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	Contents


	Foreword: The Enigma of Morphogenesis -- A Personal View	VII
	Preface	XXIII
	List of Contributors	XXV
1	Growth and Form: What is the Aim of Biomineralization? Edmund Bäuerlein	1
	Abstract	1
1.1	Introduction	1
1.2	Notions of D'Arcy Thompson on Deposition of Inorganic Material in Cells	2
1.3	Close to the Beginning of Biomineralization	3
1.3.1	Prebiotic Synthesis of Peptides	3
1.3.2	Selected Binding of Phage(Virus)-Displayed Peptides to Inorganic Materials	3
1.3.3	Synthesis of Inorganic Material by Selected Peptides	3
1.3.4	Selected Sequences with Various Functional Groups	6
1.3.5	Summary and Conclusion	7
1.4	Nucleation of Inorganic Crystals and Inorganic Amorphous/Porous Forms on Peptides	7
1.4.1	Porous Silica Spheres Synthesized by 12-Amino Acid Peptides Targets	7
1.4.2	An Amorphous CaCO₃ Core and a Crystalline CaCO₃ Envelope, Separated by an Organic Layer, Coexist on an Ascidian Skeleton	8
1.4.3	The Proteomic Analysis of the Chicken Calcified Eggshell Layer	8
1.4.4	Synthesis of Nanocrystalline Hydroxyapatite with a Crystalline Core and a Disordered Surface Region	9
1.4.5	One Iron Atom in Archaeal Ferritin Crystals as Seed for an Iron-Oxide Cluster	9
1.4.6	Directional Freezing of Aqueous Ceramic Suspensions to Shape Complex Composites	9
1.4.7	Ways to Porous Structures	10
1.5	Bacterial Filaments in the Advent of Biomineralization: Cytoskeleton-Like Proteins and Exopolysaccharides	11
1.5.1	Proteins Responsible for the Alignment of Magnetosomes in Magnetotactic Bacteria	11
1.5.1.1	Actin-Like Filaments in Magnetotactic Bacteria	11
1.5.1.2	Actin Filaments in Morphogenesis of Diatoms, Eukaryotic Unicellular Organisms	12
1.5.1.3	Renaissance of the “Grand Unified Theory?”	12
1.5.2	Filaments of Bacterial Acidic Polysaccharides as Matrices for Iron Oxide Crystals	13
1.5.2.1	Bacterial Iron Oxide Precipitations	13
1.5.2.2	Bacterial Core Strands of Acidic Exopolysaccharides Template Assembly of FeOOH Nanocrystal Fibers	13
1.5.2.3	Acidic Polysaccharides Mediating Formation of Complex Calcite (CaCO₃) Crystals in Pleurochrysis carterae, a Unicellular, Eukaryotic Organism	14
1.5.2.4	Polysaccharides or Peptides: Is There a “Unified Theory”?	14
1.6	Proteins of Similar Function and/or Structure, but Low Sequence Homology: Typical in Biomineralization	15
1.6.1	The Avian Eggshell Protein Ovocleidin-17, and Human Pancreatic Stone Protein	15
1.6.2	The Starmaker Protein of Zebrafish and Human Dentin Sialophosphoprotein (DSPP)	16
1.7	Composites: Inorganic--Organic Hybrid Materials	16
1.8	Finite Element Analysis and Conclusion	18
	References	19
I	Silica-Hydrated Polysilicondioxide	21
2	Collagen: A Huge Matrix in Glass Sponge Flexible Spicules of the Meter-Long Hyalonema sieboldi Hermann Ehrlich and Hartmut Worch	23
	Abstract	23
2.1	Introduction	23
2.2	A Modern Approach to Desilicification of Spicules in Glass Sponges	25
2.3	Glass Sponge Collagen	26
2.3.1	Chemical Etching of Spicules and Extraction of Collagen	26
2.3.2	Collagen Identification	27
2.3.3	Nanoimagery of Fibrillar Organic Matrix	29
2.4	Collagen as a Unified Template for Biomineralization	30
