Preferential manganese accumulation in dreissenid byssal threads

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Abstract

The elemental composition of byssal threads from two freshwater mussels Dreissena polymorpha (zebra) and Dreissena bugensis (quagga) has been determined by proton-induced X-ray emission spectroscopy. Sulphur and manganese are present at 30–100-fold higher concentrations in the threads than in ambient waters of Lake Erie. Calcium, phosphorus and copper levels are also somewhat enhanced in byssus. Since dreissenid byssus is not mineralized, Mn may be organometallically complexed to the functional side chains of byssal proteins.

Introduction

Sclerotized tissues in animals rely on a variety of inorganic elements for strength, hardness and toughness. In biominerals such as bone and shell, these elements are deposited as crystalline salts within an organic, usually protein, scaffold [12]. Another less familiar strategy involves extensive complexation of metals such as zinc, copper, iron and manganese by functionalized side chains in proteins and polysaccharides. Mussel byssal threads 3, 22, spider and polychaete fangs 2, 8, 17and the mandibles and claws of a variety of arthropods [10]are examples of nonmineralized tissues rich in metals. Byssal threads of marine mussels have been particularly interesting models for studying the macromolecular complexation of metals since they contain Fe, Cu and Zn [3], the high affinity binding of which can be studied in vitro with purified byssal precursor proteins. Mefp-1, for example, is a 110-kD byssal precursor protein from Mytilus edulis that contains 15 mol% 3,4-dihydroxyphenylalanine (DOPA)—a post-translational modification of tyrosine. The DOPA functionalities in this protein bind to Fe3+ in the bis-or tris-catecholato mode with log stability constants in excess of 38 [23]. Thus, the 150 residues of DOPA per molecule of Mefp-1 can bind 50–75 molecules of Fe3+ [24]. For this reason, the byssal cuticle is sometimes referred to as ironclad [24].

Nonindigenous dreissenid mussels of the Great Lakes Region also make byssal threads for attachment to solid substrata in their environment. Zebra (Dreissena polymorpha) and quagga mussels (Dreissena bugensis) are, at best, distant relatives of mytilids and contain very different proteins in their byssus 1, 15, 16. No analysis of the elemental composition has been reported for dreissenid byssus. In the present study, we have used proton-induced X-ray emission (PIXE) spectroscopy to compare the elemental composition of zebra and quagga mussel byssal threads to that of the surrounding lake water.

Section snippets

Preparation of dreissenid byssus

D. polymorpha and D. bugensis used in these studies were obtained from Lake Erie near Buffalo, NY and identified according to published characteristics [14]. They were either used immediately or maintained in a 375-l refrigerated holding tank containing aerated tap water at 12°C. Byssi were dissected from 20 mussels, 12 D. polymorpha and eight D. bugensis, each containing between five and 25 threads. Each byssus was washed in a petri dish with 100 vol. of milli-Q water and air dried. Threads

Results and discussion

Although PIXE has better spacial resolution than the atomic absorption used in previous studies [3], it has not been previously applied to the elemental analysis of byssal threads. The results for all measurements are shown in Table 1. Several trends are evident. There is no significant difference between the metal content of D. polymorpha and D. bugensis byssus. This is surprising since the two have somewhat different byssal protein compositions 1, 16. Moreover, there is no apparent difference

Acknowledgements

We thank Alan Jordan of SUNY Buffalo for collecting the mussels. The National Sea Grant Office of NOAA through the Non-Indigenous Species Program provided funds for this research.

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