Structure-function analysis of Lactiplantibacillus plantarum DltE& reveals D-alanylated lipoteichoic acids as direct cues supporting Drosophila juvenile growth

  1. Nikos Nikolopoulos
  2. Renata Matos
  3. Stephanie Ravaud
  4. Pascal Courtin
  5. Houssam Akherraz
  6. Simon Palussiere
  7. Virginie Gueguen-Chaignon
  8. Marie Salomon-Mallet
  9. Alain Guillot
  10. Yann Guerardel
  11. Marie-Pierre Chapot-Chartier  Is a corresponding author
  12. Christophe Grangeasse  Is a corresponding author
  13. François Leulier  Is a corresponding author
  1. CNRS UMR 5086, Universite Claude Bernard, France
  2. Ecole Normale Supérieure de Lyon, France
  3. Universite Paris-Saclay, INRAE, France
  4. CNRS UAR3444, INSERM US8, Universite Claude Bernard, France
  5. Univ Lille, CNRS, UMR 8576, France

Abstract

Metazoans establish mutually beneficial interactions with their resident microorganisms. However, our understanding of the microbial cues contributing to host physiology remains elusive. Previously, we identified a bacterial machinery encoded by the dlt operon involved in Drosophila melanogaster's juvenile growth promotion by Lactiplantibacillus plantarum. Here, using crystallography combined with biochemical and cellular approaches, we investigate the physiological role of an uncharacterized protein (DltE) encoded by this operon. We show that lipoteichoic acids (LTAs) but not wall teichoic acids are D-alanylated in Lactiplantibacillus plantarumNC8 cell envelope and demonstrate that DltE is a D-Ala carboxyesterase removing D-Ala from LTA. Using the mutualistic association of L. plantarumNC8 and Drosophila melanogaster as a symbiosis model, we establish that D-alanylated LTAs (D-Ala-LTAs) are direct cues supporting intestinal peptidase expression and juvenile growth in Drosophila. Our results pave the way to probing the contribution of D-Ala-LTAs to host physiology in other symbiotic models.

Data availability

-Diffraction data have been deposited in PDB under the accession codes 8AGR/8AIK/8AJI/8AKH-All data generated during this study are included in the manuscript and supporting file and a single Source Data file has been provided.

The following data sets were generated

Article and author information

Author details

  1. Nikos Nikolopoulos

    Molecular Microbiology and Structural Biochemistry, CNRS UMR 5086, Universite Claude Bernard, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Renata Matos

    Institut de Génomique Fonctionnelle d eLyon, Ecole Normale Supérieure de Lyon, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7480-6099
  3. Stephanie Ravaud

    Molecular Microbiology and Structural Biochemistry, CNRS UMR 5086, Universite Claude Bernard, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5867-0785
  4. Pascal Courtin

    Micalis Institute, Universite Paris-Saclay, INRAE, Jouy-en-Josas, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Houssam Akherraz

    Institut de Genomique Fonctionnelle de Lyon, Ecole Normale Supérieure de Lyon, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Simon Palussiere

    Micalis Institute, Universite Paris-Saclay, INRAE, Jouy-en-Josas, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Virginie Gueguen-Chaignon

    Protein Science Facility, CNRS UAR3444, INSERM US8, Universite Claude Bernard, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Marie Salomon-Mallet

    Micalis Institute, Universite Paris-Saclay, INRAE, Jouy-en-Josas, France
    Competing interests
    The authors declare that no competing interests exist.
  9. Alain Guillot

    Micalis Institute, Universite Paris-Saclay, INRAE, Jouy-en-Josas, France
    Competing interests
    The authors declare that no competing interests exist.
  10. Yann Guerardel

    Unite de Glycobiologie Structurale et Fonctionnelle, Univ Lille, CNRS, UMR 8576, Lille, France
    Competing interests
    The authors declare that no competing interests exist.
  11. Marie-Pierre Chapot-Chartier

    Micalis Institute, Universite Paris-Saclay, INRAE, Jouy-en-Josas, France
    For correspondence
    marie-pierre.chapot-chartier@inrae.fr
    Competing interests
    The authors declare that no competing interests exist.
  12. Christophe Grangeasse

    Molecular Microbiology and Structural Biochemistry, CNRS UMR 5086, Universite Claude Bernard, Lyon, France
    For correspondence
    christophe.grangeasse@ibcp.fr
    Competing interests
    The authors declare that no competing interests exist.
  13. François Leulier

    Institut de Génomique Fonctionnelle d eLyon, Ecole Normale Supérieure de Lyon, Lyon, France
    For correspondence
    francois.leulier@ens-lyon.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4542-3053

Funding

Agence Nationale de la Recherche (ANR-18-CE15-0011)

  • Nikos Nikolopoulos
  • Renata Matos
  • Stephanie Ravaud
  • Pascal Courtin
  • Houssam Akherraz
  • Simon Palussiere
  • Virginie Gueguen-Chaignon
  • Marie Salomon-Mallet
  • Alain Guillot
  • Yann Guerardel
  • Marie-Pierre Chapot-Chartier
  • Christophe Grangeasse
  • François Leulier

Fondation pour la Recherche Médicale (DEQ20180839196)

  • Renata Matos
  • Houssam Akherraz
  • François Leulier

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2023, Nikolopoulos et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Nikos Nikolopoulos
  2. Renata Matos
  3. Stephanie Ravaud
  4. Pascal Courtin
  5. Houssam Akherraz
  6. Simon Palussiere
  7. Virginie Gueguen-Chaignon
  8. Marie Salomon-Mallet
  9. Alain Guillot
  10. Yann Guerardel
  11. Marie-Pierre Chapot-Chartier
  12. Christophe Grangeasse
  13. François Leulier
(2023)
Structure-function analysis of Lactiplantibacillus plantarum DltE& reveals D-alanylated lipoteichoic acids as direct cues supporting Drosophila juvenile growth
eLife 12:e84669.
https://doi.org/10.7554/eLife.84669

Share this article

https://doi.org/10.7554/eLife.84669

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