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Oxygen isotope composition in Modiolus modiolus aragonite in the context of biological and crystallographic control

Published online by Cambridge University Press:  05 July 2018

M. Cusack ,
D. Parkinson ,
A. Freer ,
A. Pérez-Huerta ,
A. E. Fallick  and
G. B. Curry
M. Cusack*
Affiliation:
Department of Geographical and Earth Sciences, Gregory Building, University of Glasgow, Lilybank Gardens, Glasgow G12 8QQ, UK
D. Parkinson
Affiliation:
Department of Geographical and Earth Sciences, Gregory Building, University of Glasgow, Lilybank Gardens, Glasgow G12 8QQ, UK
A. Freer
Affiliation:
Department of Chemistry, Glasgow Biomedical Research Centre, University of Glasgow, 120 University Place, Glasgow G12 8TA, UK
A. Pérez-Huerta
Affiliation:
Department of Geographical and Earth Sciences, Gregory Building, University of Glasgow, Lilybank Gardens, Glasgow G12 8QQ, UK
A. E. Fallick
Affiliation:
Scottish Universities Environmental Research Centre, Rankine Avenue, East Kilbride G75 0QF, UK
G. B. Curry
Affiliation:
Department of Geographical and Earth Sciences, Gregory Building, University of Glasgow, Lilybank Gardens, Glasgow G12 8QQ, UK
*
*E-mail: maggie.cusack@ges.gla.ac.uk
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Abstract

Living systems exert exquisite control on all aspects of biomineral production and organic components, including proteins, are essential to this biological control. The protein-rich extrapallial (EP) fluid of bivalve molluscs is a strong candidate for the source of such proteins. Differences in calcium carbonate polymorphs between Modiolus modiolus and Mytilus edulis are concurrent with differences in EP fluid protein profiles. In conjunction with this biological control is the environmental influence which is interpreted using proxies such as δ18O to determine the history of ambient seawater temperature. In the horse mussel, Modiolus modiolus, the difference in oxygen isotope fractionation in the nacreous aragonite and the prismatic aragonite layer results in respective δ18O values of 2.1±0.2% and 2.5±0.2%. These δ18O values result in estimates of ambient seawater of 12.1±0.6°C and 10.2±0.6°C for nacreous and prismatic aragonite, respectively. Electron backscatter diffraction is used here to determine the crystallographic orientation at high spatial resolution, allowing the measurements of stable isotopes to be accurately mapped in terms of shell architecture. These preliminary data suggest that it is essential to account for both polymorph and crystal habit when deciphering ambient seawater temperature using δ18O as a proxy.

Keywords

bivalve molluscpolymorphcrystal habitproteinoxygen isotopescrystallographic orientationelectron backscatter diffraction (EBSD)
Type
Research Article
Information
Mineralogical Magazine , Volume 72 , Issue 2 , April 2008 , pp. 569 - 577
Copyright
Copyright © The Mineralogical Society of Great Britain and Ireland 2008

