Combined Transcriptomic and Proteomic Analysis of the Posterior Salivary Gland from the Southern Blue-Ringed Octopus and the Southern Sand Octopus

This
study provides comprehensive proteomic profiles from the venom producing
posterior salivary glands of octopus (superorder Octopodiformes) species.
A combined transcriptomic and proteomic approach was used to identify
1703 proteins from the posterior salivary gland of the southern blue-ringed
octopus, Hapalochlaena maculosa and 1300 proteins
from the posterior salivary gland of the southern sand octopus, Octopus kaurna. The two proteomes were broadly similar;
clustering of proteins into orthogroups revealed 937 that were shared
between species. Serine proteases were particularly diverse and abundant
in both species. Other abundant proteins included a large number of
secreted proteins, many of which had no known conserved domains, or
homology to proteins with known function. On the basis of homology
to known venom proteins, 23 putative toxins were identified in H. maculosa and 24 in O. kaurna. These toxins span nine protein families: CAP (cysteine rich secretory
proteins, antigen 5, parthenogenesis related), chitinase, carboxylesterase,
DNase, hyaluronidase, metalloprotease, phospholipase, serine protease
and tachykinin. Serine proteases were responsible for 70.9% and 86.3%
of putative toxin expression in H. maculosa and O. kaurna, respectively, as determined using intensity
based absolute quantification (iBAQ) measurements. Phylogenetic analysis
of the putative toxin serine proteases revealed a similar suite of
diverse proteins present in both species. Posterior salivary gland
composition of H. maculosa and O. kaurna differ in several key aspects. While O. kaurna expressed the proteinaceous neurotoxin, tachykinin, this was absent
from H. maculosa, perhaps reflecting the acquisition
of a potent nonproteinaceous neurotoxin, tetrodotoxin (TTX) produced
by bacteria in the salivary glands of that species. The dispersal
factor, hyaluronidase was particularly abundant in H. maculosa. Chitinase was abundant in both species and is believed to facilitate
envenomation in chitinous prey such as crustaceans. Cephalopods represent
a largely unexplored source of novel proteins distinct from all other
venomous taxa and are of interest for further inquiry, as novel proteinaceous
toxins derived from venoms may contribute to pharmaceutical design.