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Molecular Evolution of Mollusc Shell Proteins: Insights from Proteomic Analysis of the Edible Mussel Mytilus

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Abstract

Shell matrix proteins (SMPs) that are embedded within calcified layers of mollusc shells are believed to play an essential role in controlling the biomineral synthesis and in increasing its mechanical properties. Among the wide diversity of mollusc shell textures, nacro-prismatic shells represent a tremendous opportunity for the investigation of the SMP evolution. Indeed, nacro-prismatic texture appears early in Cambrian molluscs and is still present in the shell of some bivalves, gastropods, cephalopods and very likely also, of some monoplacophorans. One key question is to know whether these shells are constructed from similar matrix protein assemblages, i.e. whether they share a common origin. Most of the molecular data published so far are restricted to two genera, the bivalve Pinctada and the gastropod Haliotis. The shell protein content of these two genera are clearly different, suggesting independent origins or considerable genetic drift from a common ancestor. In order to describe putatively conserved mollusc shell proteins, here we have investigated the SMP set of a new bivalve model belonging to another genera, the edible mussel Mytilus, using an up-to-date proteomic approach based on the interrogation of more than 70,000 EST sequences, recently available from NCBI public databases. We describe nine novel SMPs, among which three are completely novel, four are homologues of Pinctada SMPs and two are very likely homologues of Haliotis SMPs. This latter result constitutes the first report of conserved SMPs between bivalves and gastropods. More generally, our data suggest that mollusc SMP set may follow a mosaic pattern within the different mollusc models (Mytilus, Pinctada, Haliotis). We discuss the function of such proteins in calcifying matrices, the molecular evolution of SMP genes and the origin of mollusc nacro-prismatic SMPs.

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Acknowledgments

The work of BM, NLR and FM is financially supported by an ANR (ACCRO-EARTH, ref. BLAN06-2_159971, coordinator Gilles Ramstein, LSCE) during the period 2007–2011. The “Conseil Régional de Bourgogne” (Dijon, France) provided additional supports for the acquisition of new equipment in the Biogeosciences research unit (UMR CNRS 5561). A complementary financial support was provided by INSU (Action INTERRVIE 2010). BM would like to thanks Davorin Medakovic for providing the fresh shells of Mytilus galloprovincialis and Jérome Thomas for handling shell pictures. The present protein sequences appear in the UniProtKB under the accession numbers P86853–P86861.

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  1. UMR 5561 CNRS Biogéosciences, Université de Bourgogne, 6 bd. Gabriel, Dijon, 21000, France

    Benjamin Marie, Nathalie Le Roy & Frédéric Marin

  2. IFR 128 BioSciences Gerland-Lyon Sud, UMR 5086 CNRS, Institut de Biologie et Chimie des Protéines, Université de Lyon 1, Lyon, France

    Isabelle Zanella-Cléon & Michel Becchi

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  1. Benjamin Marie
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Marie, B., Le Roy, N., Zanella-Cléon, I. et al. Molecular Evolution of Mollusc Shell Proteins: Insights from Proteomic Analysis of the Edible Mussel Mytilus . J Mol Evol 72, 531–546 (2011). https://doi.org/10.1007/s00239-011-9451-6

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