Genetic evidence for a protective role of the peritrophic matrix against intestinal bacterial infection in Drosophila melanogaster

Takayuki Kuraishi, Olivier Binggeli, Onya Opota, Nicolas Buchon, Bruno Lemaitre

Research output: Contribution to journalArticlepeer-review

160 Citations (Scopus)

Abstract

The peritrophic matrix (PM) forms a layer composed of chitin and glycoproteins that lines the insect intestinal lumen. This physical barrier plays a role analogous to that of mucous secretions of the vertebrate digestive tract and is thought to protect the midgut epithelium from abrasive food particles and microbes. Almost nothing is known aboutPMfunctions in Drosophila, and its function as an immune barrier has never been addressed by a genetic approach. Here we show that the Drosocrystallin (Dcy) protein, a putative component of the eye lens of Drosophila, contributes to adult PM formation. A loss-of-function mutation in the dcy gene results in a reduction of PM width and an increase of its permeability. Upon bacterial ingestion a higher level of expression of antibacterial peptides was observed in dcy mutants, pointing to an influence of this matrix on bacteria sensing by the Imd immune pathway. Moreover, dcy-deficient flies show an increased susceptibility to oral infections with the entomopathogenic bacteria Pseudomonas entomophila and Serratia marcescens. Dcy mutant flies also succumb faster than wild type upon ingestion of a P. entomophila toxic extract. We show that this lethality is due in part to an increased deleterious action of Monalysin, a pore-forming toxin produced by P. entomophila. Collectively, our analysis of the dcy immune phenotype indicates that the PM plays an important role in Drosophila host defense against enteric pathogens, preventing the damaging action of pore-forming toxins on intestinal cells.

Original languageEnglish
Pages (from-to)15966-15971
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume108
Issue number38
DOIs
Publication statusPublished - 2011 Oct 20

Keywords

  • Entomopathogens
  • Gut
  • Innate immunity
  • Insect immunity

ASJC Scopus subject areas

  • General

Fingerprint Dive into the research topics of 'Genetic evidence for a protective role of the peritrophic matrix against intestinal bacterial infection in Drosophila melanogaster'. Together they form a unique fingerprint.

Cite this