Differential Regulation of Immune Signaling and Survival Response in Drosophila melanogaster Larvae upon Steinernema carpocapsae Nematode Infection.

Shruti Yadav,Ioannis Eleftherianos,Sonali Gupta

doi:10.3390/insects9010017

Abstract

Drosophila melanogaster is an excellent model to dissect the molecular components and pathways of the innate anti-pathogen immune response. The nematode parasite Steinernema carpocapsae and its mutualistic bacterium Xenorhabdus nematophila form a complex that is highly pathogenic to insects, including D. melanogaster. We have used symbiotic (carrying X. nematophila) and axenic (lacking X. nematophila) nematodes to probe the regulation of genes belonging to different immune signaling pathways in D. melanogaster larvae and assess the survival response of certain mutants to these pathogens. We found that both types of S. carpocapsae upregulate MyD88 (Toll), but not PGRP-LE (Imd); whereas axenic S. carpocapsae strongly upregulate Wengen (Jnk), Domeless (Jak/Stat), Dawdle (TGFβ, Activin), and Decapentaplegic (TGFβ, BMP). We further found that inactivation of Wengen and Decapentaplegic confers a survival advantage to larvae infected with axenic S. carpocapsae, whereas mutating PGRP-LE promotes the survival of larvae infected with symbiotic nematodes.

Highlights

Entomopathogenic nematodes are natural parasites that infect a range of insect species [1,2,3].In recent years, they have emerged as excellent models to dissect the molecular basis of nematode parasitism [4,5]
At 24 h post-infection, the transcript levels of PGRP-LE were slightly increased in larvae infected with symbiotic or axenic nematodes compared to the control larvae, this induction was not statistically significant (p = 0.2984 and p = 0.1554, respectively; Figure 1A)
We show that inactivation of PGRP-LE, which plays a key role in innate immunity by activating the Imd pathway, promotes the survival of D. melanogaster against symbiotic S. carpocapsae, whereas inactivation of Wgn (Jnk pathway) or Dpp (TGFβ pathway) genes promotes larval survival in response to axenic nematode infection

Summary

Introduction

Entomopathogenic nematodes are natural parasites that infect a range of insect species [1,2,3]. In recent years, they have emerged as excellent models to dissect the molecular basis of nematode parasitism [4,5]. The entomopathogenic nematode Steinernema carpocapsae forms an excellent tool to study the molecular interplay between insect hosts and nematode parasites [6,7]. When the food source is depleted, the nematodes take up their mutualistic bacteria and exit the insect as infective juveniles in search of new susceptible hosts [10].

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Conclusion