Crystal nucleation and near-epitaxial growth in nacre

Journal of Structural Biology

Volumn 184, Issue 3, 2013, Pages 454-463

  Olson, Ian C ^a   Blonsky, Adam Z ^a   Tamura, Nobumichi ^b   Kunz, Martin ^b   Pokroy, Boaz ^c   Romao, Carl P ^d   White, Mary Anne ^d   Gilbert, Pupa U P A ^a,e  

^a University of Wisconsin Madison   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^d DALHOUSIE UNIVERSITY   (Canada)

^e UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Aragonite; Biomineral; Bridge tilting; Diffraction; Epitaxial; Epitaxy; Low angle grain boundary; Mesocrystal; Micro X ray; Mollusca; PEEM; PIC mapping; Tablet; XANES

Indexed keywords

CALCIUM CARBONATE;

ABALONE; ANIMAL SHELL; ARTICLE; ATRINA RIGIDA; BIVALVE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; HALIOTIS DISCUS; HALIOTIS IRIS; HALIOTIS LAEVIGATA; HALIOTIS PULCHERRIMA; HALIOTIS RUBRA; HALIOTIS RUFESCENS; IMAGING AND DISPLAY; LASMIGONA COMPLANATA; MOLLUSC; MYTILUS; MYTILUS CALIFORNIANUS; MYTILUS EDULIS; MYTILUS GALLOPROVINCIALIS; NACRE; NAUTILUS; NAUTILUS POMPILIUS; NONHUMAN; PINCTADA; PINCTADA FUCATA; PINCTADA MARGARITIFERA; POLARIZATION DEPENDENT IMAGING CONTRAST MAPPING; PRIORITY JOURNAL; PYGANODON GRANDIS; SPECIES DIFFERENCE; TILTING;

MOLLUSCA;

ARAGONITE; BIOMINERAL; BRIDGE TILTING; DIFFRACTION; EPITAXIAL; EPITAXY; LOW-ANGLE GRAIN BOUNDARY; MESOCRYSTAL; MICRO-X-RAY; MOLLUSCA; PEEM; PIC-MAPPING; TABLET; XANES;

ANIMAL SHELLS; ANIMALS; FINITE ELEMENT ANALYSIS; IMAGE PROCESSING, COMPUTER-ASSISTED; MOLLUSCA; NACRE; PHOTOELECTRON SPECTROSCOPY;

EID: 84888060354     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2013.10.002     Document Type: Article

References (82)