2.4.1	Evolutionary Aspects	30
2.4.2	Twisted Plywood Architecture of Collagen Fibrils in Basal Spicules of H. sieboldi	32
2.4.3	A New View on the Possible Role of Silica in Bone Mineralization	33
2.5	Collagen--Silica-Based Biomaterials	35
2.5.1	Bioactive Glass Composites	35
2.5.2	Collagen--Silica-Based Biohybrids	36
2.6	Open Questions	37
	References	38
3	Biochemistry and Molecular Genetics of Silica Biomineralization in Diatoms Nils Kröger and Nicole Poulsen	43
	Abstract	43
3.1	Introduction	43
3.2	The Cell Biology of Diatom Silica Formation	45
3.3	Thalassiosira pseudonana as a Model Organism	47
3.3.1	Genome Analysis	47
3.3.2	Silaffins and Long-Chain Polyamines from T. pseudonana	48
3.3.2.1	Silaffins	49
3.3.2.2	LCPAs	51
3.3.3	Silica Formation by Silaffins and LCPAs	52
3.3.4	Molecular Genetic Manipulation	54
	References	57
4	Formation of Siliceous Spicules in Demosponges: Example Suberites domuncula Werner E. G. Müller, Xiaohong Wang, Sergey I. Belikov, Wolfgang Tremel, Ute Schloßmacher, Antonino Natoli, David Brandt, Alexandra Boreiko, Muhammad Nawaz Tahir, Isabel M. Müller, and Heinz C. Schröder	59
	Abstract	59
4.1	Introduction	59
4.2	Early Descriptions	63
4.3	Structural Features of the Sponge Body Plan	64
4.4	Cells Involved in Spicule Formation	65
4.5	Anabolic Enzyme for the Synthesis of Silica: Silicatein	67
4.6	Silicatein-Associated Proteins	72
4.7	Catabolic Enzyme: Silicase	73
4.8	Morphology and Synthesis of Spicules in S. domuncula	73
4.9	Formation of Spicule Morphology	74
4.10	Phases of Silica Deposition during Spicule Formation	76
4.10.1	The Intracellular Phase in the Sclerocytes	76
4.10.2	The Extracellular Phase: Appositional Growth	76
4.10.3	The Extracellular Phase: Shaping	78
4.11	Final Remarks	79
	References	80
5	Interactions between Biomineralization and Function of Diatom Frustules Christian Hamm	83
	Abstract	83
5.1	Introduction	83
5.2	Approaches to Study Biominerals	85
5.3	Evolution and Diatom Shells	89
5.4	Biomechanics and Diatoms	90
5.5	The Effect of Evolutionary Feedback on Biomineralization	91
5.6	Conclusions	92
	References	93
6	The Evolution of the Diatoms Wiebe H. C. F. Kooistra	95
	Abstract	95
6.1	Introduction	95
6.2	The Silica Cell Walls of the Diatoms	96
6.2.1	The Frustule	96
6.2.2	Frustule Construction	99
6.2.3	Sexual Reproduction and Auxospore Formation	100
6.2.4	Resting Stages	102
6.3	Phylogenies	102
6.3.1	The Heterokont Relatives of the Diatoms	102
6.3.2	The Phylogeny of the Diatoms	103
6.4	The Diatom Fossil Record	105
6.5	The Origin and Evolution of the Diatom Frustule	107
6.6	Paleo-Ecology and Diatom Evolution	108
	References	109
7	Uptake of Silicon in Different Plant Species Jian Feng Ma	113
	Abstract	113
7.1	Silicon in Plants	113
7.2	Beneficial Effects of Silicon on Plant Growth	115
7.2.1	Disease Control	115
7.2.2	Alleviation of Stress	115
7.2.3	Plant Growth	116
7.3	Uptake Systems of Si in Different Plant Species	116
7.4	Genes Involved in Si Uptake	120
	References	123
II	Iron Sulfides and Oxides	125
8	Magnetic Microstructure of Magnetotactic Bacteria Richard B. Frankel, Rafal E. Dunin-Borkowski, Mihály Pósfai, and Dennis A. Bazylinski	127
	Abstract	127
8.1	Introduction	127
