Molecular Phylogeny and Evolution of the Proteins Encoded by Coleoid (Cuttlefish, Octopus, and Squid) Posterior Venom Glands

Abstract

In this study, we report for the first time a detailed evaluation of the phylogenetic history and molecular evolution of the major coleoid toxins: CAP, carboxypeptidase, chitinase, metalloprotease GON-domain, hyaluronidase, pacifastin, PLA2, SE-cephalotoxin and serine proteases, with the carboxypeptidase and GON-domain documented for the first time in the coleoid venom arsenal. We show that although a majority of sites in these coleoid venom-encoding genes have evolved under the regime of negative selection, a very small proportion of sites are influenced by the transient selection pressures. Moreover, nearly 70 % of these episodically adapted sites are confined to the molecular surface, highlighting the importance of variation of the toxin surface chemistry. Coleoid venoms were revealed to be as complex as other venoms that have traditionally been the recipient of the bulk of research efforts. The presence of multiple peptide/protein types in coleoids similar to those present in other animal venoms identifies a convergent strategy, revealing new information as to what characteristics make a peptide/protein type amenable for recruitment into chemical arsenals. Coleoid venoms have significant potential not only for understanding fundamental aspects of venom evolution but also as an untapped source of novel toxins for use in drug design and discovery.

Distribution of Chitinolytic Enzymes in the Organs and cDNA Cloning of Chitinase Isozymes from the Liver of Golden Cuttlefish <i>Sepia esculenta</i>

“…Furthermore, although high chitinolytic activity was detected in the posterior salivary gland, as shown in Figure 2, neither SeChi-1 nor SeChi-2 were expressed there. The presence of chitinases acting as poison in the posterior salivary gland of other cephalopods has been reported [33] [34]. Additionally, the presence of chitinases isozymes, which differ from SeChi-1 and SeChi-2, is suggested in the posterior salivary glandof S. esculenta.…”

“…This is consistent with the feeding habit of S. esculenta; that is, S. esculenta ingests organisms containing chitinous substances, such as shrimps and crabs [36], suggesting that S. esculenta degrades chitin from feed into GlcNAc using both endo-and exo-type enzymes. In addition, it is possible that chitinases in the posterior salivary gland act as a poison, as observed in other cephalopods [33] [34]. Furthermore, because blood chitinases in mollusks have important roles in immunity [23], chitinases in the heart and branchial heart, which are not involved in digestion, are involved in defense against organisms containing chitinous substances, such as parasitic crustaceans and nematodes.…”

“…However, the full-length genes have not yet been determined. Conversely, chitinases have been obtained from the posterior salivary gland of octopus [33] and cuttlefish [34], and found to act as poison. A chitotriosidase gene, which is involved in the induction of luminescent bacteria, has been found in the light organ of the Hawaiian bobtail squid Euprym- [35].…”

Production and packaging of a biological arsenal: Evolution of centipede venoms under morphological constraint

“…In animals that rely on venom for prey capture and handling, diet and foraging ecology is thought to be one of the major drivers of toxin evolution (3). In this scenario, diversification of toxins is driven by antagonistic coevolution between predator and prey, and is often evidenced by rapid radiation and sustained diversity of toxin gene families (4)(5)(6)(7)(8)(9).…”

Evolution and diversification of the cnidarian venom system

“…Thus, a majority of positively selected or episodically adaptive sites in neurotoxins are surface exposed. RAVER has been reported in a myriad of animal lineages and in a plethora of venom proteins, including scorpion neurotoxins [91,181,182,184,[188][189][190][191].…”