Dissecting the immune response of a lepidopteran pest to an entomopathogenic nematobacterial complex

Entomopathogenic nematobacterial complexes (NBCs) are natural symbiotic associations between nematodes and bacteria that cooperate to infect and kill insects. Due to the originality of these pathogens and to their potential for biological control of diverse crop pests, their interactions with insects have been extensively studied. Results from these studies have shown that the parasitic success largely relies on complex interactions with the host’s immune system. However, the study of the dialogue that takes place between each NBC partner and the immune system suffers from a lack of knowledge of the immune responses that insects oppose to NBC infestations. In order to improve this knowledge, we provide here the first topologic transcriptional analysis of the immune response of an insect, the lepidopteran model Spodoptera frugiperda, to an NBC, the Steinernema carpocapsae-Xenorhabdus nematophila association. Our results show that S. frugiperda strongly responds to the infestation, with a mobilization of the three main immunocompetent tissues the NBC is confronted to, which are the midgut, the fat body and the hemocytes. The responses are particularly intense in the fat body and in the hemocytes, with a time-stable mobilization of diversified humoral and cellular immunity genes and pathways. Further analysis revealed that these responses correspond to combinations of nematode- and bacterium-induced ones, which paves the way for future studies of their interactions with the NBC. Finally, this analysis also allowed the identification of new candidate immune genes whose functional characterization could reveal new types of anti-nematode immune responses.