Antimicrobial Peptides and Ectosymbiotic Relationships: Involvement of a Novel Type IIa Crustin in the Life Cycle of a Deep-Sea Vent Shrimp

Abstract

The symbiotic shrimp Rimicaris exoculata dominates the macrofauna inhabiting the active smokers of the deep-sea mid Atlantic ridge vent fields. We investigated the nature of the host mechanisms controlling the vital and highly specialized ectosymbiotic community confined into its cephalothoracic cavity. R. exoculata belongs to the Pleocyemata, crustacean brooding eggs, usually producing Type I crustins. Unexpectedly, a novel anti-Gram-positive type II crustin was molecularly identified in R. exoculata. Re-crustin is mainly produced by the appendages and the inner surfaces of the cephalothoracic cavity, embedding target epibionts. Symbiosis acquisition and regulating mechanisms are still poorly understood. Yet, symbiotic communities were identified at different steps of the life cycle such as brooding stage, juvenile recruitment and molt cycle, all of which may be crucial for symbiotic acquisition and control. Here, we show a spatio-temporal correlation between the production of Re-crustin and the main ectosymbiosis-related life-cycle events. Overall, our results highlight (i) a novel and unusual AMP sequence from an extremophile organism and (ii) the potential role of AMPs in the establishment of vital ectosymbiosis along the life cycle of deep-sea invertebrates.

A Crustin from Hydrothermal Vent Shrimp: Antimicrobial Activity and Mechanism

“…It is interesting that, based on its cysteine-rich region [ 30 ], Crus1 was classified by phylogenetic analysis as a member of the Type I crustin, which has been mainly found in crabs and lobsters [ 31 ]. This observation of Crus1 is in contrast to that of the recently reported Re-crustin from the hydrothermal vent in MAR, which is a Type II crustin [ 27 ] and, as shown in our study, shares a low sequence identity with Crus1. These results suggest the possible existence of diverse forms of crustins in deep sea hydrothermal shrimp.…”

“…MT375562). The sequence identity between Crus1 and Re-crustin, the Type II crustin identified in the shrimp from MAR [ 27 ], is 24.74%. The sequence alignment between Crus1 and representative Type I crustins indicated that the conserved WAP domain, in particular the 8 cysteines that form the four-disulfide core structure, was shared among the crustins ( Figure 1 A).…”

“…Shrimps of the family Alvinocarididae inhabit the deep waters in Atlantic, Pacific, and Indian Oceans, especially the hydrothermal vents and cold seeps, where they are often found to be the dominant fauna [ 25 , 26 ]. Recently, a novel anti-Gram-positive crustin, Re-crustin, was identified from the extremophile Pleocyemata shrimp, Rimicaris exoculata , collected from the hydrothermal vent site of the Mid-Atlantic Ridge (MAR) [ 27 ]. In a previous study, we identified several crustin-like genes from the transcriptome of the shrimp Rimicaris sp (Alvinocarididae family) from a hydrothermal vent in Desmos, manus basin [ 26 ].…”

Rimicaris exoculata: biology and ecology of a shrimp from deep-sea hydrothermal vents associated with ectosymbiotic bacteria

“…Anti-fungal activity was also demonstrated for Rsp ALF1. Le Bloa et al (2020) identified an AMP in R. exoculata, which they named Recrustin. Re-crustin is mainly synthesized in the tissues on which the ectosymbiotic community of the branchial chamber develops, i.e.…”

“…the branchiostegite and scaphognathite. As it is mostly expressed at the juvenile stage, Re-crustin has been proposed to be involved in symbiont attraction and adhesion (Le Bloa et al 2020). AMPs could thus also play a role in host symbiont recognition and not just in the regulation of their proliferation.…”