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Biophysical Reviews

, Volume 8, Issue 4, pp 309–329 | Cite as

Mineralization and non-ideality: on nature’s foundry

  • Ashit RaoEmail author
  • Helmut CölfenEmail author
Review

Abstract

Understanding how ions, ion-clusters and particles behave in non-ideal environments is a fundamental question concerning planetary to atomic scales. For biomineralization phenomena wherein diverse inorganic and organic ingredients are present in biological media, attributing biomaterial composition and structure to the chemistry of singular additives may not provide a holistic view of the underlying mechanisms. Therefore, in this review, we specifically address the consequences of physico-chemical non-ideality on mineral formation. Influences of different forms of non-ideality such as macromolecular crowding, confinement and liquid-like organic phases on mineral nucleation and crystallization in biological environments are presented. Novel prospects for the additive-controlled nucleation and crystallization are accessible from this biophysical view. In this manner, we show that non-ideal conditions significantly affect the form, structure and composition of biogenic and biomimetic minerals.

Keywords

Biomineralization Crystallization Liquid phase Molecular crowding Non-ideality Nucleation 

Notes

Acknowledgment

AR thanks the Freiburg Institute for Advanced Studies for its kind support.

Compliance with ethical standards

Conflict of interests

Ashit Rao declares that he has no conflicts of interest. Helmut Cölfen declares that he has no conflicts of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

