The shell proteome of the deep-sea barnacle Bathylasma hirsutum and the convergency in barnacle and molluscan shell proteins

Abstract

AbstractBackgroundAs a group of sessile crustaceans that were being misclassified as mollusks by Carl Linnaeus, barnacles produce calcareous shell plates which, in most species, are permanently attached to the substratum. As biomineralization has independently evolved in multiple marine invertebrate taxa, a key question is how biomineralization has driven the evolution of genetic toolkits underlying shell formation. Here, we explore the shell proteome of the deep-sea acorn barnacleBathylasma hirsutum(Hoek, 1883) using an integrated transcriptomic-proteomic approach and compare the properties of barnacle shell proteins with molluscan shell matrix proteins.ResultsWe identified 31B. hirsutumbarnacle shell proteins (BSPs), including a series of key biomineralization proteins, such as carbonic anhydrase and C-type lectin. More than half of barnacle specific shell proteins (BSSPs) exhibit unknown functions. The amino acid composition of these BSSPs were biased toward A, D, E, G, S, P and Q, and were acidic and hydrophilic. Almost all BSSPs were detected with repetitive low complexity domains. Similar to molluscan shell matrix proteins, RLCDs in D-, and E-rich BSSPs constituted up to 50% amino acid of the whole protein. RLCDs in Q-rich proteins also exhibited similarity to a Q-rich abalone shell matrix protein and an insect cuticle protein.ConclusionFrom theB. hirsutumshell proteome, certain proteins such as carbonic anhydrase, C-type lectin, and peroxidase were implicated in shell formation or protein cross-linking across sessile invertebrate taxa. Despite the lack of sequence homology, D- and Q-rich BSSPs share similar features with molluscan shell matrix proteins in sequence redundancy, amino acid bias and thereby protein isoelectric point and hydropathy. Such convergence may reflect that similar selection pressures shape the molecular evolution of biomineralization and shell formation genes in marine invertebrates.