8.1.1	Magnetotactic Bacteria	127
8.1.2	Magnetosomes	128
8.1.3	Magnetite Magnetosomes	129
8.1.4	Greigite Magnetosomes	131
8.1.5	Magnetic Properties of Magnetosomes	132
8.1.6	Cellular Magnetic Dipole	133
8.2	Experimental Measurements of the Magnetic Microstructure of Magnetosomes	133
8.2.1	Off-Axis Electron Holography: An Overview	134
8.2.2	Off-Axis Electron Holography of Magnetite Magnetosome Chains	135
8.2.3	Off-Axis Electron Holography of Greigite Magnetosome Chains	138
8.3	Conclusions	141
	References	142
9	Genetic and Biochemical Analysis of Magnetosome Formation in Magnetospirillum gryphiswaldense Christian Jogler and Dirk Schüler	145
	Abstract	145
9.1	Introduction	145
9.2	Genetics of Magnetosome Formation	146
9.2.1	Genomic Organization of Magnetosome Genes	146
9.2.2	Genes Encoding Magnetosome-Associated Proteins are Co-Transcribed within the mam- and mms-Operons	150
9.2.3	The Magnetosome Island is a Highly Unstable Genomic Region and Undergoes Spontaneous Rearrangements	150
9.3	Magnetosome-Associated Proteins	151
9.3.1	Biochemical Characterization of the Magnetosome Membrane	151
9.3.1.1	TPR Proteins (MamA)	153
9.3.1.2	CDF Proteins	153
9.3.1.3	HtrA-like Serine Proteases	156
9.3.1.4	MMPs with Unknown Function	156
9.3.2	MamJ and MamK Control Subcellular Organization and Assembly of Magnetosomes Chains	157
9.4	Mechanism of Magnetosome Formation and Magnetite Biomineralization	158
	References	160
10	Physical and Chemical Principles of Magnetosensation in Biology Michael Winklhofer and Thorsten Ritz	163
	Abstract	163
10.1	Introduction	163
10.2	A Biochemical Compass Mechanism	164
10.2.1	Magnetic Field Effects on Radical-Pair Reactions	164
10.2.2	A Hypothetical Radical-Pair Based Compass	165
10.2.3	Evidence for a Radical-Pair Mechanism in Migratory Birds	166
10.3	Biogenic Magnetite as a Basis of Magnetoreception	167
10.3.1	Pitfalls with the Magnetite Hypothesis	168
10.3.2	Magnetite-Based Magnetoreceptors	169
10.3.3	Hypothetical Transduction Mechanisms	171
10.3.4	Testing the Magnetite Hypothesis with Pulse Experiments	172
10.3.5	Biomineralization of Magnetite in Vertebrates	173
10.3.6	Non-Destructive Techniques Used to Detect Magnetite in Tissue	174
10.3.6.1	SQUID Measurements	174
10.3.6.2	X-Ray Fluorescence (XRF) and X-Ray Absorption Spectroscopy (XAS)	175
10.3.6.3	Ferromagnetic Resonance (FMR) Spectroscopy	175
10.3.6.4	Nuclear Magnetic Resonance (NMR) Relaxometry	176
10.4	Conclusions	176
	References	177
III	Calcium Carbonates and Sulfates	181
11	The Morphogenesis and Biomineralization of the Sea Urchin Larval Skeleton Fred H. Wilt and Charles A. Ettensohn	183
	Abstract	183
11.1	Introduction	183
11.2	Developmental Aspects of Sea Urchin Biomineralization	184
11.2.1	A General Description of Skeletogenesis	184
11.2.2	PMC Specification	189
11.2.2.1	Embryological Studies	189
11.2.2.2	The Micromere-PMC Gene Regulatory Network	189
11.2.3	Regulation of Skeletal Patterning in the Embryo	190
11.2.4	Cell Interactions and Skeletogenesis	192
11.2.4.1	Cell Interactions and PMC Specification	192
11.2.4.2	Cell Interactions and Skeletal Morphogenesis	192
11.3	The Composition and Formation of the Skeletal Spicule	194
