Tricks of the puppet masters: morphological adaptations to the interaction with nervous system underlying host manipulation by rhizocephalan barnacle Polyascus polygeneus

Anastasia Lianguzova; Natalia Arbuzova; Ekaterina Laskova; Elizaveta Gafarova; Egor Repkin; Dzmitry Matach; Irina Enshina; Aleksei Miroliubov

doi:10.7717/peerj.16348

Tricks of the puppet masters: morphological adaptations to the interaction with nervous system underlying host manipulation by rhizocephalan barnacle Polyascus polygeneus

PeerJ. 2023 Nov 14:11:e16348. doi: 10.7717/peerj.16348. eCollection 2023.

Authors

Anastasia Lianguzova^{1

2}, Natalia Arbuzova^{1

2}, Ekaterina Laskova¹, Elizaveta Gafarova¹, Egor Repkin^{1

3}, Dzmitry Matach¹, Irina Enshina¹, Aleksei Miroliubov²

Affiliations

¹ Department of Invertebrate Zoology, St. Petersburg State University, St Petersburg, Russian Federation.
² Laboratory of Parasitic Worms and Protists, Zoological Institute of the Russian Academy of Science, St Petersburg, Russian Federation.
³ Research Park, Center for Molecular and Cell Technologies, St. Petersburg State University, St Petersburg, Russian Federation.

Abstract

Background: Rhizocephalan interaction with their decapod hosts is a superb example of host manipulation. These parasites are able to alter the host's physiology and behavior. Host-parasite interaction is performed, presumably, via special modified rootlets invading the ventral ganglions.

Methods: In this study, we focus on the morphology and ultrastructure of these special rootlets in Polyascus polygeneus (Lützen & Takahashi, 1997), family Polyascidae, invading the neuropil of the host's nervous tissue. The ventral ganglionic mass of the infected crabs were fixed, and the observed sites of the host-parasite interplay were studied using transmission electron microscopy, immunolabeling and confocal microscopy.

Results: The goblet-shaped organs present in the basal families of parasitic barnacles were presumably lost in a common ancestor of Polyascidae and crown "Akentrogonida", but the observed invasive rootlets appear to perform similar functions, including the synthesis of various substances which are transferred to the host's nervous tissue. Invasive rootlets significantly differ from trophic ones in cell layer composition and cuticle thickness. Numerous multilamellar bodies are present in the rootlets indicating the intrinsic cell rearrangement. The invasive rootlets of P. polygeneus are enlaced by the thin projections of glial cells. Thus, glial cells can be both the first hosts' respondents to the nervous tissue damage and the mediator of the rhizocephalan interaction with the nervous cells. One of the potential molecules engaged in the relationships of P. polygeneus and its host is serotonin, a neurotransmitter which is found exclusively in the invasive rootlets but not in trophic ones. Serotonin participates in different biological pathways in metazoans including the regulation of aggression in crustaceans, which is reduced in infected crabs. We conclude that rootlets associated with the host's nervous tissue are crucial for the regulation of host-parasite interplay and for evolution of the Rhizocephala.

Keywords: Crustaceans; Glial cells; Host manipulation; Host-parasite interaction; Nervous system; Rhizocephala; Serotonin.

MeSH terms

Animals
Brachyura* / parasitology
Host-Parasite Interactions
Lice Infestations*
Nervous System
Parasites*
Serotonin
Thoracica* / anatomy & histology

Substances

Serotonin

Grants and funding

This study was funded by grant of the Ministry of Science and Higher Education of the Russian Federation (No. 075-15-2021-1069). Anastasia Lianguzova was funded by a stipend from the Gennady Komissarov Foundation for the Support of Young Scientists. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.