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Gut Dysbiosis during Influenza Contributes to Pulmonary Pneumococcal Superinfection through Altered Short-Chain Fatty Acid Production

Valentin Sencio 1 Adeline Barthélémy 1 Luciana Tavares 2 Marina Machado 1, 2 Daphnée Soulard 1 Céline Cuinat 3, 4 Celso Martins Queiroz-Junior 2 Marie-Louise Noordine 4, 3 Sophie Salomé-Desnoulez 1 Lucie Deryuter 1 Benoit Foligne 5 Céline Wahl 6 Benoit Frisch 7 Angelica Vieira 2 Christophe Paget 1 Graeme Milligan 8 Trond Ulven 9 Isabelle Wolowczuk 1 Christelle Faveeuw 1 Ronan Le Goffic 10 Muriel Thomas 4, 3 Stéphanie Ferreira 6 Mauro Teixeira 2 François Trottein 1, *
* Corresponding author
1 CIIL - Centre d’Infection et d’Immunité de Lille - INSERM U 1019 - UMR 9017 - UMR 8204
2 Instituto de Ciencias Biologicas [Minas Gerais]
3 Université Paris-Saclay
4 MICALIS - MICrobiologie de l'ALImentation au Service de la Santé
5 INFINITE (Ex-Liric) - Institute for Translational Research in Inflammation - U 1286
6 Genoscreen [Lille]
7 LCB - Laboratoire de chimie bioorganique
8 Institute of Molecular, Cell and Systems Biology - Centre for Translational Pharmacology [Glasgow, Scotland, UK]
9 Department of Pharmacology [Copenhagen, Denmark]
10 VIM (UR 0892) - Virologie et Immunologie Moléculaires
Abstract : Secondary bacterial infections often complicate viral respiratory infections. We hypothesize that perturbation of the gut microbiota during influenza A virus (IAV) infection might favor respiratory bacterial superinfection. Sublethal infection with influenza transiently alters the composition and fermentative activity of the gut microbiota in mice. These changes are attributed in part to reduced food consumption. Fecal transfer experiments demonstrate that the IAV-conditioned microbiota compromises lung defenses against pneumococcal infection. In mechanistic terms, reduced production of the predominant short-chain fatty acid (SCFA) acetate affects the bactericidal activity of alveolar macrophages. Following treatment with acetate, mice colonized with the IAV-conditioned microbiota display reduced bacterial loads. In the context of influenza infection, acetate supplementation reduces, in a free fatty acid receptor 2 (FFAR2)-dependent manner, local and systemic bacterial loads. This translates into reduced lung pathology and improved survival rates of double-infected mice. Lastly, pharmacological activation of the SCFA receptor FFAR2 during influenza reduces bacterial superinfection.
Keywords : gut microbiota free fatty acid receptor 2 food restriction bacterial superinfection short-chain fatty acid acetate influenza A virus macrophages microbial dysbiosis
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Valentin Sencio, Adeline Barthélémy, Luciana Tavares, Marina Machado, Daphnée Soulard, et al.. Gut Dysbiosis during Influenza Contributes to Pulmonary Pneumococcal Superinfection through Altered Short-Chain Fatty Acid Production. Cell Reports, Elsevier Inc, 2020, 30 (9), pp.2934-2947.e6. ⟨10.1016/j.celrep.2020.02.013⟩. ⟨inserm-02501395⟩

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