Drosophila host defense after oral infection by an entomopathogenic Pseudomonas species

Abstract

Drosophila has been shown to be a valuable model for the investigation of host-pathogen interactions. Study of the Drosophila immune response has been hampered, however, by the lack of true Drosophila pathogens. In nearly all studies reported, the bacteria used were directly injected within the body cavity of the insect, bypassing the initial steps of a natural interaction. Here, we report the identification of a previously uncharacterized bacterial species, Pseudomonas entomophila (Pe), which has the capacity to induce the systemic expression of antimicrobial peptide genes in Drosophila after ingestion. In contrast to previously identified bacteria, Pe is highly pathogenic to both Drosophila larvae and adults, and its persistence in larvae leads to a massive destruction of gut cells. Using this strain, we have analyzed the modulation of the larval transcriptome upon bacterial infection. We found that natural infection by Pe induces a dramatic change in larval gene expression. In addition to immunity genes, our study identifies many genes associated with Pe pathogenesis that have been previously unreported.innate immunity ͉ microarray ͉ host-microbe interaction

Bacterial strategies to overcome insect defences

“…when the Erwinia persistence factor evf is overexpressed in Erwinia strains, infected larvae stop feeding (suggesting a food-uptake blockage), bacteria proliferate and a strong lethality is observed 36,37 . A third example of toxicity towards the insect gut is observed with P. entomophila, a bacterium that can infect and kill D. melanogaster larvae and adults after ingestion 31 . D. melanogaster infection by P. entomophila is also characterized by a cessation of feeding.…”

“…D. melanogaster infection by P. entomophila is also characterized by a cessation of feeding. Electron microscopy observations showed that infection with P. entomophila causes a loss of larval midgut integrity 31 . Comparative transcriptome analysis of D. melanogaster larvae orally infected by P. entomophila or E. c. carotovora 15 revealed that the expression of 205 genes is altered during a lethal infection compared with a non-lethal infection.…”

“…Most of these genes are important in gut physiology, which indicates that P. entomophila modifies the gut epithelium during the infectious process. one example of this is the activation of insect genes that encode cytoskeleton components that are regulated by the JNK pathway 31 .…”

“…AMP production in the gut epithelium can be triggered by E. c. carotovora 15 (REF. 36), P. entomophila 31 and S. marcescens 33 . This local response is mediated by the nuclear factor (NF)-κB signalling pathway called Imd 18,45 , through the recognition of Gram-negative peptidoglycan by the peptidoglycan recognition proteins (PGRPs), such as PGRP-LC 46 …”

“…A central role in gut tolerance to bacteria has been attributed to amidase PGRPs (PGRP-LB and PGRP-SC) as they abrogate the immunostimulatory activity of peptidoglycan fragments that are released by commensals 46,47 . It is also interesting to note the existence of specialization in the gut epithelium as only parts of the epithelium are immunoreactive, whereas bacteria are present throughout the midgut after infection 18,30,31 .…”