Proteo-transcriptomic analysis of the venom of the endoparasitoid wasp Pimpla turionellae and its impact on host insect epigenetic mechanisms

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OezbekRabia_2021_03_30.pdf (15.45 MB)

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2020

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DOI:
http://dx.doi.org/10.22029/jlupub-10591

Abstract

Parasitoid wasps are hymenopterans that use other insects as hosts for their offspring. Females deposit their eggs either in (endoparasitoid) or on (ectoparasitoid) the host and inject maternal venoms and viruses to modulate host physiology to ensure the survival of the wasp eggs. The endoparasitoid wasp Pimpla turionellae (Linnaeus) injects its venom with the egg to sabotage the host s cellular and humoral defense, arrest further host development, and paralyze the host pupa to promote their offspring s survival. In this work, the impact of parasitization was analyzed to test whether idiobiont endoparasitoids induce epigenetic reprogramming to overcome host immune defense and disturb host development, and P. turionellae venom components were characterized using a combined proteo-transcriptomic approach.The impact of parasitization was tested by monitoring differentially expressed genes involved in the immunity and developmental hormone signaling pathways of parasitized and control hosts, Galleria mellonella (Linnaeus). My results indicate that parasitization induces the suppression of host immune responses and the modulation of host development. The changes in gene expressions were related to alterations in the host s epigenetic mechanisms. Parasitization by P. turionellae induced changes in the acetylation ratios of specific histones and a transient decrease in the host s global DNA methylation. Additionally, I observed strong parasitization-specific changes in the host s microRNAs pattern that regulate gene expression at the post-transcriptional level.On a second level, the transcriptomic analysis of venom glands and the proteomic study of the crude venom of endoparasitoid wasp P. turionellae were combined and resulted in the identification of several enzymes, cysteine-rich peptides, and other proteins. Possible biological functions of the identified proteins were characterized with respect to other known parasitoid venoms. Interestingly, any evidence of pimplin, the previously described main paralytic factor of Pimpla hypochondriaca venom, was not identified. However, a new cysteine inhibitor knot (ICK) family (pimplin2) that is highly similar to known ICK-like neurotoxins was found as a highly expressed venom component.In conclusion, my thesis characterizes the venom composition of P. turionellae, describing the known and novel venom protein families. Furthermore, the new insights reveal that parasitization reprograms the epigenetic mechanisms of the host to disrupt its development and suppress its immune system. Finally, some of the identified but functionally unknown components, such as the linear, short protein pimplin4, will be bioactivity tested to perform an in-depth assessment of their promising potential in bioinsecticidal or antimicrobial applications.

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