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References

  1. Addadi L, Raz S, Weiner S (2003) Taking advantage of disorder: amorphous calcium carbonate and its roles in biomineralization. Adv Mater 15:959–970CrossRefGoogle Scholar
  2. Arakawa T, Timasheff SN (1985) Mechanism of polyethylene glycol interaction with proteins. Biochemistry 24:6756–6762PubMedCrossRefGoogle Scholar
  3. Arias JL, Fernández MAS (2008) Polysaccharides and proteoglycans in calcium carbonate-based biomineralization. Chem Rev 108:4475–4482PubMedCrossRefGoogle Scholar
  4. Behera RK, Theil EC (2014) Moving Fe2+ from ferritin ion channels to catalytic OH centers depends on conserved protein cage carboxylates. Proc Natl Acad Sci U S A 111:7925–7930PubMedPubMedCentralCrossRefGoogle Scholar
  5. Beinert H, Holm RH, Münck E (1997) Iron-sulfur clusters: nature’s modular, multipurpose structures. Science 277:653–659PubMedCrossRefGoogle Scholar
  6. Bentov S, Weil S, Glazer L, Sagi A, Berman A (2010) Stabilization of amorphous calcium carbonate by phosphate rich organic matrix proteins and by single phosphoamino acids. J Struct Biol 171:207–215PubMedCrossRefGoogle Scholar
  7. Berg JK, Jordan T, Binder Y, Börner HG, Gebauer D (2013) Mg2+ tunes the wettability of liquid precursors of CaCO3: toward controlling mineralization sites in hybrid materials. J Am Chem Soc 135:12512–12515PubMedCrossRefGoogle Scholar
  8. Bertinetti L, Masic A, Schuetz R, Barbetta A, Seidt B, Wagermaier W, Fratzl P (2015) Osmotically driven tensile stress in collagen-based mineralized tissues. J Mech Behav Biomed Mater 52:14–21PubMedCrossRefGoogle Scholar
  9. Bewernitz MA, Gebauer D, Long J, Cölfen H, Gower LB (2012) A metastable liquid precursor phase of calcium carbonate and its interactions with polyaspartate. Faraday Discuss 159:291–312CrossRefGoogle Scholar
  10. Bolen D (2004) Effects of naturally occurring osmolytes on protein stability and solubility: issues important in protein crystallization. Methods 34:312–322PubMedCrossRefGoogle Scholar
  11. Brangwynne CP, Eckmann CR, Courson DS, Rybarska A, Hoege C, Gharakhani J, Jülicher F, Hyman AA (2009) Germline P granules are liquid droplets that localize by controlled dissolution/condensation. Science 324:1729–1732PubMedCrossRefGoogle Scholar
  12. Brangwynne CP, Mitchison TJ, Hyman AA (2011) Active liquid-like behavior of nucleoli determines their size and shape in Xenopus laevis oocytes. Proc Natl Acad Sci U S A 108:4334–4339PubMedPubMedCentralCrossRefGoogle Scholar
  13. Brangwynne CP, Tompa P, Pappu RV (2015) Polymer physics of intracellular phase transitions. Nat Phys 11:899–904CrossRefGoogle Scholar
  14. Brubach J-B, Mermet A, Filabozzi A, Gerschel A, Lairez D, Krafft M, Roy P (2001) Dependence of water dynamics upon confinement size. J Phys Chem B 105:430–435CrossRefGoogle Scholar
  15. Brunner E, Lutz K, Sumper M (2004) Biomimetic synthesis of silica nanospheres depends on the aggregation and phase separation of polyamines in aqueous solution. Phys Chem Chem Phys 6:854–857CrossRefGoogle Scholar
  16. Butler MF, Glaser N, Weaver AC, Kirkland M, Heppenstall-Butler M (2006) Calcium carbonate crystallization in the presence of biopolymers. Cryst Growth Des 6:781–794CrossRefGoogle Scholar
  17. Cartwright JH, Checa AG, Escribano B, Sainz-Díaz CI (2009) Spiral and target patterns in bivalve nacre manifest a natural excitable medium from layer growth of a biological liquid crystal. Proc Natl Acad Sci U S A 106:10499–10504PubMedPubMedCentralCrossRefGoogle Scholar
  18. Cartwright JH, Checa AG, Gale JD, Gebauer D, Sainz‐Díaz CI (2012) Calcium carbonate polyamorphism and its role in biomineralization: how many amorphous calcium carbonates are there? Angew Chem Int Ed 51:11960–11970CrossRefGoogle Scholar
  19. Cartwright JH, Checa AG, Rousseau M (2013) Pearls are self-organized natural ratchets. Langmuir 29:8370–8376PubMedCrossRefGoogle Scholar
