Central Nervous System Responses of the Oriental migratory, Locusta migratoria manilensis, to Fungal Infection

Wei Zhang,Yuxian Xia,Qinlv Wei,Kai Jin,Jianhong Chen,Nemat O Keyhani

doi:10.1038/s41598-017-10622-5

Abstract

Responses of the central nervous system (CNS) to microbial challenge and the interplay between the CNS and the immune system are important for defending against pathogen attack. We have examined the CNS transcriptional response of Locusta migratoria manilensis to infection by the locust-specific fungal pathogen, Metarhizium acridum. CNS responses were examined during spore attachment, fungal germination and pre-penetration of the cuticle, and cuticle penetration/hemocoel ingress and proliferation. Effects were seen at the earliest time points (4 h post-infection) and the number of differentially expressed genes (DEGs) was highest during late mycosis (72 h post-infection). Significantly affected neurological pathways included genes involved in serotonergic, cholinergic, dopaminergic, GABAergic, and glutamergic synapse responses, as well as pathways responsible for synaptic vesicle cycle, long-term potentiation and depression, and neurotrophin and retrograde endocannabinoid signaling. In addition, a significant number of immune related DEGs were identified. These included components of the Toll, Imd and JAK/STAT pathways, consistent with interactions between the CNS and immune systems. The activation of immune response related CNS genes during early stage infection highlights the rapid detection of microbial pathogens and suggests an important role for the CNS in modulating immunity potentially via initiating behavioral adaptations along with innate immune responses.

Highlights

The central nervous system (CNS) integrates both external and internal sensory inputs, generating behavioral responses and regulating many physiological processes[1]
Despite well-known behavioral effects many fungal insect pathogens can have on their hosts[21], there are few reports that have examined invertebrate gene expression responses in the CNS within the context of a specialized microbial pathogen that infects via penetration and invasion of the insect cuticle
The change in gene expression indicate differing CNS response strategies that could be related to changes during M. acridum infection that include different fungal structures, e.g. spore, germ tube, appressoria, hyphae, and hyphal bodies, changes in infection location, i.e from cuticle to internal tissues, and altered components released by M. acridum, e.g. cuticle degrading enzymes, and secondary metabolites/toxins

Summary

Introduction

The central nervous system (CNS) integrates both external and internal sensory inputs, generating behavioral responses and regulating many physiological processes[1]. Insect pathogenic fungi of the Clavicipitaceae family, e.g. of the Beauveria and Metarhizium genera have been used in a wide range of insect biological control applications, including towards grasshoppers and locusts[14] Conidia of these fungi attach to the cuticle where they germinate and penetrate the exoskeleton of the insect via mechanical pressure and the production of a battery of cuticle degrading enzymes, whose products provide nutrients to the growing fungal hyphae[15]. RNA-seq was used to identify relative genes expression differences between infection and control groups pairwise over six representative infection stages These functional analyses were used to provide global gene expression responses concerning (1) the locust CNS response to fungal infection at representative infection stages, and (2) CNS transcripts implicated in immune regulation

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