1. Addadi L., Weiner S. Interactions between acidic proteins and crystals: stereochemical requirements in biomineralization. Proc. Natl. Acad. Sci. USA 1985, 82:4110-4114.
2. Addadi L., Weiner S. Biomineralization: a pavement of pearl. Nature 1997, 389:912-915.
3. Addadi L., Joester D., Nudelman F., Weiner S. Mollusk shell formation: a source of new concepts for understanding biomineralization processes. Chem. Eur. J. 2006, 12:980-987.
4. Amini S., Miserez A. Wear and abrasion resistance selection maps of biological materials. Acta Biomater. 2013, 9:7895-7907.
5. Anderson T.L. Fracture Mechanics: Fundamentals and Applications 2005, CRC Press. third ed.
6. Belcher A.M., Wu X.H., Christensen R.J., Hansma P.K., Stucky G.D., et al. Control of crystal phase switching and orientation by soluble mollusc-shell proteins. Nature 1996, 381:56-58.
7. Bevelander G., Nakahara H. An electron microscope study of the formation of the nacreous layer in the shell of certain bivalve molluscs. Calcif. Tissue Res. 1969, 3:84-92.
8. Bonderer L.J., Studart A.R., Gauckler L.J. Bioinspired design and assembly of platelet reinforced polymer films. Science 2008, 319:1069-1073.
9. Cartwright J.H.E., Checa A.G., Escribano B., Sainz-Diaz C.I. Spiral and target patterns in bivalve nacre manifest a natural excitable medium from layer growth of a biological liquid crystal. Proc. Natl. Acad. Sci. USA 2009, 106:10499-10504.
10. Checa A.G., Rodriguez-Navarro A.B. Geometrical and crystallographic constraints determine the self-organization of shell microstructures in Unionidae (Bivalvia: Mollusca). Proc. R. Soc. Lond. Ser. B Biol. Sci. 2001, 268:771-778.
11. Checa A.G., Rodriguez-Navarro A.B. Self-organisation of nacre in the shells of Pterioida (Bivalvia: Mollusca). Biomaterials 2005, 26:1071-1079.
12. Checa A.G., Rodriguez-Navarro A.B., Esteban-Delgado F.J. The nature and formation of calcitic columnar prismatic shell layers in pteriomorphian bivalves. Biomaterials 2005, 26:6404-6414.
13. Checa A.G., Okamoto T., Ramirez J. Organization pattern of nacre in Pteriidae (Bivalvia: Mollusca) explained by crystal competition. Proc. R. Soc. B Biol. Sci. 2006, 273:1329-1337.
14. Checa A.G., Cartwright J.H.E., Willinger M.G. Mineral bridges in nacre. J. Struct. Biol. 2011, 176:330-339.
15. Checa A.G., Esteban-Delgado F.J., Ramirez-Rico J., Rodriguez-Navarro A.B. Crystallographic reorganization of the calcitic prismatic layer of oysters. J. Struct. Biol. 2009, 167:261-270.
16. Checa A.G., Bonarski J.T., Willinger M.G., Faryna M., Berent K., et al. Crystallographic orientation inhomogeneity and crystal splitting in biogenic calcite. J. R. Soc. Interface 2013, 10.
17. Crenshaw M.A. Inorganic composition of molluscan extrapallial fluid. Biol. Bull. 1972, 143:506-512.
18. Dalbeck P., England J., Cusack M., Lee M.R., Fallick A.E. Crystallography and chemistry of the calcium carbonate polymorph switch in M. edulis shells. Eur. J. Mineral. 2006, 18:601-609.
19. De Stasio G., Koranda S.F., Tonner B.P., Harp G.R., Mercanti D., et al. X-ray secondary-emission microscopy (XSEM) of neurons. Europhys. Lett. 1992, 19:655-659.
20. De Stasio G., Hardcastle S., Koranda S.F., Tonner B.P., Mercanti D., et al. Photoemission spectromicroscopy of neurons. Phys. Rev. E 1993, 47:2117-2121.
21. De Stasio G., Dunham D., Tonner B.P., Mercanti D., Ciotti M.T., et al. Aluminum in rat cerebellar neural cultures. Neuroreport 1993, 4:1175-1178.
