Zinc and mechanical prowess in the jaws of Nereis, a marine worm

Higher animals typically rely on calcification to harden certain tissues such as bones and teeth. Some notable exceptions can be found in invertebrates: The fangs, teeth, and mandibles of diverse arthropod species have been reported to contain high levels of zinc. Considerable quantities of zinc also occur in the jaws of the marine polychaete worm Nereis sp. High copper levels in the polychaete worm Glycera dibranchiata recently were attributed to a copper-based biomineral reinforcing the jaws. In the present article, we attempt to unravel the role of zinc in Nereis limbata jaws, using a combination of position-resolved state-of-the-art techniques. It is shown that the local hardness and stiffness of the jaws correlate with the local zinc concentration, pointing toward a structural role for zinc. Zinc always is detected in tight correlation with chlorine, suggesting the presence of a zinc–chlorine compound. No crystalline inorganic phase was found, however, and results from x-ray absorption spectroscopy further exclude the presence of simple inorganic zinc–chlorine compounds in amorphous form. The correlation of local histidine levels in the protein matrix and zinc concentration leads us to hypothesize a direct coordination of zinc and chlorine to the protein. A comparison of the role of the transition metals zinc and copper in the jaws of two polychaete worm species Nereis and Glycera, respectively, is presented.

[1]  H. W. Lefevre,et al.  Short Communication: High Concentrations of Zinc in the Fangs and Manganese in the Teeth of Spiders , 1989 .

[2]  P. Fratzl,et al.  Evaluation of 3D small-angle scattering from non-spherical particles in single crystals , 1993 .

[3]  P. Fratzl,et al.  Hydration Dependence of the Wood-Cell Wall Structure in Picea abies. A Small-Angle X-ray Scattering Study , 1996 .

[4]  J. Vincent,et al.  The presence of zinc or manganese as the predominant metal in the mandibles of adult, stored-product beetles , 1984 .

[5]  Mehmet Sarikaya,et al.  Nano-mechanical properties profiles across dentin–enamel junction of human incisor teeth , 1999 .

[6]  F. Young Biochemistry , 1955, The Indian Medical Gazette.

[7]  P. E. Gibbs,et al.  Metals in nereid polychaetes: the contribution of metals in the jaws to the total body burden , 1980, Journal of the Marine Biological Association of the United Kingdom.

[8]  H. Lowenstam,et al.  Magnetite in Denticle Capping in Recent Chitons (Polyplacophora) , 1962 .

[9]  P. Fratzl,et al.  Graded Microstructure and Mechanical Properties of Human Crown Dentin , 2001, Calcified Tissue International.

[10]  R. Schofield,et al.  Tooth hardness increases with zinc-content in mandibles of young adult leaf-cutter ants , 2002, Naturwissenschaften.

[11]  C. Perry,et al.  An x-ray analytical study of mandibles from Calanus pacificus, an herbivorous copepod , 1988 .

[12]  P. E. Gibbs,et al.  Copper-the Major Metal Component of Glycerid Polychaete Jaws , 1980, Journal of the Marine Biological Association of the United Kingdom.

[13]  T. Sosnick,et al.  Engineered metal binding sites map the heterogeneous folding landscape of a coiled coil , 2001, Nature Structural Biology.

[14]  A. Ankudinov,et al.  REAL-SPACE MULTIPLE-SCATTERING CALCULATION AND INTERPRETATION OF X-RAY-ABSORPTION NEAR-EDGE STRUCTURE , 1998 .

[15]  K Nadassy,et al.  Analysis of zinc binding sites in protein crystal structures , 1998, Protein science : a publication of the Protein Society.

[16]  P. E. Gibbs,et al.  Zinc - a major inorganic component of nereid polychaete jaws , 1979, Journal of the Marine Biological Association of the United Kingdom.

[17]  J. C. Elliott Biomineralization: chemical and biochemical perspectives , 1990 .

[18]  R. J. Williams,et al.  Biomineralization: Chemical and Biochemical Perspectives , 1989 .

[19]  G. Lawes,et al.  Scanning Electron Microscopy and X-Ray Microanalysis , 1987 .

[20]  Carmay Lim,et al.  Principles governing Mg, Ca, and Zn binding and selectivity in proteins. , 2003, Chemical reviews.

[21]  G. Pharr,et al.  An improved technique for determining hardness and elastic modulus using load and displacement sensing indentation experiments , 1992 .

[22]  W. T. Morgan,et al.  The histidine-rich glycoprotein of serum has a domain rich in histidine, proline, and glycine that binds heme and metals. , 1985, Biochemistry.

[23]  C. Tanford Macromolecules , 1994, Nature.

[24]  C. Fierke,et al.  Function and mechanism of zinc metalloenzymes. , 2000, The Journal of nutrition.

[25]  H. Lowenstam Lepidocrocite, an Apatite Mineral, and Magnetite in Teeth of Chitons (Polyplacophora) , 1967, Science.

[26]  T. N. Bhat,et al.  The Protein Data Bank , 2000, Nucleic Acids Res..

[27]  J. Rehr,et al.  Parallel calculation of electron multiple scattering using Lanczos algorithms , 2002 .

[28]  J. Vincent,et al.  The Specific Location of Zinc in Insect Mandibles , 1982 .

[29]  H. Lowenstam,et al.  Goethite in Radular Teeth of Recent Marine Gastropods , 1962, Science.

[30]  J. Vincent,et al.  ON THE INDENTATION HARDNESS OF INSECT CUTICLE , 1982 .

[31]  G. Stucky,et al.  High Abrasion Resistance with Sparse Mineralization: Copper Biomineral in Worm Jaws , 2002, Science.