11.3.1	Sources of Calcium, its Precipitation, and Secretion	194
11.3.2	The Spicule Compartment	195
11.3.3	Growth of the Spicule	196
11.3.4	Integral Matrix Proteins of the Spicule	197
11.3.5	Mineral--Matrix Relationships	200
11.3.6	Functions of Matrix Proteins	202
11.3.7	Adult Mineralized Structures	202
11.3.8	Function of Non-Matrix Proteins	204
11.4	Generalizations about Biomineralization of Calcium Carbonates	205
	References	207
12	Regulation of Coccolith Calcification in Pleurochrysis carterae Mary E. Marsh	211
	Abstract	211
12.1	Introduction	211
12.2	Pleurochrysis Coccolith Structure	213
12.3	Pleurochrysis Coccolith Formation	214
12.3.1	Ion Accumulation	215
12.3.2	Calcite Nucleation	217
12.3.3	Crystal Growth	218
12.3.4	Growth Termination	219
12.4	Identifying Other Regulatory Elements in Coccolith Mineralization	219
12.5	*The Non-Mineralizing Phases of Pleurochrysis* and Other Coccolithophores**	221
12.6	Coccolith Calcification and the Ocean Carbon Cycle	223
	References	224
13	Molecular Approaches to Emiliana huxleyi Coccolith Formation Betsy A. Read and Thomas M. Wahlund	227
	Abstract	227
13.1	Introduction	227
13.2	Cellular Physiology of Biomineralization	228
13.3	Traditional Biochemical Approaches	229
13.4	Genomics	231
13.5	Functional Genomics	232
13.5.1	Suppressive Subtractive Hybridization	233
13.5.2	Microarray	234
13.5.3	Real-Time RT-PCR	235
13.6	Future Directions and Approaches	239
	References	240
14	Organic Matrix and Biomineralization of Scleractinian Corals Sylvie Tambutté, Eric Tambutté, Didier Zoccola, and Denis Allemand	243
	Abstract	243
14.1	Introduction	243
14.2	Coral Anatomy and Histology	245
14.3	The Proportion of the Organic Matrix in the Skeleton	247
14.4	The Relationship between the Organic Matrix and Calcification	248
14.5	The Composition of the Organic Matrix	249
14.6	Localization of Organic Matrix Synthesis	249
14.7	The Role of Zooxanthellae and Heterotrophic Feeding in Organic Matrix Synthesis	251
14.8	Characterization of Organic Matrix Proteins	252
14.9	Comparative Studies between Organic Matrix Proteins from Different Organisms	253
14.10	Organic Matrix and Skeleton Microarchitecture	254
14.11	Organic Matrix and Its Implications for Paleo-/Geo-Chemistry and Diagenesis	255
14.12	Conclusions	256
	References	257
15	Statoliths of Calcium Sulfate Hemihydrate are used for Gravity Sensing in Rhopaliophoran Medusae (Cnidaria) Fabienne Boßelmann, Matthias Epple, Ilka Sötje, and Henry Tiemann	261
	Abstract	261
15.1	Diversity of Alkaline Earth Sulfates in Organisms and Nature	261
15.2	Morphology of Rhopalia, Statoliths, and their Function	262
15.3	Examination of Statoliths	264
15.4	Formation and Growth of Statoliths	266
15.5	Occurrence of Calcium Sulfate Hemihydrate in the Different Taxa with Phylogenetic Aspects	269
	References	271
16	Unusually Acidic Proteins in Biomineralization Frédéric Marin and Gilles Luquet	273
	Abstract	273
16.1	Introduction: Unusually Acidic Proteins and the History of their Discovery	273
16.2	What Makes a Protein Unusually Acidic?	275
16.3	Biochemical Techniques for Studying Unusually Acidic Proteins	277
16.4	Interactions of Acidic Proteins with Calcium Carbonate Crystals and Organo-Mineral Models	279
