Early Stage Biomineralization in the Periostracum of the ‘Living Fossil’ Bivalve Neotrigonia

Antonio G Checa,Carmen Salas,Elizabeth M Harper,Juan De Dios Bueno-Pérez,Masaya Yamamoto

doi:10.1371/journal.pone.0090033

Antonio G Checa, Carmen Salas + Show 3 more

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https://doi.org/10.1371/journal.pone.0090033

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Abstract

A detailed investigation of the shell formation of the palaeoheterodont ‘living fossil’ Neotrigonia concentrated on the timing and manufacture of the calcified ‘bosses’ which stud the outside of all trigonioid bivalves (extant and fossil) has been conducted. Electron microscopy and optical microscopy revealed that Neotrigonia spp. have a spiral-shaped periostracal groove. The periostracum itself is secreted by the basal cell, as a thin dark pellicle, becoming progressively transformed into a thin dark layer by additions of secretions from the internal outer mantle fold. Later, intense secretion of the internal surface of the outer mantle fold forms a translucent layer, which becomes transformed by tanning into a dark layer. The initiation of calcified bosses occurred at a very early stage of periostracum formation, deep within the periostracal groove immediately below the initialmost dark layer. At this stage, they consist of a series of polycyclically twinned crystals. The bosses grow as the periostracum traverse through the periostracal groove, in coordination with the thickening of the dark periostracal layer and until, upon reaching the mantle edge, they impinge upon each other and become transformed into large prisms separated by dark periostracal walls. In conclusion, the initial bosses and the external part of the prismatic layer are fully intraperiostracal. With later growth, the prisms transform into fibrous aggregates, although the details of the process are unknown. This reinforces the relationships with other groups that have the ability to form intraperiostracal calcifications, for example the unionoids with which the trigonioids form the clade Paleoheterodonta. The presence of similar structures in anomalodesmatans and other euheterodonts raises the question of whether this indicates a relationship or represents a convergence. The identification of very early calcification within an organic sheet has interesting implications for our understanding of how shells may have evolved.

Highlights

Molluscan shells are biocomposites formed by highly ordered calcium carbonate crystals in an organic matrix
The way in which molluscs make their shells has been of great interest for a variety of reasons; because of their advantageous mechanical properties, understanding their formation is of interests in the search for novel synthetic materials [1], [2] and biomedicine application [3]–[6], while the arrangement of different microstructures within their shells has been shown to have significance in the study of phylogenetic relationships [7]–[9] and of the adaptive significance of different microstructures, e.g. [10]–[12], within the phylum
The majority of research has focussed on the calcium carbonate structures of the shell [13]–[16] but more recently new researches have focussed on the role of the organic macromolecules in the formation and biomineral assembly [17]–[20]

Summary

Introduction

Molluscan shells are biocomposites formed by highly ordered calcium carbonate crystals in an organic matrix. The majority of research has focussed on the calcium carbonate structures of the shell [13]–[16] but more recently new researches have focussed on the role of the organic macromolecules in the formation and biomineral assembly [17]–[20]. Few studies, have investigated the role of the predominantly organic periostracum, an outer shell layer which is secreted by the mantle before the calcareous part of the shell and which has a fundamental importance in shell manufacture, in both isolating the site of biomineralization from the contaminating effects of seawater and providing the template onto which the mineralization process of the shell is carried out [21]–[24]. The varied nature of the calcification suggests perhaps that these are not synapomorphic characters that link particular taxa but rather reflect a deeper homology in the possession of some characters within the periostraca that facilitate calcification [34], while other authors [28], [37] have suggested that these structures may represent a symplesiomorphic bivalve condition

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