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Abstract
An external skeleton is an essential part of the body plan of many animals and is thought to be one of the key factors that enabled the great expansion in animal diversity and disparity during the Cambrian explosion. Molluscs are considered ideal to study the evolution of biomineralization because of their diversity of highly complex, robust and patterned shells. The molluscan shell forms externally at the interface of animal and environment, and involves controlled deposition of calcium carbonate within a framework of macromolecules that are secreted from the dorsal mantle epithelium. Despite its deep conservation within Mollusca, the mantle is capable of producing an incredible diversity of shell patterns, and macro- and micro-architectures. Here we review recent developments within the field of molluscan biomineralization, focusing on the genes expressed in the mantle that encode secreted proteins. The so-called mantle secretome appears to regulate shell deposition and patterning and in some cases becomes part of the shell matrix. Recent transcriptomic and proteomic studies have revealed marked differences in the mantle secretomes of even closely-related molluscs; these typically exceed expected differences based on characteristics of the external shell. All mantle secretomes surveyed to date include novel genes encoding lineage-restricted proteins and unique combinations of co-opted ancient genes. A surprisingly large proportion of both ancient and novel secreted proteins containing simple repetitive motifs or domains that are often modular in construction. These repetitive low complexity domains (RLCDs) appear to further promote the evolvability of the mantle secretome, resulting in domain shuffling, expansion and loss. RLCD families further evolve via slippage and other mechanisms associated with repetitive sequences. As analogous types of secreted proteins are expressed in biomineralizing tissues in other animals, insights into the evolution of the genes underlying molluscan shell formation may be applied more broadly to understanding the evolution of metazoan biomineralization.
Highlights
According to the fossil record many animal phyla diversified during the Late Precambrian to Early Cambrian, roughly 515–541 million years ago
The integration of the fields of genomics and proteomics into the study of molluscan biomineralization has revealed that shell formation is controlled by the highly coordinated expression of hundreds of genes, and the regulated secretion of proteins and other macromolecules
The dissection of the mantle gene regulatory network controlling shell fabrication is in its infancy, there is evidence, at least in early developmental stages, for a deep conservation of expression patterns of regulatory genes
Summary
According to the fossil record many animal phyla diversified during the Late Precambrian to Early Cambrian, roughly 515–541 million years ago (mya; [1, 2]). The mantle secretome markedly differs between molluscs In recent years, several studies have been conducted to identify proteins responsible for shell formation by isolating proteins contained in shells and/or genes expressed in the mantle that encode a signal peptide, which indicate a protein is either secreted or localized on the cell surface.
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