A single gene that promotes interaction of a phytopathogenic bacterium with its insect vector, Drosophila melanogaster

Abstract

Insects are major vectors of plant and animal disease, and bacterial phytopathogens are often disseminated by flies. We have previously reported that some isolates of the phytopathogenic bacterial species Erwinia carotovora infect Drosophila and activate an immune response. Using a genetic screen, we have now identified two genes that are required by E. carotovora to infect Drosophila. One of these genes has a regulatory role whereas the other, evf, confers an infectious phenotype: its transfer to non-infectious Erwinia strains or to several enterobacteria improves survival in the gut and triggers the immune response. Overexpression of Erwinia virulence factor (evf) allowed bacteria to colonize the apical side of the gut epithelium and in some cases to spread to the body cavity. Our results demonstrate a specific interaction between plant pathogens and flies that promote their dissemination.

Bacterial strategies to overcome insect defences

“…overexpression of evf results in massive bacterial accumulation in the gut and insect mortality. Interestingly, no lethality was observed after direct injection of such bacteria into the body cavity, which indicates that Evf-mediated persistence is specific to the physiology and architecture of the D. melanogaster larval gut 36 .…”

“…The evf (Erwinia virulence factor) gene is required for bacterial persistence 36 . Transfer of the evf gene to other Gram-negative bacteria allows them to persist in D. melanogaster, indicating that a single determinant can enable persistence of bacteria in a host 36 .…”

“…The evf (Erwinia virulence factor) gene is required for bacterial persistence 36 . Transfer of the evf gene to other Gram-negative bacteria allows them to persist in D. melanogaster, indicating that a single determinant can enable persistence of bacteria in a host 36 . Evf does not seem to be involved in detoxifying or neutralizing molecules that participate in bacterial clearance, such as RoS and AMP, or in reprogramming metabolic pathways that render the bacterial cells refractory to elimination 37 .…”

“…Afp is not the only persistence factor that might perturb (directly or indirectly) gut physiology through a toxic effect on epithelial cells 41 . 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 .…”

“…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 …”