  20. Chang EP, Williamson G, Evans JS (2015) Focused ion beam tomography reveals the presence of micro-, meso-, and macroporous intracrystalline regions introduced into calcite crystals by the gastropod nacre protein AP7. Cryst Growth Des 15:1577–1582CrossRefGoogle Scholar
  21. Chang EP, Perovic I, Rao A, Cölfen H, Evans JS (2016a) In vitro glycosylation and its impact on the functionality of a recombinant intracrystalline nacre protein, AP24. Biochemistry 55(7):1024–1035Google Scholar
  22. Chang EP, Roncal-Herrero T, Morgan T, Dunn KE, Rao A, Kunitake JA, Lui S, Bilton M, Estroff LA, Kröger R (2016b) Synergistic biomineralization phenomena created by a combinatorial nacre protein model system. Biochemistry 55(16):2401–2410Google Scholar
  23. Chebotareva NA, Harding SE, Winzor DJ (2001) Ultracentrifugal studies of the effect of molecular crowding by trimethylamine N‐oxide on the self‐association of muscle glycogen phosphorylase b. Eur J Biochem 268:506–513PubMedCrossRefGoogle Scholar
  24. Checa AG, Cartwright JH, Willinger M-G (2011) Mineral bridges in nacre. J Struct Biol 176:330–339PubMedCrossRefGoogle Scholar
  25. Checa AG, Macías-Sánchez E, Harper EM, Cartwright JH (2016) Organic membranes determine the pattern of the columnar prismatic layer of mollusc shells. Proc R Soc Lond B 283:20160032Google Scholar
  26. Cölfen H (2010) Biomineralization: a crystal-clear view. Nat Mater 9:960–961PubMedCrossRefGoogle Scholar
  27. Cölfen H, Antonietti M (2008) Mesocrystals and nonclassical crystallization. Wiley, ChichesterGoogle Scholar
  28. Cölfen H, Winzor DJ (1997) A computer program based on the psi function for model-independent analysis of sedimentation equilibrium distributions reflecting macromolecular interactions. In: Jaenicke R, Durchschlag H (eds) Analytical ultracentrifugation IV. Springer, Berlin, pp 36–42Google Scholar
  29. Cölfen H, Harding SE, Vårum KM, Winzor DJ (1996) A study by analytical ultracentrifugation on the interaction between lysozyme and extensively deacetylated chitin (chitosan). Carbohydr Polym 30:45–53CrossRefGoogle Scholar
  30. Cölfen H, Harding SE, Wilson EK, Scrutton NS, Winzor DJ (1997) Low temperature solution behaviour of Methylophilus methylotrophus electron transferring flavoprotein: a study by analytical ultracentrifugation. Eur Biophys J 25:411–416CrossRefGoogle Scholar
  31. Davis-Searles PR, Saunders AJ, Erie DA, Winzor DJ, Pielak GJ (2001) Interpreting the effects of small uncharged solutes on protein-folding equilibria. Annu Rev Biophys Biomol Struct 30(1):271–306PubMedCrossRefGoogle Scholar
  32. de Nooijer LJ, Toyofuku T, Kitazato H (2009) Foraminifera promote calcification by elevating their intracellular pH. Proc Natl Acad Sci U S A 106:15374–15378PubMedPubMedCentralCrossRefGoogle Scholar
  33. De Yoreo JJ, Gilbert PU, Sommerdijk NA, Penn RL, Whitelam S, Joester D, Zhang H, Rimer JD, Navrotsky A, Banfield JF (2015) Crystallization by particle attachment in synthetic, biogenic, and geologic environments. Science 349:aaa6760PubMedCrossRefGoogle Scholar
  34. Demichelis R, Raiteri P, Gale JD, Quigley D, Gebauer D (2011) Stable prenucleation mineral clusters are liquid-like ionic polymers. Nat Commun 2:590PubMedPubMedCentralCrossRefGoogle Scholar
  35. Derganc J, Čopič A (2016) Membrane bending by protein crowding is affected by protein lateral confinement. Biochim Biophys Acta Biomembr 1858:1152–1159CrossRefGoogle Scholar
  36. Deszczynski M, Harding SE, Winzor DJ (2006) Negative second virial coefficients as predictors of protein crystal growth: evidence from sedimentation equilibrium studies that refutes the designation of those light scattering parameters as osmotic virial coefficients. Biophys Chem 120:106–113PubMedCrossRefGoogle Scholar
  37. Dewavrin J-Y, Hamzavi N, Shim V, Raghunath M (2014) Tuning the architecture of three-dimensional collagen hydrogels by physiological macromolecular crowding. Acta Biomater 10:4351–4359PubMedCrossRefGoogle Scholar
