TY - JOUR

T1 - Tricks of the puppet masters: morphological adaptations to the interaction with nervous system underlying host manipulation by rhizocephalan barnacle Polyascus polygeneus

AU - Лянгузова, Анастасия Дмитриевна

AU - Арбузова, Наталья Алексеевна

AU - Ласкова, Екатерина Павловна

AU - Гафарова, Елизавета Рустамовна

AU - Репкин, Егор Алексеевич

AU - Матач, Дмитрий Александрович

AU - Еньшина, Ирина

AU - Миролюбов, Алексей Александрович

PY - 2023/11/14

Y1 - 2023/11/14

N2 - 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.

AB - 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.

KW - Animals

KW - Brachyura/parasitology

KW - Host-Parasite Interactions

KW - Lice Infestations

KW - Nervous System

KW - Parasites

KW - Serotonin

KW - Thoracica/anatomy & histology

UR - https://www.mendeley.com/catalogue/5b7da9f0-6e09-3c00-8897-db0cdf85fbbf/

U2 - 10.7717/peerj.16348

DO - 10.7717/peerj.16348

M3 - Article

C2 - 38025701

VL - 11

JO - PeerJ

JF - PeerJ

SN - 2167-8359

M1 - e16348

ER -