22. De Stasio G., Perfetti P., Oddo N., Galli P., Mercanti D., et al. Metal uptake in neuron cultures - a systematic study. Neuroreport 1992, 3:965-968.
23. DiMasi E., Sarikaya M. Synchrotron X-ray microbeam diffraction from abalone shell. J. Mater. Res. 2004, 19:1471-1476.
24. Falini G., Albeck S., Weiner S., Addadi L. Control of aragonite or calcite polymorphism by mollusk shell macromolecules. Science 1996, 271:67-69.
25. Freer A., Greenwood D., Chung P., Pannell C.L., Cusack M. Aragonite prism, àí nacre interface in freshwater mussels Anodonta anatina (Linnaeus, 1758) and Anodonta cygnea (L. 1758). Cryst. Growth Des. 2009, 10:344-347.
26. Fritz M., Belcher A.M., Radmacher M., Walters D.A., Hansma P.K., et al. Flat pearls from biofabrication of organized composites on inorganic substrates. Nature 1994, 371:49-51.
27. Gilbert B., Frazer B.H., Naab F., Fournelle J., Valley J.W., et al. X-ray absorption spectroscopy of silicates for in situ, sub-micrometer mineral identification. Am. Mineral. 2003, 88:763-769.
28. Gilbert P.U.P.A. Polarization-dependent imaging contrast (PIC) mapping reveals nanocrystal orientation patterns in carbonate biominerals. Journal of Electron Spectroscopy and Related Phenomena, Special Issue on Photoelectron Microscopy, Time-Resolved Pump-Probe PES 2012, 395-405. Elsevier. M. Kiskinova, A. Scholl (Eds.).
29. Gilbert P.U.P.A. Photoemission spectromicroscopy for the biomineralogist. Biomineralization Handbook, Characterization of Biominerals and Biomimetic Materials 2014, Taylor & Francis, Boca Raton, FL. E. DiMasi, L.B. Gower (Eds.).
30. 3) nanocrystals using X-ray absorption spectroscopy. Proc. Natl. Acad. Sci. USA 2011, 108:11350-11355.
31. Gilbert P.U.P.A., Metzler R.A., Zhou D., Scholl A., Doran A., et al. Gradual ordering in red abalone nacre. J. Am. Chem. Soc. 2008, 130:17519-17527.
32. Gong Y.U.T., Killian C.E., Olson I.C., Appathurai N.P., Amasino A.L., et al. Phase transitions in biogenic amorphous calcium carbonate. Proc. Natl. Acad. Sci. USA 2012, 109:6088-6093.
33. Gries K., Kröger R., Kübel C., Schowalter M., Fritz M., et al. Correlation of the orientation of stacked aragonite platelets in nacre and their connection via mineral bridges. Ultramicroscopy 2009, 109:230-236.
34. Johnson C.L., Høtch M.J., Buseck P.R. Nanoscale waviness of low-angle grain boundaries. Proc. Natl. Acad. Sci. USA 2004, 101:17936-17939.
35. Keene E.C., Evans J.S., Estroff L.A. Silk fibroin hydrogels coupled with the n16N-beta-chitin complex an in vitro organic matrix for controlling calcium carbonate mineralization. Cryst. Growth Des. 2010, 10:5169-5175.
36. Killian C.E., Metzler R.A., Gong Y.T., Olson I.C., Aizenberg J., et al. The mechanism of calcite co-orientation in the sea urchin tooth. J. Am. Chem. Soc. 2009, 131:18404-18409.
37. Killian C.E., Metzler R.A., Gong Y.U.T., Churchill T.H., Olson I.C., et al. Self-sharpening mechanism of the sea urchin tooth. Adv. Funct. Mater. 2011, 21:682-690.
38. Kobayashi S., Tsurekawa S., Watanabe T. Grain boundary hardening and triple junction hardening in polycrystalline molybdenum. Acta Mater. 2005, 53:1051-1057.
39. Levi-Kalisman Y., Falini G., Addadi L., Weiner S. Structure of the nacreous organic matrix of a bivalve mollusk shell examined in the hydrated state using cryo-TEM. J. Struct. Biol. 2001, 135:8-17.
40. MacDonald J., Freer A., Cusack M. Alignment of crystallographic c-axis throughout the four distinct microstructural layers of the oyster Crassostrea gigas. Cryst. Growth Des. 2010, 10:1243-1246.