  38. Dey A, Bomans PH, Müller FA, Will J, Frederik PM, de With G, Sommerdijk NA (2010) The role of prenucleation clusters in surface-induced calcium phosphate crystallization. Nat Mater 9:1010–1014PubMedCrossRefGoogle Scholar
  39. Dill KA, Ghosh K, Schmit JD (2011) Physical limits of cells and proteomes. Proc Natl Acad Sci U S A 108:17876–17882PubMedPubMedCentralCrossRefGoogle Scholar
  40. DiMasi E, Olszta MJ, Patel VM, Gower LB (2003) When is template directed mineralization really template directed? CrystEngComm 5:346–350CrossRefGoogle Scholar
  41. Edidin M (2003) The state of lipid rafts: from model membranes to cells. Annu Rev Biophys Biomol Struct 32:257–283PubMedCrossRefGoogle Scholar
  42. Ellis RJ (2001) Macromolecular crowding: obvious but underappreciated. Trends Biochem Sci 26:597–604PubMedCrossRefGoogle Scholar
  43. Ellis RJ, Minton AP (2003) Cell biology: join the crowd. Nature 425:27–28PubMedCrossRefGoogle Scholar
  44. Erickson HP (2009) Size and shape of protein molecules at the nanometer level determined by sedimentation, gel filtration, and electron microscopy. Biol Proced Online 11:32PubMedPubMedCentralCrossRefGoogle Scholar
  45. Erlkamp M, Marion J, Martinez N, Czeslik C, Peters J, Winter R (2015) Influence of pressure and crowding on the sub-nanosecond dynamics of globular proteins. J Phys Chem B 119:4842–4848PubMedCrossRefGoogle Scholar
  46. Evans JS (2008) “Tuning in” to mollusk shell nacre-and prismatic-associated protein terminal sequences. Implications for biomineralization and the construction of high performance inorganic − organic composites. Chem Rev 108:4455–4462PubMedCrossRefGoogle Scholar
  47. Falini G, Fermani S, Gazzano M, Ripamonti A (2000) Polymorphism and architectural crystal assembly of calcium carbonate in biologically inspired polymeric matrices. J Chem Soc Dalton Trans :3983–3987Google Scholar
  48. Fan W, Li C, Li S, Feng Q, Xie L, Zhang R (2007) Cloning, characterization, and expression patterns of three sarco/endoplasmic reticulum Ca2 + −ATPase isoforms from pearl oyster (Pinctada fucata). Acta Biochim Biophys Sin 39:722–730PubMedCrossRefGoogle Scholar
  49. Feng J, Wu G, Qing C (2016) Biomimetic synthesis of hollow calcium carbonate with the existence of the agar matrix and bovine serum albumin. Mater Sci Eng C 58:409–411CrossRefGoogle Scholar
  50. Fernandez‐Martinez A, Kalkan B, Clark SM, Waychunas GA (2013) Pressure-induced polyamorphism and formation of ‘Aragonitic’Amorphous calcium carbonate. Angew Chem Int Ed 52:8354–8357CrossRefGoogle Scholar
  51. Frenkel J (1939) Statistical theory of condensation phenomena. J Chem Phys 7:200–201CrossRefGoogle Scholar
  52. Gebauer D, Cölfen H (2011) Prenucleation clusters and non-classical nucleation. Nano Today 6:564–584CrossRefGoogle Scholar
  53. Gebauer D, Völkel A, Cölfen H (2008) Stable prenucleation calcium carbonate clusters. Science 322:1819–1822PubMedCrossRefGoogle Scholar
  54. Gebauer D, Cölfen H, Verch A, Antonietti M (2009) The multiple roles of additives in CaCO3 crystallization: a quantitative case study. Adv Mater 21:435–439CrossRefGoogle Scholar
  55. Gebauer D, Kellermeier M, Gale JD, Bergström L, Cölfen H (2014) Pre-nucleation clusters as solute precursors in crystallisation. Chem Soc Rev 43:2348–2371PubMedCrossRefGoogle Scholar
  56. Gong H, Yang Y, Pluntke M, Marti O, Majer Z, Sewald N, Volkmer D (2014) Calcium carbonate crystal growth beneath Langmuir monolayers of acidic β-hairpin peptides. Dalton Trans 43:16857–16871PubMedCrossRefGoogle Scholar
  57. Goswami N, Giri A, Bootharaju MS, Xavier PL, Pradeep T, Pal SK (2011) Copper quantum clusters in protein matrix: potential sensor of Pb2+ Ion. Anal Chem 83:9676–9680PubMedCrossRefGoogle Scholar
