Structure–function analysis of Lactiplantibacillus plantarum DltE reveals D-alanylated lipoteichoic acids as direct cues supporting Drosophila juvenile growth
Nikos Nikolopoulos,
Renata C 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
Affiliations
Nikos Nikolopoulos
Molecular Microbiology and Structural Biochemistry, CNRS UMR 5086, Université Claude Bernard Lyon 1, Lyon, France
Molecular Microbiology and Structural Biochemistry, CNRS UMR 5086, Université Claude Bernard Lyon 1, Lyon, France
Pascal Courtin
Université Paris-Saclay, INRAE, AgroParisTech, Micalis Institute, Jouy-en-Josas, France
Houssam Akherraz
Institut de Génomique Fonctionnelle de Lyon, Ecole Normale Supérieure de Lyon, CNRS UMR 5242, Université Claude Bernard Lyon 1, Lyon, France
Simon Palussiere
Université Paris-Saclay, INRAE, AgroParisTech, Micalis Institute, Jouy-en-Josas, France
Virginie Gueguen-Chaignon
Protein Science Facility, CNRS UAR3444, INSERM US8, Université Claude Bernard Lyon 1, Ecole Normale Supérieur de Lyon, Lyon, France
Marie Salomon-Mallet
Université Paris-Saclay, INRAE, AgroParisTech, Micalis Institute, Jouy-en-Josas, France
Alain Guillot
Université Paris-Saclay, INRAE, AgroParisTech, Micalis Institute, Jouy-en-Josas, France
Yann Guerardel
Institute for Glyco-core Research (iGCORE), Gifu University, Gifu, Japan; Univ. Lille, CNRS, UMR 8576 - UGSF - Unité de Glycobiologie Structurale et Fonctionnelle, Lille, France
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.