"Molecular dialog between Lactiplantibacillus plantarum and Drosophila: a tale of bacterial symbiotic cues"

Abstract :

Metazoans establish mutually beneficial interactions with their resident microorganisms. These interactions contribute to different aspects of host physiology including juvenile growth, a post-natal developmental process marked by rapid body-size increase and organ maturation. Drosophila melanogaster is a valuable experimental model to study the physiological consequences and underlying mechanisms of host-commensal bacteria interactions. Bacterial strains associated with Drosophila, including members of the genus Lactiplantibacillus, influence multiple physiological processes including juvenile growth, and in several occasions, the underlying symbiotic cues, i.e. bacterial molecules directly impacting host functionalities, have been identified.

Recently, in an effort to further characterize the bacterial machinery involved in Lactiplantibacillus plantarum (Lp)-mediated juvenile growth promotion, we identified through a forward genetic screening, the dltEXABCD operon as an important determinant of Lp-induced Drosophila larval growth(Matos et al., 2017; Nikolopoulos et al., 2023). These genes encode a multi-protein machinery responsible for the D-alanylation of Teichoic Acids (TA) in diverse gram-positive bacteria and in Lp (Nikolopoulos et al., 2022a, 2023). In a thorough study of D-Alanylation of TAs we showed that only lipoteichoic acid (LTAs) and not wall teichoic acids (WTAs) are D-alanylated in Lp cell envelopes and demonstrated that d-Ala-LTAs, in addition to peptidoglycan, are direct symbiotic cues supporting intestinal peptidase expression and juvenile growth in Drosophila (Nikolopoulos et al., 2023). Furthermore, in a study in which we looked for non-nutritional symbiotic cues that allow Drosophila’s symbiotic bacteria to influence the physiology of their host, we determined that Lp can support its host’s growth through a molecular dialog that requires functional operons encoding ribosomal and transfer RNAs (r/tRNAs) in Lp and the GCN2 kinase in Drosophila’s enterocytes. Our data indicate that Lp r/tRNAs activate GCN2 in a subset of larval enterocytes, a mechanism necessary to remodel the intestinal transcriptome and ultimately to support anabolic growth (Grenier et al., 2023).

The question remains how symbiotic cues in general, and d-Ala-LTA, peptidoglycan and r/tRNAs in particular, reach Drosophila intestinal cells in order to execute their beneficial effect on host physiology. Secreted bacterial vesicles are attractive candidates to support this interkingdom crosstalk, delivering bacterial motifs and/or effector molecules to intestinal cells. I will present our latest results and working hypothesis on this specific topic.

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