Sea shell diversity and rapidly evolving secretomes: insights into the evolution of biomineralization

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.

Co-option and de novo gene evolution underlie molluscan shell diversity

“…Conchiferan shells are layered and often covered by a thin, organic outer layer called the periostracum (Kocot et al 2016). The underlying calcified layers, typically comprising aragonitic or calcite crystals, confer specific physical properties to the shell, and are classified based on their crystalline microstructures [i.e., prismatic, nacreous, crossed lamellar or homogeneous (Chateigner et al 2000; Furuhashi et al 2009)].…”

Comparative proteomics of octocoral and scleractinian skeletomes and the evolution of coral calcification

“…These studies showed that invertebrate skeletal proteomes include varying fractions of novel proteins -producing no significant matches against DNA sequence databases -and do exhibit contrasting rates of conservation between and within lineages. For instance, about 40% of the skeletal proteome is shared among echinoderms (Flores & Livingston 2017) , while in molluscs the fraction of shared proteins is only about 10% (Kocot et al 2016) .…”

Connecting pattern to process: Growth of spiral shell sculpture in the gastropod Nucella ostrina (Muricidae: Ocenebrinae)

“…The model presented here offers a straightforward mechanism for the development of spiral shell sculpture that would be worth testing in other gastropods. Numerous transcriptomic and genetic surveys suggest that the molecular pathways and signaling for shell secretion is complicated, and some components are not very conserved (reviewed in Kocot, Aguilera, McDougall, Jackson, & Degnan, 2016). However, as modern tools and mollusc sampling improves, our ability to understand the formation and evolution shell morphology, both in terms of shell sculpture and shell color (Williams, 2017) improves.…”