Specialized structures on the border between rhizocephalan parasites and their host’s nervous system reveal potential sites for host-parasite interactions

Abstract

Rhizocephalan barnacles are a unique group of endoparasitic crustaceans. In their extreme adaptation to endoparasitism, rhizocephalan adults have lost almost all features of their free-living relatives but acquired an outstanding degree of control over the body of their hosts (mostly decapods). The subtle influence exercised by rhizocephalans on the physiology, morphology and behaviour of their hosts is a vivid example of the most intimate host-parasite interactions but their mechanisms are very poorly known. In this study we examined the morphology and the adaptive ultrastructure of the organs invading the nervous system of the host in two rhizocephalan species from the families Peltogastridae, (Peltogaster paguri) and Peltogasterellidae (Peltogasterella gracilis). We found two essentially different types of structures involved in interactions of these two rhizocephalans with the nervous system of their hosts: modified rhizocephalan rootlets lying inside the ganglia and the neural fibres of the host enlacing the trophic rootlets of the parasites. We suggest that both these structures may be highly specialized tools allowing the parasite to interact with the host on the humoral level via neuromediators, hormones, attractants and trophic factors.

Genomic Adaptations to an Endoparasitic Lifestyle in the Morphologically Atypical CrustaceanSacculina carcini(Cirripedia: Rhizocephala)

“…We also observed an unanticipated difference between the two interna samples from the host midgut and thoracic ganglia ( fig. 5 ), supporting recent reports showing the differing morphology and activity of rootlets in the rhizocephalan species Peltogasterella gracilis ( Miroliubov et al 2020 ) and Sacculina pilosella ( Lianguzova et al 2021 ). These studies describe morphological differentiation of those rootlets in contact with host nerve chords and indicate that these sites allow for humoral interactions between the parasite and host.…”

“…5 ). Recent studies with other Rhizocephala have shown that rootlets in different regions of the host take on different characteristics ( Miroliubov et al 2020 ). The 1870 differentially expressed genes (DEGs) included 1012 with conserved protein domains and we were able to assign Gene Ontology (GO) terms to 661 of them.…”

“…Parasitized crabs are mainly found submerged in seawater, whereas nonparasitized crabs sometimes forage on shallow water and tideland, suggesting additional behavioral changes ( Rasmussen 1959 ). Several detailed studies have focused on the morphological aspects of Rhizocephala, including S. carcini ( Bresciani and Høeg 2001 ; Glenner 2001 ; Miroliubov et al 2020 ). These have shown that the rootlet system can damage host tissue during infiltration, leading to necrosis and partial organ degeneration ( Powell and Rowley 2008 ; Rowley et al 2020 ).…”

From head to rootlet: comparative transcriptomic analysis of a rhizocephalan barnacle Peltogaster reticulata (Crustacea: Rhizocephala)

“…The body of an adult rhizocephalan female is represented by the interna, a system of hollow, ramifying rootlets infiltrating the body cavity of the host (also crustaceans, usually decapods), and the externa, a sac-like body protruding outside the host. The interna is responsible for absorbing nutrients from the host hemolymph and their transportation to the externa 1 as well as for interactions with the host 3 , 4 . The externa is a temporary structure thought to be an organ of sexual reproduction 5 .…”

“…These parasites can take control of the molting cycle of the hosts, change their metabolism, behaviour, and even body shape 2 , 10 – 20 . Specialized sites responsible for host-parasite interactions have recently been described 3 , 4 , with a network of the host’s neurons enlacing the rootlets of the parasite, but the molecular mechanisms of these interactions remained enigmatic. The authors suggested that the parasite may emit some signal molecules attracting the growth of the host’s neurons 3 .…”