Airway environment drives the selection of quorum sensing mutants and promote Staphylococcus aureus chronic lifestyle

Xiongqi Ding, Catherine Robbe-Masselot, Xiali Fu, Renaud Léonard, Benjamin Marsac, Charlene J. G. Dauriat, Agathe Lepissier, Héloïse Rytter, Elodie Ramond, Marion Dupuis, Daniel Euphrasie, Iharilalao Dubail, Cécile Schimmich, Xiaoquan Qin, Jessica Parraga, Maria Leite- de-Moraes, Agnes Ferroni, Benoit Chassaing, Isabelle Sermet-Gaudelus, Alain Charbit, Mathieu Coureuil () and Anne Jamet ()
Additional contact information
Xiongqi Ding: Université Paris Cité, INSERM UMR-S1151, CNRS UMR-S8253, Institut Necker Enfants Malades
Catherine Robbe-Masselot: Université Lille, CNRS, UMR 8576 - UGSF - Unité de Glycobiologie Structurale et Fonctionnelle
Xiali Fu: Université Paris Cité, INSERM UMR-S1151, CNRS UMR-S8253, Institut Necker Enfants Malades
Renaud Léonard: Université Lille, CNRS, UMR 8576 - UGSF - Unité de Glycobiologie Structurale et Fonctionnelle
Benjamin Marsac: Université Lille, CNRS, UMR 8576 - UGSF - Unité de Glycobiologie Structurale et Fonctionnelle
Charlene J. G. Dauriat: INSERM U1016, CNRS UMR8104, Université Paris Cité, Team «Mucosal Microbiota in Chronic Inflammatory Diseases»
Agathe Lepissier: Université Paris Cité, INSERM UMR-S1151, CNRS UMR-S8253, Institut Necker Enfants Malades
Héloïse Rytter: Université Paris Cité, INSERM UMR-S1151, CNRS UMR-S8253, Institut Necker Enfants Malades
Elodie Ramond: Genoscope, UMR8030, Laboratory of Systems & Synthetic Biology (LISSB), Xenome team
Marion Dupuis: Université Paris Cité, INSERM UMR-S1151, CNRS UMR-S8253, Institut Necker Enfants Malades
Daniel Euphrasie: Université Paris Cité, INSERM UMR-S1151, CNRS UMR-S8253, Institut Necker Enfants Malades
Iharilalao Dubail: Université Paris Cité, INSERM UMR-S1151, CNRS UMR-S8253, Institut Necker Enfants Malades
Cécile Schimmich: Physiopathology and epidemiology of equine diseases (PhEED), RD 675
Xiaoquan Qin: Université Paris Cité, Institut de physique du globe de Paris, CNRS
Jessica Parraga: AP-HP Centre Université de Paris Cité
Maria Leite- de-Moraes: Université Paris Cité, INSERM UMR-S1151, CNRS UMR-S8253, Institut Necker Enfants Malades
Agnes Ferroni: AP-HP Centre Université de Paris Cité
Benoit Chassaing: INSERM U1016, CNRS UMR8104, Université Paris Cité, Team «Mucosal Microbiota in Chronic Inflammatory Diseases»
Isabelle Sermet-Gaudelus: Université Paris Cité, INSERM UMR-S1151, CNRS UMR-S8253, Institut Necker Enfants Malades
Alain Charbit: Université Paris Cité, INSERM UMR-S1151, CNRS UMR-S8253, Institut Necker Enfants Malades
Mathieu Coureuil: Université Paris Cité, INSERM UMR-S1151, CNRS UMR-S8253, Institut Necker Enfants Malades
Anne Jamet: Université Paris Cité, INSERM UMR-S1151, CNRS UMR-S8253, Institut Necker Enfants Malades

Nature Communications, 2023, vol. 14, issue 1, 1-13

Abstract: Abstract Staphylococcus aureus is a predominant cause of chronic lung infections. While the airway environment is rich in highly sialylated mucins, the interaction of S. aureus with sialic acid is poorly characterized. Using S. aureus USA300 as well as clinical isolates, we demonstrate that quorum-sensing dysfunction, a hallmark of S. aureus adaptation, correlates with a greater ability to consume free sialic acid, providing a growth advantage in an air-liquid interface model and in vivo. Furthermore, RNA-seq experiment reveals that free sialic acid triggers transcriptional reprogramming promoting S. aureus chronic lifestyle. To support the clinical relevance of our results, we show the co-occurrence of S. aureus, sialidase-producing microbiota and free sialic acid in the airway of patients with cystic fibrosis. Our findings suggest a dual role for sialic acid in S. aureus airway infection, triggering virulence reprogramming and driving S. aureus adaptive strategies through the selection of quorum-sensing dysfunctional strains.

Date: 2023
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DOI: 10.1038/s41467-023-43863-2

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