From head to rootlet: comparative transcriptomic analysis of a rhizocephalan barnacle Peltogaster reticulata (Crustacea: Rhizocephala) [version 2; 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, a system of rootlets, and the externa, a sac-like reproductive body. Moreover,...

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Main Authors: Aleksei Miroliubov, Maksim Nesterenko
Format: Article
Language:English
Published: F1000 Research Ltd 2023-01-01
Series:F1000Research
Subjects:
Online Access:https://f1000research.com/articles/11-583/v2
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author Aleksei Miroliubov
Maksim Nesterenko
author_facet Aleksei Miroliubov
Maksim Nesterenko
author_sort Aleksei Miroliubov
collection DOAJ
description 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, a 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 are no genomic or transcriptomic data about any Rhizocephala. Methods: We collected transcriptomes from four body parts of an adult female rhizocephalan Peltogaster reticulata: the externa, and the 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’s 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 any rhizocephalan. Based on the results obtained, the spatial heterogeneity of protein-coding gene expression in different regions of the adult female body of P. reticulata 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 their metamorphosis”, even at the 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 these extraordinary parasites.
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spelling doaj.art-7cf153014cf040338cbaa1bd518e169b2023-01-10T01:00:00ZengF1000 Research LtdF1000Research2046-14022023-01-0111142646From head to rootlet: comparative transcriptomic analysis of a rhizocephalan barnacle Peltogaster reticulata (Crustacea: Rhizocephala) [version 2; peer review: 2 approved]Aleksei Miroliubov0Maksim Nesterenko1https://orcid.org/0000-0002-8807-1115Laboratory of parasitic worms and protists, Zoological Institute of Russian Academy of Sciences, St Petersburg, 199034, Russian FederationDepartment of Invertebrate Zoology, St Petersburg State University, St Petersburg, 199034, Russian FederationBackground: 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, a 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 are no genomic or transcriptomic data about any Rhizocephala. Methods: We collected transcriptomes from four body parts of an adult female rhizocephalan Peltogaster reticulata: the externa, and the 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’s 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 any rhizocephalan. Based on the results obtained, the spatial heterogeneity of protein-coding gene expression in different regions of the adult female body of P. reticulata 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 their metamorphosis”, even at the 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 these extraordinary parasites.https://f1000research.com/articles/11-583/v2Rhizocephala parasitic barnacles evolutionary transcriptomics host manipulation colonialityeng
spellingShingle Aleksei Miroliubov
Maksim Nesterenko
From head to rootlet: comparative transcriptomic analysis of a rhizocephalan barnacle Peltogaster reticulata (Crustacea: Rhizocephala) [version 2; peer review: 2 approved]
F1000Research
Rhizocephala
parasitic barnacles
evolutionary transcriptomics
host manipulation
coloniality
eng
title From head to rootlet: comparative transcriptomic analysis of a rhizocephalan barnacle Peltogaster reticulata (Crustacea: Rhizocephala) [version 2; peer review: 2 approved]
title_full From head to rootlet: comparative transcriptomic analysis of a rhizocephalan barnacle Peltogaster reticulata (Crustacea: Rhizocephala) [version 2; peer review: 2 approved]
title_fullStr From head to rootlet: comparative transcriptomic analysis of a rhizocephalan barnacle Peltogaster reticulata (Crustacea: Rhizocephala) [version 2; peer review: 2 approved]
title_full_unstemmed From head to rootlet: comparative transcriptomic analysis of a rhizocephalan barnacle Peltogaster reticulata (Crustacea: Rhizocephala) [version 2; peer review: 2 approved]
title_short From head to rootlet: comparative transcriptomic analysis of a rhizocephalan barnacle Peltogaster reticulata (Crustacea: Rhizocephala) [version 2; peer review: 2 approved]
title_sort from head to rootlet comparative transcriptomic analysis of a rhizocephalan barnacle peltogaster reticulata crustacea rhizocephala version 2 peer review 2 approved
topic Rhizocephala
parasitic barnacles
evolutionary transcriptomics
host manipulation
coloniality
eng
url https://f1000research.com/articles/11-583/v2
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AT maksimnesterenko fromheadtorootletcomparativetranscriptomicanalysisofarhizocephalanbarnaclepeltogasterreticulatacrustacearhizocephalaversion2peerreview2approved