  58. Gower LB (2008) Biomimetic model systems for investigating the amorphous precursor pathway and its role in biomineralization. Chem Rev 108:4551–4627PubMedCrossRefGoogle Scholar
  59. Gower LB, Odom DJ (2000) Deposition of calcium carbonate films by a polymer-induced liquid-precursor (PILP) process. J Cryst Growth 210:719–734CrossRefGoogle Scholar
  60. Guilak F, Erickson GR, Ting-Beall HP (2002) The effects of osmotic stress on the viscoelastic and physical properties of articular chondrocytes. Biophys J 82:720–727PubMedPubMedCentralCrossRefGoogle Scholar
  61. Guo C, Irudayaraj J (2011) Fluorescent Ag clusters via a protein-directed approach as a Hg(II) ion sensor. Anal Chem 83:2883–2889PubMedCrossRefGoogle Scholar
  62. Ha J-M, Wolf JH, Hillmyer MA, Ward MD (2004) Polymorph selectivity under nanoscopic confinement. J Am Chem Soc 126:3382–3383PubMedCrossRefGoogle Scholar
  63. Hall DR, Jacobsen MP, Winzor DJ (1995) Stabilizing effect of sucrose against irreversible denaturation of rabbit muscle lactate dehydrogenase. Biophys Chem 57(1):47–54PubMedCrossRefGoogle Scholar
  64. Hamilton BD, Hillmyer MA, Ward MD (2008) Glycine polymorphism in nanoscale crystallization chambers. Cryst Growth Des 8:3368–3375CrossRefGoogle Scholar
  65. Hamley IW (2010) Liquid crystal phase formation by biopolymers. Soft Matter 6:1863–1871CrossRefGoogle Scholar
  66. Heiss A, Jahnen-Dechent W, Endo H, Schwahn D (2007) Structural dynamics of a colloidal protein-mineral complex bestowing on calcium phosphate a high solubility in biological fluids. Biointerphases 2:16–20PubMedCrossRefGoogle Scholar
  67. Heiss A, Pipich V, Jahnen-Dechent W, Schwahn D (2010) Fetuin-A is a mineral carrier protein: small angle neutron scattering provides new insight on Fetuin-A controlled calcification inhibition. Biophys J 99:3986–3995PubMedPubMedCentralCrossRefGoogle Scholar
  68. Hyman AA, Brangwynne CP (2011) Beyond stereospecificity: liquids and mesoscale organization of cytoplasm. Dev Cell 21:14–16PubMedCrossRefGoogle Scholar
  69. Hyman AA, Weber CA, Jülicher F (2014) Liquid-liquid phase separation in biology. Annu Rev Cell Dev Biol 30:39–58PubMedCrossRefGoogle Scholar
  70. Ianeselli L, Zhang F, Skoda MWA, Jacobs RMJ, Martin RA, Callow S, Prévost S, Schreiber F (2010) Protein − protein interactions in ovalbumin solutions studied by small-angle scattering: effect of ionic strength and the chemical nature of cations. J Phys Chem B 114:3776–3783PubMedCrossRefGoogle Scholar
  71. Jackson DJ, McDougall C, Woodcroft B, Moase P, Rose RA, Kube M, Reinhardt R, Rokhsar DS, Montagnani C, Joubert C (2010) Parallel evolution of nacre building gene sets in molluscs. Mol Biol Evol 27:591–608PubMedCrossRefGoogle Scholar
  72. Jain G, Pendola M, Rao A, Cölfen H, Evans JS (2016) A model sea urchin spicule matrix protein self-associates to form mineral-modifying protein hydrogels. Biochemistry 55(31):4410–4421PubMedCrossRefGoogle Scholar
  73. Jolivet J-P, Tronc E, Chanéac C (2006) Iron oxides: from molecular clusters to solid. A nice example of chemical versatility. Compt Rendus Geosci 338:488–497CrossRefGoogle Scholar
  74. Knight DP, Vollrath F (2002) Biological liquid crystal elastomers. Philos Trans R Soc Lond B 357:155–163CrossRefGoogle Scholar
  75. Knothe TM (2003) “Whither flows the fluid in bone?” An osteocyte’s perspective. J Biomech 36:1409–1424CrossRefGoogle Scholar
  76. Konno H, Taylor LS (2006) Influence of different polymers on the crystallization tendency of molecularly dispersed amorphous felodipine. J Pharm Sci 95:2692–2705PubMedCrossRefGoogle Scholar
  77. Kory N, Thiam A-R, Farese RV, Walther TC (2015) Protein crowding is a determinant of lipid droplet protein composition. Dev Cell 34:351–363PubMedPubMedCentralCrossRefGoogle Scholar
  78. Kosanović C, Falini G, Kralj D (2010) Mineralization of calcium carbonates in gelling media. Cryst Growth Des 11:269–277CrossRefGoogle Scholar
