Abstract

The zebra mussel Dreissena polymorpha is a well-established invasive model organism. Although extensively used in environmental sciences, virtually nothing is known of the molecular process of its shell calcification. By describing the microstructure, geochemistry and biochemistry/proteomics of the shell, the present study aims at promoting this species as a model organism in biomineralization studies, in order to establish a bridge with ecotoxicology, while sketching evolutionary conclusions. The shell of D. polymorpha exhibits the classical crossed-lamellar/complex crossed lamellar combination found in several heterodont bivalves, in addition to an external thin layer, the characteristics of which differ from what was described in earlier publication. We show that the shell selectively concentrates some heavy metals, in particular uranium, which predisposes D. polymorpha to local bioremediation of this pollutant. We establish the biochemical signature of the shell matrix, demonstrating that it interacts with the in vitro precipitation of calcium carbonate and inhibits calcium carbonate crystal formation, but these two properties are not strongly expressed. This matrix, although overall weakly glycosylated, contains a set of putatively calcium-binding proteins and a set of acidic sulphated proteins. 2D-gels reveal more than fifty proteins, twenty of which we identify by MS-MS analysis. We tentatively link the shell protein profile of D. polymorpha and the peculiar recent evolution of this invasive species of Ponto-Caspian origin, which has spread all across Europe in the last three centuries.

Highlights

  • In ecotoxicology, the usefulness of molluscs as sentinel organisms for tracing anthropic or natural pollution is well established [1]

  • At 30 μg of matrix, the inhibition is stronger, not complete since no plateau is obtained. These results suggest that the inhibitory capacity of the acid soluble matrix (ASM) of the shell of D. polymorpha is moderate

  • By characterizing the shell structure, chemistry and proteome of the invasive pollutant-tolerant bivalve Dreissena polymorpha this study lays the first foundation for correlating the biochemical properties of the shell matrix of D. polymorpha to the level of pollution of its surrounding environment

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Summary

Introduction

The usefulness of molluscs as sentinel organisms for tracing anthropic or natural pollution is well established [1]. Molluscs are widespread and versatile and can be used in almost all environments including marine [2], freshwater [3], terrestrial [4] and in PLOS ONE | DOI:10.1371/journal.pone.0154264. Other species withstand pollution and exhibit the capacity to accumulate high content of heavy metals or organic pollutants in their living tissues and in their shell [8], without any apparent impairment of their physiological functions. An example of such shell accumulation is the edible mussel Mytilus galloprovincialis, whose shell nacreous layer is a faultless recorder of lead contaminations in Galizian Rias [9]

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