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ARS Home » Northeast Area » Newark, Delaware » Beneficial Insects Introduction Research Unit » Research » Publications at this Location » Publication #364214
Research Project: Host Specificity and Systematics of Insect Biological Control Agents

Location: Beneficial Insects Introduction Research Unit

Title: Immune suppressive extracellular vesicle proteins of Leptopilina heterotoma are encoded in the wasp genome

Author
item WEY, BRIAN - City University Of New York
item HEAVNER, MARY ELLEN - Rockefeller University
item Wittmeyer, Kameron
item BRIESE, THOMAS - Columbia University
item Hopper, Keith
item GOVIND, SHUBHA - City University Of New York

Submitted to: Journal of Hymenoptera Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/22/2019
Publication Date: 11/1/2019
Citation: Wey, B., Heavner, M., Wittmeyer, K.T., Briese, T., Hopper, K.R., Govind, S. 2019. Immune suppressive extracellular vesicle proteins of Leptopilina heterotoma are encoded in the wasp genome. Journal of Hymenoptera Research. 10:1-12. https://doi.org/10.1534/g3.119.400349.
DOI: https://doi.org/10.1534/g3.119.400349

Interpretive Summary: Leptopilina heterotoma are obligate parasitic wasps that develop within the bodies of their fruitfly hosts. Female L. heterotoma inject venom containing small extracellular vesicles into larval hosts. These vesicles contain proteins that play a critical role in wasp success by destroying host blood cells. In previous research, we identified 161 proteins in these vesicles than include infection and immunity-related proteins. Here we report 246 proteins from these vesicles. Sequencing and assembly of the genome of L. heterotoma revealed at least 30,000 genes, including 80% of genes found in most insects. Among genes in the genome, we identified those for a majority of the vesicle proteins. These results explain the stable association of the vesicles and wasps, and their transmission between females and their offspring. While our results do not rule out a viral origin of these genes, they support the production of vesicular proteins by the wasp genome and suggest that the strategy for co-opting cellular machinery for immune suppression may be shared by other wasps to gain advantage over their hosts.

Technical Abstract: Leptopilina heterotoma are obligate parasitoid wasps and develop within the body of their Drosophila hosts. During oviposition, female wasps introduce venom containing discrete 300 nm-wide mixed-strategy extracellular vesicles (MSEVs) into the larval host’s body cavity. Previously referred to as virus-like particles, MSEVs play a critical role in wasp success by destroying host blood cells. In recent proteomics analyses of MSEVs, we identified 161 proteins in three classes: conserved eukaryotic proteins, infection and immunity related proteins, and proteins without clear annotation. Here we report 246 additional MSEV proteins from the L. heterotoma proteome. An enrichment analysis of the entire proteome supports vesicular nature of these structures. Transcripts of more than 90% of these proteins were present in whole body Lh14 transcriptomes. Sequencing and assembly of the 460 Mb-sized Lh genome revealed at least wasp 30,000 genes, including 80% of the BUSCOs in the Insecta set. We identified genes for a majority of MSEV proteins within the genomic scaffolds. Altogether, these results explain the stable association of MSEVs with their wasps, and like other wasp structures, their vertical genetic pattern of inheritance. While our results do not rule out a viral origin of MSEVs, they support a vesicular nature and suggest that the strategy for co-opting cellular machinery for immune suppression may be shared by other wasps to gain advantage over their hosts. These results are relevant to our understanding of the evolution of figitid wasps.