From head to rootlet: comparative transcriptomic analysis of a rhizocephalan barnacle Peltogaster reticulata (Crustacea: Rhizocephala) [version 1; peer review: 2 approved]

Background: Rhizocephalan barnacles stand out in the diverse world of metazoan parasites. The body of a rhizocephalan female is modified beyond revealing any recognizable morphological features, consisting of the interna, the system of rootlets, and the externa, a sac-like reproductive body. Moreover, rhizocephalans have an outstanding ability to control their hosts, literally turning them into “zombies”. Despite all these amazing traits, there is no genomic and transcriptomic data about any Rhizocephala. Methods: We collected transcriptomes from four body parts of an adult female rhizocephalan Peltogaster reticulata: externa and main, growing, and thoracic parts of the interna. We used all prepared data for the de novo assembly of the reference transcriptome. Next, a set of encoded proteins was determined, the expression levels of protein-coding genes in different parts of the parasite body were calculated and lists of enriched bioprocesses were identified. We also in silico identified and analyzed sets of potential excretory / secretory proteins. Finally, we applied phylostratigraphy and evolutionary transcriptomics approaches to our data. Results: The assembled reference transcriptome included transcripts of 12,620 protein-coding genes and was the first for both P. reticulata and Rhizocephala. Based on the results obtained, the spatial heterogeneity of protein-coding genes expression in different regions of P. reticulata adult female body was established. The results of both transcriptomic analysis and histological studies indicated the presence of germ-like cells in the lumen of the interna. The potential molecular basis of the interaction between the nervous system of the host and the parasite's interna was also determined. Given the prolonged expression of development-associated genes, we suggest that rhizocephalans “got stuck in the metamorphosis”, even in their reproductive stage. Conclusions: The results of the first comparative transcriptomic analysis for Rhizocephala not only clarified but also expanded the existing ideas about the biology of this amazing parasites.