41. Marie B., Joubert C., Tayale A., Zanella-Cleon I., Belliard C. Different secretory repertoires control the biomineralization processes of prism and nacre deposition of the pearl oyster shell. Proc. Natl. Acad. Sci. USA 2012, 109:20986-20991.
42. Metzler R.A., Abrecht M., Olabisi R.M., Ariosa D., Johnson C.J., et al. Architecture of columnar nacre, and implications for its formation mechanism. Phys. Rev. Lett. 2007, 98:268102.
43. Metzler R.A., Zhou D., Abrecht M., Chiou J.-W., Guo J., et al. Polarization-dependent imaging contrast in abalone shells. Phys. Rev. B 2008, 77:666.
44. Metzler R.A., Zhou D., Abrecht M., Chiou J.W., Guo J.H., et al. Polarization-dependent imaging contrast in abalone shells. Phys. Rev. B 2008, 77. 064110-064111/064119.
45. Metzler R.A., Evans J.S., Killian C.E., Zhou D., Churchill T.H., et al. Nacre protein fragment templates lamellar aragonite growth. J. Am. Chem. Soc. 2010, 132:6329-6334.
46. Meyers M.A., McKittrick J., Chen P.-Y. Structural biological materials: critical mechanics-materials connections. Science 2013, 339:773-779.
47. Ming N.B., Wang M., Peng R.W. Nucleation-limited aggregation in fractal growth. Phys. Rev. E 1993, 48:621-624.
48. Munch E., Launey M.E., Alsem D.H., Saiz E., Tomsia A.P., et al. Tough, bio-inspired hybrid materials. Science 2008, 322:1516-1520.
49. Mutvei H. Ultrastructural relationships between the prismatic and nacreous layers in Nautilus (Cephalopoda). Biomin. Res. Rep. 1972, 4:81-86.
50. Mutvei H. On the internal structures of the nacreous tablets in molluscan shells. Scanning Electron Microsc. 1979, II:451-462.
51. Nakahara H. An electron microscope study of the growing surface of nacre in two gastropod species, Turbo cornutus and Tegula pfeifferi. Venus 1979, 38:205-211.
52. Nassif N., Pinna N., Gehrke N., Antonietti M., Jager C., et al. Amorphous layer around aragonite platelets in nacre. Proc. Natl. Acad. Sci. USA 2005, 102:12653-12655.
53. Nudelman F., Gotliv B.A., Addadi L., Weiner S. Mollusk shell formation: mapping the distribution of organic matrix components underlying a single aragonitic tablet in nacre. J. Struct. Biol. 2006, 153:176-187.
54. Nys Y., Gautron J., Garcia-Ruiz J.M., Hincke M.T. Avian eggshell mineralization: biochemical and functional characterization of matrix proteins. C.R. Palevol 2004, 3:549-562.
55. Olson I.C., Kozdon R.H., Valley J.W., Gilbert P.U.P.A. Mollusk shell nacre ultrastructure correlates with environmental temperature and pressure. J. Am. Chem. Soc. 2012, 134:7351-7358.
56. Olson I.C., Metzler R.A., Tamura N., Kunz M., Killian C.E., et al. Crystal lattice tilting in prismatic calcite. J. Struct. Biol. 2013, 183:180-190.
57. Ortiz C., Boyce M.C. Bioinspired structural materials. Science 2008, 319:1053-1054.
58. Perez-Huerta A., Dauphin Y., Cuif J.-P., Cusack M. High resolution electron backscatter diffraction (EBSD) data from calcite biominerals in recent gastropod shells. Micron 2011, 42:246-251.
59. Pokroy B., Zolotoyabko E. Microstructure of natural plywood-like ceramics: a study by high-resolution electron microscopy and energy-variable X-ray diffraction. J. Mater. Chem. 2003, 13:682-688.
60. Pokroy B., Zolotoyabko E. Aragonite growth on single-crystal substrates displaying a threefold axis. Chem. Commun. 2005, 2140-2142.
61. 3). Cryst. Growth Des. 2007, 7:1580-1583.
62. Pokroy B., Fieramosca J.S., Von Dreele R.B., Fitch A.N., Caspi E.N., et al. Atomic structure of biogenic aragonite. Chem. Mater. 2007, 19:3244-3251.
