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Airway Prevotella promote TLR2-dependent neutrophil activation and rapid clearance of Streptococcus pneumoniae from the lung

Author

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  • Kadi J. Horn

    (University of Colorado School of Medicine, Department of Otolaryngology)

  • Melissa A. Schopper

    (University of Colorado School of Medicine, Department of Otolaryngology)

  • Zoe G. Drigot

    (University of Colorado School of Medicine, Department of Otolaryngology
    University of Colorado Boulder, College of Arts and Sciences)

  • Sarah E. Clark

    (University of Colorado School of Medicine, Department of Otolaryngology)

Abstract

This study investigates how specific members of the lung microbiome influence the early immune response to infection. Prevotella species are a major component of the endogenous airway microbiota. Increased abundance of Prevotella melaninogenica correlates with reduced infection with the bacterial pathogen Streptococcus pneumoniae, indicating a potentially beneficial role. Here, we show that P. melaninogenica enhances protection against S. pneumoniae, resulting in rapid pathogen clearance from the lung and improved survival in a mouse lung co-infection model. This response requires recognition of P. melaninogenica lipoproteins by toll-like receptor (TLR)2, the induction of TNFα, and neutrophils, as the loss of any of these factors abrogates Prevotella-induced protection. Improved clearance of S. pneumoniae is associated with increased serine protease-mediated killing by lung neutrophils and restraint of P. melaninogenica-induced inflammation by IL-10 in co-infected mice. Together, these findings highlight innate immune priming by airway Prevotella as an important protective feature in the respiratory tract.

Suggested Citation

  • Kadi J. Horn & Melissa A. Schopper & Zoe G. Drigot & Sarah E. Clark, 2022. "Airway Prevotella promote TLR2-dependent neutrophil activation and rapid clearance of Streptococcus pneumoniae from the lung," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31074-0
    DOI: 10.1038/s41467-022-31074-0
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    1. Sudip Das & Eric Bernasconi & Angela Koutsokera & Daniel-Adrien Wurlod & Vishwachi Tripathi & Germán Bonilla-Rosso & John-David Aubert & Marie-France Derkenne & Louis Mercier & Céline Pattaroni & Alex, 2021. "A prevalent and culturable microbiota links ecological balance to clinical stability of the human lung after transplantation," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    2. Rebecca L. Brown & Richard P. Sequeira & Thomas B. Clarke, 2017. "The microbiota protects against respiratory infection via GM-CSF signaling," Nature Communications, Nature, vol. 8(1), pages 1-11, December.
    3. Beom Seok Park & Dong Hyun Song & Ho Min Kim & Byong-Seok Choi & Hayyoung Lee & Jie-Oh Lee, 2009. "The structural basis of lipopolysaccharide recognition by the TLR4–MD-2 complex," Nature, Nature, vol. 458(7242), pages 1191-1195, April.
    4. Evelyn Balsells & Laurence Guillot & Harish Nair & Moe H Kyaw, 2017. "Serotype distribution of Streptococcus pneumoniae causing invasive disease in children in the post-PCV era: A systematic review and meta-analysis," PLOS ONE, Public Library of Science, vol. 12(5), pages 1-20, May.
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    1. Georgios D. Kitsios & Khaled Sayed & Adam Fitch & Haopu Yang & Noel Britton & Faraaz Shah & William Bain & John W. Evankovich & Shulin Qin & Xiaohong Wang & Kelvin Li & Asha Patel & Yingze Zhang & Jos, 2024. "Longitudinal multicompartment characterization of host-microbiota interactions in patients with acute respiratory failure," Nature Communications, Nature, vol. 15(1), pages 1-18, December.

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