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

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 about PM functions 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.gut | innate immunity | insect immunity | entomopathogens

Pathogen-mediated manipulation of arthropod microbiota to promote infection

“…Interestingly, we previously showed that A. phagocytophilum infection of Ixodes ticks reduces expression of stat, and that colonization is enhanced when stat is silenced (65); this suggests a role for the PM as a contributing factor during A. phagocytophilum infection of the tick. The glycan-rich PM layer separates the gut lumen from the epithelial cells and provides a protective barrier in arthropods against microbes and components of the incoming blood meal (66). Periodic acid-Schiff (PAS) staining of A. phagocytophilum-infected and P1-injected nymphal guts showed a significant decrease of the PM-like layer, which leads to increased PM permeability.…”

Protective effects of <i>Phaseolus vulgaris</i> lectin against viral infection in <i>Drosophila </i>

“…An analysis with fluorescence-labeled lectin indicated the presence of lectin in the midgut of the digestive tracts of flies. However, we speculate that lectin did not enter the body across the wall of the tract due to the peritrophic matrix, which serves as a barrier against microbial pathogens (25). Therefore, the antiviral effects of P. vulgaris PHA do not appear to occur through a direct interaction with the virus, but by indirectly altering host responses against viral infection.…”

Friend, foe or food? Recognition and the role of antimicrobial peptides in gut immunity and Drosophila –microbe interactions

“…The gut is also the major contact point for microorganisms, whether pathogens, members of the microbiota or food (dietary microbes) [21,41]. Under normal conditions, the microbiota reside in the gut lumen within the endoperitrophic space [42], which is delimited by the peritrophic matrix, a grid-like structure of chitin polymers and proteins that lines the midgut [18,43] and limits the passage of luminal contents and pathogens [44]. Another physical barrier is provided by a mucus layer, composed of polysaccharides and proteins (mucins), which is located between the peritrophic matrix and the epithelium [18].…”