16.5	Occurrence of Unusually Acidic Proteins in Selected Metazoan CaCO₃-Mineralizing Phyla	282
16.6	Concluding Remarks	285
	References	286
17	Fish Otolith Calcification in Relation to Endolymph Chemistry Denis Allemand, Nicole Mayer-Gostan, Hélène de Pontual, Gilles Boeuf, and Patrick Payan	291
	Abstract	291
17.1	Introduction	291
17.2	Basic Calcification Principles as Applied to Fish Otoliths	293
17.2.1	Basic Equations	293
17.2.2	Difference between a Chemical Crystal and a Biocrystal	293
17.2.3	The Players Involved in Calcification	295
17.2.4	The Case of Fish Otoliths	296
17.3	The Fish Endolymph: a Complex Heterogeneous Medium	296
17.3.1	The Standard View	296
17.3.2	Spatial Heterogeneity of Endolymph Composition	297
17.3.3	Complexity of the Saccular Epithelium	298
17.3.4	Dynamics of the Components of the Endolymph	299
17.4	Are Levels of Calcifying Parameters in Endolymph Associated with Otolith Growth?	300
17.4.1	The Nychthemeral Cycle	300
17.4.1.1	Plasma Calcium Levels	300
17.4.1.2	Incorporation of Precursors in the Otolith	300
17.4.1.3	Acid--Base Balance	300
17.4.1.4	Organic Compounds	301
17.4.2	Environmental Factors	301
17.4.3	Conclusion	302
17.5	Questions and Future Research Directions	302
17.5.1	Daily Variations in Endolymph Protein Concentrations	302
17.5.2	[Ca²⁺] and [HCO₃^-] in the Endolymph	302
17.5.3	Physico-Chemical Originalities of the Distal Endolymph	303
17.5.4	Difficulties in the Analysis of the OM	304
17.5.5	Weak Analogy between the Organic Components of OM and Endolymph	305
17.5.6	Comparative Study of the OM of Carbonated Biominerals	306
17.5.7	Organic Chemistry of the Endolymph	306
	References	307
18	Eggshell Growth and Matrix Macromolecules José Luis Arias, Karlheinz Mann, Yves Nys, Juan Manuel Garcia Ruiz, and Maria Soledad Fernández	309
	Abstract	309
18.1	Introduction	309
18.2	Eggshell Structure and Formation	310
18.3	Crystalline Structure of the Eggshell	311
18.4	Eggshell Organic Matrix Components and Their Localization	312
18.5	The Unique Eggshell Organic Components	314
18.5.1	Ovoglycan and Ovocleidin-116	314
18.5.2	C-Type Lectin-Like Proteins of the Avian Eggshell	314
18.5.3	Ovocalyxins	319
18.6	A Proteomic Inventory of the Chicken Calcified Eggshell Matrix	319
18.7	Role of the Organic Components in Eggshell Mineralization	323
	References	324
IV	Calcium Phosphates	329
19	Genetic Basis for the Evolution of Vertebrate Mineralized Tissue Kazuhiko Kawasaki and Kenneth M. Weiss	331
	Abstract	331
19.1	Introduction	331
19.2	Dental Tissue Mineralization	332
19.3	Matrix Proteins of Dental Tissues	333
19.4	Mammalian SCPP Genes	334
19.5	Chicken and Frog SCPP Genes	339
19.6	Teleost SCPP Genes	340
19.7	The Origin of the SCPP Family	341
19.8	The Function of SCPPs and Intrinsic Disorder	342
19.9	Conclusions	343
	References	344
20	Skeletogenesis in Zebrafish Embryos (Danio rerio) Shao-Jun Du	349
	Abstract	349
20.1	Introduction	349
20.2	Craniofacial Skeleton	350
20.2.1	Anatomy and Development of Zebrafish Craniofacial Skeleton	350
20.2.2	Molecular Regulation of Craniofacial Skeleton Development and Patterning	352
20.2.3	Mutational Analyses of Craniofacial Skeletons	353