  79. Lareu RR, Subramhanya KH, Peng Y, Benny P, Chen C, Wang Z, Rajagopalan R, Raghunath M (2007) Collagen matrix deposition is dramatically enhanced in vitro when crowded with charged macromolecules: the biological relevance of the excluded volume effect. FEBS Lett 581:2709–2714PubMedCrossRefGoogle Scholar
  80. Li H, Estroff LA (2009) Calcite growth in hydrogels: assessing the mechanism of polymer-network incorporation into single crystals. Adv Mater 21:470–473CrossRefGoogle Scholar
  81. Lin Y, Protter DS, Rosen MK, Parker R (2015) Formation and maturation of phase-separated liquid droplets by RNA-binding proteins. Mol Cell 60:208–219PubMedPubMedCentralCrossRefGoogle Scholar
  82. Lingwood D, Simons K (2010) Lipid rafts as a membrane-organizing principle. Science 327:46–50PubMedCrossRefGoogle Scholar
  83. Liu B, Zeng HC (2005) Symmetric and asymmetric Ostwald ripening in the fabrication of homogeneous core–shell semiconductors. Small 1:566–571PubMedCrossRefGoogle Scholar
  84. Lowenstam HA, Weiner S (1989) On biomineralization. Oxford University Press, Oxford; on demandGoogle Scholar
  85. Mackinder L, Wheeler G, Schroeder D, von Dassow P, Riebesell U, Brownlee C (2011) Expression of biomineralization-related ion transport genes in Emiliania huxleyi. Environ Microbiol 13:3250–3265PubMedCrossRefGoogle Scholar
  86. Mahamid J, Sharir A, Gur D, Zelzer E, Addadi L, Weiner S (2011) Bone mineralization proceeds through intracellular calcium phosphate loaded vesicles: a cryo-electron microscopy study. J Struct Biol 174:527–535PubMedCrossRefGoogle Scholar
  87. Mann S (2001) Biomineralization: principles and concepts in bioinorganic materials chemistry, vol 5. Oxford University Press, Oxford, on demandGoogle Scholar
  88. Mann K, Maček B, Olsen JV (2006) Proteomic analysis of the acid-soluble organic matrix of the chicken calcified eggshell layer. Proteomics 6:3801–3810PubMedCrossRefGoogle Scholar
  89. Mann K, Wilt FH, Poustka AJ (2010) Proteomic analysis of sea urchin (Strongylocentrotus purpuratus) spicule matrix. Proteome Sci 8:1CrossRefGoogle Scholar
  90. Marie B, Marie A, Jackson DJ, Dubost L, Degnan BM, Milet C, Marin F (2010) Proteomic analysis of the organic matrix of the abalone Haliotis asinina calcified shell. Proteome Sci 8:1CrossRefGoogle Scholar
  91. Meldrum FC, Cölfen H (2008) Controlling mineral morphologies and structures in biological and synthetic systems. Chem Rev 108:4332–4432PubMedCrossRefGoogle Scholar
  92. Minton AP (1992) Confinement as a determinant of macromolecular structure and reactivity. Biophys J 63:1090PubMedPubMedCentralCrossRefGoogle Scholar
  93. Minton AP (1995) Confinement as a determinant of macromolecular structure and reactivity. II. Effects of weakly attractive interactions between confined macrosolutes and confining structures. Biophys J 68:1311PubMedPubMedCentralCrossRefGoogle Scholar
  94. Minton AP (2001) The influence of macromolecular crowding and macromolecular confinement on biochemical reactions in physiological media. J Biol Chem 276:10577–10580PubMedCrossRefGoogle Scholar
  95. Minton AP (2006) Macromolecular crowding. Curr Biol 16:R269–R271PubMedCrossRefGoogle Scholar
  96. Moilanen DE, Levinger NE, Spry D, Fayer M (2007) Confinement or the nature of the interface? Dynamics of nanoscopic water. J Am Chem Soc 129:14311–14318PubMedPubMedCentralCrossRefGoogle Scholar
  97. Molliex A, Temirov J, Lee J, Coughlin M, Kanagaraj AP, Kim HJ, Mittag T, Taylor JP (2015) Phase separation by low complexity domains promotes stress granule assembly and drives pathological fibrillization. Cell 163:123–133PubMedPubMedCentralCrossRefGoogle Scholar
  98. Morissette SL, Almarsson Ö, Peterson ML, Remenar JF, Read MJ, Lemmo AV, Ellis S, Cima MJ, Gardner CR (2004) High-throughput crystallization: polymorphs, salts, co-crystals and solvates of pharmaceutical solids. Adv Drug Deliv Rev 56:275–300PubMedCrossRefGoogle Scholar
