Midgut transcriptome assessment of the cockroach-hunting wasp Ampulex compressa (Apoidea: Ampulicidae)

PLoS One. 2021 Jun 24;16(6):e0252221. doi: 10.1371/journal.pone.0252221. eCollection 2021.

Abstract

The emerald jewel wasp Ampulex compressa (Hymenoptera: Ampulicidae) is a solitary wasp that is widely known for its specialized hunting of cockroaches as larvae provision. Adult wasps mainly feed on pollen and nectar, while their larvae feed on the cockroachs' body, first as ecto- and later as endoparsitoids. Little is known about the expression of digestive, detoxification and stress-response-related genes in the midgut of A. compressa, or about its transcriptional versatility between life stages. To identify gut-biased genes related to digestion, detoxification, and stress response, we explored the midgut transcriptome of lab-reared A. compressa, for both adults and larvae, by focusing on the top 100 significantly up- and down-regulated genes. From the top 100 significantly differentially expressed genes (DEGs), we identified 39 and 36 DEGs putatively related to digestion and detoxification in the adult wasps and larvae, respectively. The two carbohydrases alpha-glucosidase (containing an alpha-amylase domain) and glycosyl hydrolase family 31, as well as the two proteinases chymotrypsin and trypsin, revealed the highest gene diversity. We identified six significant DEGs related to detoxification, which comprise glutathione S-transferase, cytochrome P450s and UDP-glucuronosyltransferase. The gene expression levels that were significantly expressed in both life stages vary strongly between life stages, as found in genes encoding for chymotrypsin and trypsin or glycosyl hydrolases family 31. The number of genes related to alpha-glucosidase, glycosyl hydrolase family 31, and cytochrome P450s was found to be similar across nine reference hymenopteran species, except for the identified glycosyl hydrolase family 31 gene, which was absent in all reference bee species. Phylogenetic analyses of the latter candidate genes revealed that they cluster together with their homologous genes found in the reference hymenopteran species. These identified candidate genes provide a basis for future comparative genomic and proteomic studies on (ontogenetic) dietary transitions in Hymenoptera.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cockroaches / physiology*
  • Digestive System / growth & development
  • Digestive System / metabolism*
  • Gene Expression Profiling
  • Gene Expression Regulation, Developmental*
  • Host-Parasite Interactions*
  • Inactivation, Metabolic
  • Larva / physiology
  • Oxidative Stress
  • Phylogeny
  • Transcriptome*
  • Wasps / genetics*
  • Wasps / physiology

Grants and funding

This research was supported by grants given by the University of Freiburg, Germany (Project-ID 2100189601) to MS. JMJM was supported by a PhD scholarship from the Consejo Nacional de Ciencia y Tecnologia (CONACyT, Mexico) and by a grant from the German Academic Exchange Service (DAAD). The article processing charge was funded by the Baden-Wuerttemberg Ministry of Science, Research and Art and the University of Freiburg in the funding programme Open Access Publishing. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.