARS-CoV-2 Omicron BA.1 breakthrough infection drives late remodeling of the memory B cell repertoire in vaccinated individuals

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Sokal, Aurélien | Barba-Spaeth, Giovanna | Hunault, Lise | Fernandez, Ignacio | Broketa, Matteo | Meola, Annalisa | Fourati, Slim | Azzaoui, Imane | Vandenberghe, Alexis | Lagouge-Roussey, Pauline | Broutin, Manon | Roeser, Anais | Bouvier-Alias, Magali | Crickx, Etienne | Languille, Laetitia | Fournier, Morgane | Michel, Marc | Godeau, Bertrand | Gallien, Sébastien | Melica, Giovanna | Nguyen, Yann | Canoui-Poitrine, Florence | Pirenne, France | Megret, Jérôme | Pawlotsky, Jean-Michel | Fillatreau, Simon | Reynaud, Claude-Agnès | Weill, Jean-Claude | Rey, Félix | Bruhns, Pierre | Mahévas, Matthieu | Chappert, Pascal

Edité par CCSD ; Elsevier -

International audience. How infection by a viral variant showing antigenic drift impacts a preformed mature human memory B cell (MBC) repertoire remains an open question. Here, we studied the MBC response up to 6 months after SARS-CoV-2 Omicron BA.1 breakthrough infection in individuals previously vaccinated with three doses of the COVID-19 mRNA vaccine. Longitudinal analysis, using single-cell multi-omics and functional analysis of monoclonal antibodies from RBD-specific MBCs, revealed that a BA.1 breakthrough infection mostly recruited pre-existing cross-reactive MBCs with limited de novo response against BA.1-restricted epitopes. Reorganization of clonal hierarchy and new rounds of germinal center reactions, however, combined to maintain diversity and induce progressive maturation of the MBC repertoire against common Hu-1 and BA.1, but not BA.5-restricted, SARS-CoV-2 Spike RBD epitopes. Such remodeling was further associated with a marked improvement in overall neutralizing breadth and potency. These findings have fundamental implications for the design of future vaccination booster strategies.

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