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References

Addadi, L., Joester, D., Nudelman, F. and Weiner, S. (2006) Mollusk shell formation: a source of new concepts for understanding biomineralization processes. Chemistry — A European Journal, 12, 981–987.CrossRefGoogle ScholarPubMed
Auclair, A.-C, Joachimski, M.M. and Lecuyer, C. (2003) Deciphering kinetic, metabolic and environmental controls on stable isotope fractions between seawater and the shell of Terebratalia transversa (Brachiopoda). Chemical Geology, 202, 59–78.CrossRefGoogle Scholar
Belcher, A.M., Wu, X.H., Christensen, R.J., Hansma, P.K., Stucky, G.D. and Morse, D.E. (1996) Control of crystal phase switching and orientation by soluble mollusc-shell proteins. Nature, 381, 56–58.CrossRefGoogle Scholar
Belcher, A.M., Hansma, P.K., Stucky, G.D. and Morse, D.E. (1998) First steps in harnessing the potential of biomineralization as a route to new high-performance composite materials. Ada Materialia, 46, 733–736.Google Scholar
Bohm, F., Joachimski, M.M., Dullo, W.C., Eisenhauer, A., Lehnert, H., Reitner, J. and Worheide, G. (2000) Oxygen isotope fractionation in marine aragonite of coralline sponges. Geochimica et Cosmochimica Ada, 64, 1695–1703.CrossRefGoogle Scholar
Crowley, S.F. and Taylor, P.D. (2000) Stable isotope composition of the modern bryozoan skeletal carbonate from the Otago shelf, New Zealand. New Zealand Journal of Marine and Freshwater Research, 34, 333–353.CrossRefGoogle Scholar
Cusack, M., Laing, J.H., Brown, K. and Walton, D. (2000) Amino acids and proteins of calcitic brachiopod shells. Trends in Comparative Biochemistry and Physiology B, 6, 47–56.Google Scholar
Cusack, M., England, J., Parkinson, D., Dalbeck, P., Lee, MX., Curry, G.B. and Fallick, A.E. (2008) Oxygen isotope composition, magnesium distribution and crystallography of Terebratulina retusa. Fossils and Strata, 54, 259–267.Google Scholar
Cusack, M., England, J., Parkinson, D., Dalbeck, P., Lee, MX., Curry, G.B. and Fallick, A.E. (2008) Oxygen isotope composition, magnesium distribution and crystallography of Terebratulina retusa. Fossils and Strata, 54, 259–267.Google Scholar
Dalbeck, P., England, J., Cusack, M., Lee, M.R. and Fallick, A.E. (2006) Crystallography and chemistry of the calcium carbonate polymorph switch in M. edulis shells. European Journal of Mineralogy, 18, 601–609.CrossRefGoogle Scholar
Dickson, J.A.D. (1997) Synchronous intracrystalline 513C and 518O differences in natural calcite crystals. Mineralogical Magazine, 61, 243–248.CrossRefGoogle Scholar
Erez, J. (1978) Vital effect on stable-isotope composition seen in foraminifera and coral skeletons. Nature, 273, 199–202.CrossRefGoogle Scholar
Falini, G., Albeck, S., Weiner, S. and Addadi, L. (1996) Control of aragonite or calcite polymorphisms by mollusk shell macromolecules. Science, 271, 67–69.CrossRefGoogle Scholar
Feng, Q.L., Li, H.B., Pu, G., Zhang, D.M., Cui, F.Z. and Li, H.D. (2000) Crystallographic alignment of calcite prisms in the oblique prismatic layer of Mytilus edulis shell. Journal of Materials Science, 35, 3337–3340.CrossRefGoogle Scholar
Fritz, M., Belcher, A.M., Radmacher, M., Walters, D.A., Hansma, P.K., Stucky, G.D. and Mann, S. (1994) Flat pearls from biofabrication of organized composites on inorganic substrates. Nature, 371, 49–51.CrossRefGoogle Scholar
Gaffey, SJ. and Bronnimann, C.E. (1993) Effects of bleaching on organic and mineral phases in biogenic carbonates. Journal of Sedimentary Research, 63, 752–754.CrossRefGoogle Scholar
Grossman, EX. and Ku, T.-L. (1986) Oxygen and carbon isotope fractionation in biogenic aragonite: temperature effects. Chemical Geology, 59, 59–74.CrossRefGoogle Scholar
Harper, E.M. (2000) Are calcitic layers an effective adaptation against shell dissolution in the bivalvia? Journal of Zoology, London, 251, 179–186.CrossRefGoogle Scholar
Hattan, S.J., Laue, T.M. and Chasteen, N.D. (2001) Purification and characterization of a novel calcium-binding protein from the extrapallial fluid of the mollusc, Mytilus edulis. The Journal of Biological Chemistry, 276, 4461–4468.CrossRefGoogle Scholar
