Localization and Bioreactivity of Cysteine-Rich Secretions in the Marine Gastropod Nucella lapillus.

Mariaelena D'Ambrosio,Mariana Calmão,Cátia Gonçalves,Maria Rodrigues,Pedro M Costa

doi:10.3390/md19050276

Abstract

Marine biodiversity has been yielding promising novel bioproducts from venomous animals. Despite the auspices of conotoxins, which originated the paradigmatic painkiller Prialt, the biotechnological potential of gastropod venoms remains to be explored. Marine bioprospecting is expanding towards temperate species like the dogwhelk Nucella lapillus, which is suspected to secrete immobilizing agents through its salivary glands with a relaxing effect on the musculature of its preferential prey, Mytilus sp. This work focused on detecting, localizing, and testing the bioreactivity of cysteine-rich proteins and peptides, whose presence is a signature of animal venoms and poisons. The highest content of thiols was found in crude protein extracts from the digestive gland, which is associated with digestion, followed by the peribuccal mass, where the salivary glands are located. Conversely, the foot and siphon (which the gastropod uses for feeding) are not the main organs involved in toxin secretion. Ex vivo bioassays with Mytilus gill tissue disclosed the differential bioreactivity of crude protein extracts. Secretions from the digestive gland and peribuccal mass caused the most significant molecular damage, with evidence for the induction of apoptosis. These early findings indicate that salivary glands are a promising target for the extraction and characterization of bioactive cysteine-rich proteinaceous toxins from the species.

Highlights

The current work disclosed the presence of differentially-bioactive thiol-rich proteins in various organs of the muricid marine gastropod Nucella lapillus
The highest concentrations of thiolic proteinaceous substances were found in peribuccal glandular mass, where the salivary glands are located, and in the digestive gland
The low concentration of thiols found in N. lapillus siphon likely indicates that this organ might be used only during predation process for injecting the venom rather than being primarily responsible for toxin secretion

Summary

Introduction

Venoms and poisons are constituted by complex mixtures of bioactives, from toxins to permeabilizing enzymes and co-factors, salts, and small peptides [3,4] that have been recruited into poisonous secretions through intricate evolutionary processes [2]. These bioreactive compounds are mostly used for defense, competition, and predation [5], and, due to their potential specificity towards a wide range of molecular targets, they gave rise to a considerable interest for drug discovery purposes [6]. Scorpions, and spiders have been receiving attention for their potential biomedical applications and were recently joined by marine invertebrates like cnidarians, annelids, cone snails, and even cephalopods [7,8,9]

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Conclusion