  99. Murr MM, Thakur GS, Li Y, Tsuruta H, Mezic I, Morse DE (2009) New pathway for self-assembly and emergent properties. Nano Today 4:116–124CrossRefGoogle Scholar
  100. Nakahara H (1991) Nacre formation in bivalve and gastropod molluscs. In: Suga S, Nakahara H (eds) Mechanisms and phylogeny of mineralization in biological systems. Springer, Berlin, pp 343–350Google Scholar
  101. Navrotsky A (2004) Energetic clues to pathways to biomineralization: precursors, clusters, and nanoparticles. Proc Natl Acad Sci U S A 101:12096–12101PubMedPubMedCentralCrossRefGoogle Scholar
  102. Niederberger M, Cölfen H (2006) Oriented attachment and mesocrystals: non-classical crystallization mechanisms based on nanoparticle assembly. Phys Chem Chem Phys 8:3271–3287PubMedCrossRefGoogle Scholar
  103. Nikolov S, Petrov M, Lymperakis L, Friák M, Sachs C, Fabritius HO, Raabe D, Neugebauer J (2010) Revealing the design principles of high-performance biological composites using Ab initio and multiscale simulations: the example of lobster cuticle. Adv Mater 22:519–526PubMedCrossRefGoogle Scholar
  104. Nudelman F, Pieterse K, George A, Bomans PH, Friedrich H, Brylka LJ, Hilbers PA, de With G, Sommerdijk NA (2010) The role of collagen in bone apatite formation in the presence of hydroxyapatite nucleation inhibitors. Nat Mater 9:1004–1009PubMedPubMedCentralCrossRefGoogle Scholar
  105. Oaki Y, Hayashi S, Imai H (2007) A hierarchical self-similar structure of oriented calcite with association of an agar gel matrix: inheritance of crystal habit from nanoscale. Chem Commun 27:2841–2843Google Scholar
  106. Ogston AG, Winzor DJ (1975) Treatment of thermodynamic nonideality in equilibrium studies on associating solutes. J Phys Chem 79:2496–2500CrossRefGoogle Scholar
  107. Olszta MJ, Odom DJ, Douglas EP, Gower LB (2009) A new paradigm for biomineral formation: mineralization via an amorphous liquid-phase precursor. Connect Tissue Res 44(Suppl 1):326–334Google Scholar
  108. Oparin AI (1938) The origin of life. Macmillan, New YorkGoogle Scholar
  109. Panheleux M, Bain M, Fernandez M, Morales I, Gautron J, Arias J, Solomon S, Hincke M, Nys Y (1999) Organic matrix composition and ultrastructure of eggshell: a comparative study. Br Poult Sci 40:240–252PubMedCrossRefGoogle Scholar
  110. Patel CN, Noble SM, Weatherly GT, Tripathy A, Winzor DJ, Pielak GJ (2002) Effects of molecular crowding by saccharides on α‐chymotrypsin dimerization. Protein Sci 11(5):997–1003PubMedPubMedCentralCrossRefGoogle Scholar
  111. Pereira-Mouriès L, Almeida MJ, Ribeiro C, Peduzzi J, Barthélemy M, Milet C, Lopez E (2002) Soluble silk-like organic matrix in the nacreous layer of the bivalve Pinctada maxima. Eur J Biochem 269:4994–5003PubMedCrossRefGoogle Scholar
  112. Perovic I, Chang EP, Lui M, Rao A, Cölfen H, Evans JS (2014) A nacre protein, n16. 3, self-assembles to form protein oligomers that dimensionally limit and organize mineral deposits. Biochemistry 53:2739–2748PubMedCrossRefGoogle Scholar
  113. Poon J, Bailey M, Winzor DJ, Davidson BE, Sawyer WH (1997) Effects of molecular crowding on the interaction between DNA and the Escherichia coli regulatory protein TyrR. Biophys J 73:3257–3264PubMedPubMedCentralCrossRefGoogle Scholar
  114. Prajapati S, Tao J, Ruan Q, De Yoreo JJ, Moradian-Oldak J (2016) Matrix metalloproteinase-20 mediates dental enamel biomineralization by preventing protein occlusion inside apatite crystals. Biomaterials 75:260–270PubMedCrossRefGoogle Scholar
  115. Qin C, Baba O, Butler W (2004) Post-translational modifications of sibling proteins and their roles in osteogenesis and dentinogenesis. Crit Rev Oral Biol Med 15:126–136PubMedCrossRefGoogle Scholar
  116. Raabe D, Romano P, Sachs C, Fabritius H, Al-Sawalmih A, Yi S-B, Servos G, Hartwig H (2006) Microstructure and crystallographic texture of the chitin–protein network in the biological composite material of the exoskeleton of the lobster Homarus americanus. Mater Sci Eng A 421:143–153CrossRefGoogle Scholar