63. Rousseau M., Lopez E., Stempfle P., Brendle M., Franke L., et al. Multiscale structure of sheet nacre. Biomaterials 2005, 26:6254-6262.
64. Schäffer T.E., Ionescu-Zanetti C., Proksch R., Fritz M., Walters D.A., et al. Does abalone nacre form by heteroepitaxial nucleation or by growth through mineral bridges?. Chem. Mater. 1997, 9:1731-1740.
65. Schmahl W.W., Griesshaber E., Kelm K., Goetz A., Jordan G., et al. Hierarchical structure of marine shell biomaterials: biomechanical functionalization of calcite by brachiopods. Z. Fur Kristallogr. 2012, 227:793-804.
66. Schneider A., Heiland B., Peter N., Guth C., Arzt E., et al. Hierarchical super-structure identified by polarized light microscopy, electron microscopy and nanoindentation: implications for the limits of biological control over the growth mode of abalone sea shells. BMC Biophys. 2012, 5:19.
67. Su X., Belcher A.M., Zaremba C.M., Morse D.E., Stucky G.D., et al. Structural and microstructural characterization of the growth lines and prismatic microarchitecture in red abalone shell and the microstructures of abalone "flat pearls". Chem. Mater. 2002, 14:3106-3117.
68. Suzuki M., Saruwatari K., Kogure T., Yamamoto Y., Nishimura T., et al. An acidic matrix protein, pif, is a key macromolecule for nacre formation. Science 2009, 325:1388-1390.
69. Tamura N., Gilbert P.U.P.A. X-ray microdiffraction of biominerals. Research Methods in Biomineralization Science 2013, Elsevier, Oxford. J.J. De Yoreo (Ed.).
70. Tamura N., MacDowell A.A., Spolenak R., Valek B.C., Bravman J.C., et al. Scanning X-ray microdiffraction with submicrometer white beam for strain/stress and orientation mapping in thin films. J. Synch. Radiat. 2003, 10:137-143.
71. Ubukata T. Architectural constraints on the morphogenesis of prismatic structure in Bivalvia. Palaeontology 1994, 37:241-262.
72. Wada K. Nucleation and growth of aragonite crystals in the nacre of some bivalve molluscs. Biomineralisation 1972, 6:141-159.
73. Wang M., Liu X.Y., Strom C.S., Bennema P., van Enckevort W., et al. Fractal aggregations at low driving force with strong anisotropy. Phys. Rev. Lett. 1998, 80:3089-3092.
74. Wang M., Zhong S., Yin X.B., Zhu J.M., Peng R.W., et al. Nanostructured copper filaments in electrochemical deposition. Phys. Rev. Lett. 2001, 86:3827-3830.
75. Weiner S., Hood L. Soluble protein of the organic matrix of mollusk shells: a potential template for shell formation. Science 1975, 190:987-989.
76. Weiner S., Traub W. X-ray diffraction study of the insoluble organic matrix of mollusk shells. FEBS Lett. 1980, 111:311-316.
77. Weiner S., Lowenstam H. Organization of extracellularly mineralized tissues: a comparative study of biological crystal growth. Crit. Rev. Biochem. Mol. Biol. 1986, 20:365-408.
78. Weiner S., Traub W., Parker S.B. Macromolecules in mollusc shells and their functions in biomineralization [and Discussion]. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1984, 304:425-434.
79. Wise S.W. Microarchitecture and deposition of gastropod nacre. Science 1970, 167:1486-1488.
80. Younis S., Kauffmann Y., Bloch L., Zolotoyabko E. Inhomogeneity of nacre lamellae on the nanometer length scale. Cryst. Growth Des. 2012, 12:4574-4579.
81. Zaremba C.M., Belcher A.M., Fritz M., Li Y., Mann S., et al. Critical transitions in the biofabrication of abalone shells and flat pearls. Chem. Mater. 1996, 8:679-690.
82. Zhang G.F., Fang X.D., Guo X.M., Li L., Luo R.B., et al. The oyster genome reveals stress adaptation and complexity of shell formation. Nature 2012, 490:49-54.