20.3	The Axial Skeleton	354
20.3.1	Anatomy and Development of the Axial Skeleton	354
20.3.2	Development of the Intervertebral Disc	356
20.3.3	The Notochord Plays Key Roles in Vertebral Column Development	358
20.3.4	Retinoic Acid and Hedgehog are Involved in Notochord Segmentation and IVD Formation	358
20.3.5	Genetic Screening for Vertebral Mutants	360
20.4	Fin Skeleton	361
20.4.1	Development of Median Fins	361
20.4.2	Development of Paired Fins	361
20.4.3	Molecular Regulation of Fin Formation and Growth	362
20.5	Summary	363
	References	364
21	The Application of Synchrotron Radiation-Based Micro-Computer Tomography in Biomineralization Frank Neues, Felix Beckmann, Andreas Ziegler, and Matthias Epple	369
	Abstract	369
21.1	Synchrotron Radiation-Based Micro-Computer Tomography (SR CT)	369
21.2	*SR CT applied to Bones and Teeth of the Zebrafish (Danio rerio)*	371
21.2.1	Overview of the Skeleton	372
21.2.2	The Teeth	372
21.2.3	The Vertebral Column	374
21.3	SR CT applied to the Cuticle of P. scaber	375
21.3.1	Overview of the Mineralized Exoskeleton	375
21.3.2	Molting and Sternal Deposits	376
21.4	Summary	378
	References	379
22	Mechanical and Structural Properties of Skeletal Bone in Wild-Type and Mutant Zebrafish (Danio rerio) Fuzhai Cui and Xiumei Wang	381
	Abstract	381
22.1	Introduction	381
22.2	The Potential of Zebrafish as a Model for Bone Mineralization	382
22.2.1	Hierarchical Structures of Zebrafish Skeleton Bone	382
22.2.2	Microstructural Characteristics and Nanomechanical Properties across the Thickness of Zebrafish Skeletal Bone	383
22.2.3	Surface Mineralization of Collagen Fibrils in Zebrafish Skeleton Bone	386
22.2.4	Conclusion	390
22.3	*Hierarchical Structural Comparisons of Bones from Wild-Type and liliput^dtc232 (lil)* Gene-Mutated Zebrafish**	390
22.3.1	Alteration of Vertebrae Development	390
22.3.2	Fracture Topography and Fibrils Array Patterns	390
22.3.3	Mineralized Collagen Fibrils	391
22.3.4	Type I Collagen Fibrils	391
22.3.5	The Hydoxyapatite Minerals	391
22.4	Variation of Nanomechanical Properties of Bone by Gene Mutation in the Zebrafish	392
22.5	Conclusion	395
	References	395
23	Nanoscale Mechanisms of Bone Deformation and Fracture Peter Fratzl and Himadri S. Gupta	397
	Abstract	397
23.1	The Hierarchical Structure of Bone	397
23.2	Structural Design of Bone at the Nanoscale	400
23.3	The Lamellar Organization of Bone	404
23.4	Bone Deformation at the Nanoscale	408
	References	412
24	Formation and Structure of Calciprotein Particles: The Calcium Phosphate--Ahsg/Fetuin-A Interface Alexander Heiss and Dietmar Schwahn	415
	Abstract	415
24.1	The Protein--Mineral Interface	415
24.1.1	Mineral Formation	415
24.1.2	Fetuin-A	418
24.2	Small-Angle Neutron-Scattering Studies	419
24.2.1	Instrumental Set-Up	419
24.2.2	Theoretical Background	420
24.3	Calciprotein Particle Formation and Transformation	422
24.3.1	Fetuin-A	422
24.3.2	Inhibition of Mineral Sedimentation Effected by the Serum Proteins Fetuin-A and Albumin	423
24.3.3	Calciprotein Particle Formation	424
24.3.4	CPP Structure	426
24.4	Conclusions	428
	References	430
	Index	433

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