Hincke, M.T., Gautron, J., Tsang, C.P.W., McKee, M.D. and Nys, Y. (1999) Molecular cloning and ultra-structural localisation of the core protein of an eggshell matrix proteoglycan, ovocleidin-116. The Journal of Biological Chemistry, 274, 32915–32923.CrossRefGoogle Scholar
Kono, M., Hayashi, N. and Samata, T. (2000) Molecular mechanism of the nacreous layer formation in pinctada maxima. Biochemical and Biophysical Research Communications, 269, 213–218.CrossRefGoogle ScholarPubMed
Kranz, D.E., Williams, D.F. and Jones, D.S. (1987) Ecological and palaeoenvironmental information using stable isotope profiles from living and fossil molluscs. Palaeogeography Palaeoclimatology Palaeoecology, 58, 249–266.CrossRefGoogle Scholar
Lecuyer, C, Reynard, B. and Martineau, F. (2004) Stable isotope fractionation between mollusc shells and marine waters from Martinique island. Chemical Geology, 213, 293–305.CrossRefGoogle Scholar
Leveque, I., Cusack, M., Davis, S.A. and Mann, S. (2004) Promotion of fluorapatite crystallization by soluble-matrix proteins from lingula anatina shells. Angewandte Chemie — International Edition, 43, 885–888.CrossRefGoogle ScholarPubMed
Matsushiro, A., Miyashita, T., Miyamoto, H., Morimoto, K., Tonomura, B., Tanaka, A. and Sato, K. (2003) Presence of protein complex in prerequisite for aragonite crystallization in the nacreous layer. Marine Biotechnology, 5, 37–44.Google ScholarPubMed
Meibom, A., Yurimoto, H., Cuif, J.-P., Domart-Coulon, I., Houlbreque, F., Constantz, B., Dauphin, Y., Tambutte, E., Tambutte, S., Allemand, D., Wooden, J. and Dunbar, R. (2006) Vital effects in coral skeletal composition display strict three-dimensional control. Geophysical Research Letters, 33, 1–4.CrossRefGoogle Scholar
Parkinson, D., Curry, G.B., Cusack, M. and Fallick, A.E. (2005) Shell structure, patterns and trends of oxygen and carbon stable isotopes in modern brachiopod shells. Chemical Geology, 219, 193–235.CrossRefGoogle Scholar
Prior, D.J., Boyle, A.P., Brenker, F., Cheadle, M.C., Day, A., Lopez, G., Peruzzo, L., Potts, G.J., Reddy, S., Spiess, R., Timms, N.E., Trimby, P., Wheeler, J. and Zetterstrom, L. (1999) The application of electron backscatter diffraction and orientation contrast imaging in the SEM: the textural problems. American Mineralogist, 84, 1741 — 1759.CrossRefGoogle Scholar
Rahimpour-Bonab, H., Bone, Y. and Moussavi-Harami, R. (1997) Stable isotope aspects of modern molluscs, brachiopods, and marine cements from cool-water carbonates, Lacepede shelf, South Australia. Geochimica et Cosmochimica Ada, 61, 207–218.CrossRefGoogle Scholar
Samata, T., Hayashi, N., Kono, M., Hasegawa, K., Horita, C. and Akera, S. (1999) A new matrix protein family related to the nacreous layer formation of Pinctada fucata. FEBS Letters, 462, 225–229.CrossRefGoogle Scholar
Thompson, J.B., Paloczi, G.T., Kindt, J.H., Michenfelder, M., Smith, B.L., Stucky, G., Morse, D.E. and Hansma, P.K (2000) Direct observation of the transition from calcite to aragonite growth as induced by abalone shell proteins. Biophysical Journal, 79, 3307–3312.CrossRefGoogle ScholarPubMed
Vander Putten, E., Dehairs, F., Keppens, E. and Baeyens, W. (2000) High resolution distribution of trace elements in the calcite shell layer of modern Mytilus edulis: environmental and biological controls. Geochimica et Cosmochimica Ada, 64, 997–1011.CrossRefGoogle Scholar
Watanabe, T., Fukuda, I., China, K. and Isa, Y. (2003) Molecular analyses of protein components of the organic matrix in the exoskeleton of two scleractinian coral species. Comparative Biochemistry and Physiology B, 136, 767–774.CrossRefGoogle ScholarPubMed
Yin, Y., Huang, D., Paine, M.L., Reinhold, V.N. and Chasteen, N.D. (2005a) Characterization of the primary structure of the EP protein from the extrapallial fluid of the mollusc, Mytilus edulis. Abstracts of Papers of The American Chemical Society, 229, U228-U9.Google Scholar
Yin, Y., Huang, J., Paine, M.L., Reinhold, V.N. and Chasteen, N.D. (2005b) Structural characterization of the major extrapallial fluid protein of the mollusc Mytilus edulis: implications for function. Biochemistry, 44, 10720–10731.CrossRefGoogle Scholar