The venomous cocktail of the vampire snail Colubraria reticulata (Mollusca, Gastropoda)

Abstract

BackgroundHematophagy arose independently multiple times during metazoan evolution, with several lineages of vampire animals particularly diversified in invertebrates. However, the biochemistry of hematophagy has been studied in a few species of direct medical interest and is still underdeveloped in most invertebrates, as in general is the study of venom toxins. In cone snails, leeches, arthropods and snakes, the strong target specificity of venom toxins uniquely aligns them to industrial and academic pursuits (pharmacological applications, pest control etc.) and provides a biochemical tool for studying biological activities including cell signalling and immunological response. Neogastropod snails (cones, oyster drills etc.) are carnivorous and include active predators, scavengers, grazers on sessile invertebrates and hematophagous parasites; most of them use venoms to efficiently feed. It has been hypothesized that trophic innovations were the main drivers of rapid radiation of Neogastropoda in the late Cretaceous.We present here the first molecular characterization of the alimentary secretion of a non-conoidean neogastropod, Colubraria reticulata. Colubrariids successfully feed on the blood of fishes, throughout the secretion into the host of a complex mixture of anaesthetics and anticoagulants. We used a NGS RNA-Seq approach, integrated with differential expression analyses and custom searches for putative secreted feeding-related proteins, to describe in detail the salivary and mid-oesophageal transcriptomes of this Mediterranean vampire snail, with functional and evolutionary insights on major families of bioactive molecules.ResultsA remarkably low level of overlap was observed between the gene expression in the two target tissues, which also contained a high percentage of putatively secreted proteins when compared to the whole body. At least 12 families of feeding-related proteins were identified, including: 1) anaesthetics, such as ShK Toxin-containing proteins and turripeptides (ion-channel blockers), Cysteine-rich secretory proteins (CRISPs), Adenosine Deaminase (ADA); 2) inhibitors of primary haemostasis, such as novel vWFA domain-containing proteins, the Ectonucleotide pyrophosphatase/phosphodiesterase family member 5 (ENPP5) and the wasp Antigen-5; 3) anticoagulants, such as TFPI-like multiple Kunitz-type protease inhibitors, Peptidases S1 (PS1), CAP/ShKT domain-containing proteins, Astacin metalloproteases and Astacin/ShKT domain-containing proteins; 4) additional proteins, such the Angiotensin-Converting Enzyme (ACE: vasopressive) and the cytolytic Porins.ConclusionsColubraria feeding physiology seems to involve inhibitors of both primary and secondary haemostasis, anaesthetics, a vasoconstrictive enzyme to reduce feeding time and tissue-degrading proteins such as Porins and Astacins. The complexity of Colubraria venomous cocktail and the divergence from the arsenal of the few neogastropods studied to date (mostly conoideans) suggest that biochemical diversification of neogastropods might be largely...

A key tyrosine substitution restricts nucleotide hydrolysis by the ectoenzyme NPP5

“…The vampire snail Colubraria reticulata secretes anticoagulants during feeding, and a protein similar to NPP5 is highly expressed in its salivary tissue [19]. The vampire snail Colubraria reticulata secretes anticoagulants during feeding, and a protein similar to NPP5 is highly expressed in its salivary tissue [19].…”

“…Orthologs of NPP5 have also been reported in nonvertebrates. The vampire snail Colubraria reticulata secretes anticoagulants during feeding, and a protein similar to NPP5 is highly expressed in its salivary tissue [19]. In the parasitic flatworms Schistosoma mansoni and Schistosoma japonicum, which live in blood capillaries, an ortholog of NPP5 is also present, on the outer layer of the worm [20,21].…”

“…In contrast, it was identified as an angiogenesisrelated gene in pediatric high-grade glioma [18]. Orthologs of this enzyme have been reported in the salivary tissue of the vampire snail which feeds on the blood of fish [19] and in parasitic flatworms that live in blood capillaries [20][21][22]. Metabolism of nucleotides in the circulation was proposed as a function for these homologs.…”

Insights into the Hypertensive Effects of Tityus serrulatus Scorpion Venom: Purification of an Angiotensin-Converting Enzyme-Like Peptidase

“…Also, functional ACE-like activity was detected in animal venoms of the fish-hunting cone snail [13], vampire snail [28], and solitary endoparasitic wasp [14]. In scorpions, ACE-like peptidases were detected by transcriptome analysis in Hottentotta judaicus [29], Tityus stigmurus [30], and Tityus bahiensis [17] venoms.…”

Purificação e caracterização de peptidases presentes no veneno do escorpião <i>Tityus serrulatus</i>.

“…Also, functional ACE-like activity was detected in animal venoms of the fish-hunting cone snail [13], vampire snail [28], and solitary endoparasitic wasp [14]. In scorpions, ACE-like peptidases were detected by transcriptome analysis in Hottentotta judaicus [29], Tityus stigmurus [30], and Tityus bahiensis [17] venoms.…”