  117. Raiteri P, Gale JD (2010) Water is the key to nonclassical nucleation of amorphous calcium carbonate. J Am Chem Soc 132:17623–17634PubMedCrossRefGoogle Scholar
  118. Rajapaksha A, Stanley CB, Todd BA (2015) Effects of macromolecular crowding on the structure of a protein complex: a small-angle scattering study of superoxide dismutase. Biophys J 108:967–974PubMedPubMedCentralCrossRefGoogle Scholar
  119. Rao A, Cölfen H (2016) On the biophysical regulation of mineral growth: standing out from the crowd. J Struct Biol. doi: 10.1016/j.jsb.2016.03.021
  120. Rao A, Seto J, Berg JK, Kreft SG, Scheffner M, Cölfen H (2013) Roles of larval sea urchin spicule SM50 domains in organic matrix self-assembly and calcium carbonate mineralization. J Struct Biol 183:205–215PubMedCrossRefGoogle Scholar
  121. Rao A, Berg JK, Kellermeier M, Gebauer D (2014) Sweet on biomineralization: effects of carbohydrates on the early stages of calcium carbonate crystallization. Eur J Mineral 26:537–552CrossRefGoogle Scholar
  122. Rao A, Fernández MS, Cölfen H, Arias JL (2015) Distinct effects of avian egg derived anionic proteoglycans on the early stages of calcium carbonate mineralization. Cryst Growth Des 15:2052–2056CrossRefGoogle Scholar
  123. Rao A, Vásquez-Quitral P, Fernández MS, Berg JK, Sánchez M, Drechsler M, Neira-Carrillo A, Arias JL, Gebauer D, Cölfen H (2016) pH-dependent schemes of calcium carbonate formation in the presence of alginates. Cryst Growth Des 16:1349–1359CrossRefGoogle Scholar
  124. Rivas G, Fernandez JA, Minton AP (1999) Direct observation of the self-association of dilute proteins in the presence of inert macromolecules at high concentration via tracer sedimentation equilibrium: theory, experiment, and biological significance. Biochemistry 38:9379–9388PubMedCrossRefGoogle Scholar
  125. Romano P, Fabritius H, Raabe D (2007) The exoskeleton of the lobster Homarus americanus as an example of a smart anisotropic biological material. Acta Biomater 3:301–309PubMedCrossRefGoogle Scholar
  126. Saeidi N, Karmelek KP, Paten JA, Zareian R, DiMasi E, Ruberti JW (2012) Molecular crowding of collagen: a pathway to produce highly-organized collagenous structures. Biomaterials 33:7366–7374PubMedPubMedCentralCrossRefGoogle Scholar
  127. Samiotakis A, Wittung-Stafshede P, Cheung MS (2009) Folding, stability and shape of proteins in crowded environments: experimental and computational approaches. Int J Mol Sci 10:572–588PubMedPubMedCentralCrossRefGoogle Scholar
  128. Schuck P (2003) On the analysis of protein self-association by sedimentation velocity analytical ultracentrifugation. Anal Biochem 320:104–124PubMedCrossRefGoogle Scholar
  129. Schwartz DK (2001) Mechanisms and kinetics of self-assembled monolayer formation. Annu Rev Phys Chem 52:107–137PubMedCrossRefGoogle Scholar
  130. Scott DJ, Patel TR, Besong DM, Stetefeld J, Winzor DJ (2011) Examination of the discrepancy between size estimates for ovalbumin from small-angle X-ray scattering and other physicochemical measurements. J Phys Chem B 115:10725–10729PubMedCrossRefGoogle Scholar
  131. Seto J, Picker A, Chen Y, Rao A, Evans JS, Cölfen H (2014) Nacre protein sequence compartmentalizes mineral polymorphs in solution. Cryst Growth Des 14(4):1501–1505CrossRefGoogle Scholar
  132. Shearwin KE, Winzor DJ (1988) Effect of sucrose on the dimerization of α-chymotrypsin allowance for thermodynamic nonideality arising from the presence of a small inert solute. Biophys Chem 31:287–294PubMedCrossRefGoogle Scholar
  133. Shearwin KE, Winzor DJ (1990a) Effect of calcium ion on the dimerization of α-chymotrypsin. Biochim Biophys Acta 1038(1):136–138PubMedCrossRefGoogle Scholar
  134. Shearwin KE, Winzor DJ (1990b) Thermodynamic nonideality in macromolecular solutions. Eur J Biochem 190:523–529PubMedCrossRefGoogle Scholar
  135. Shtilerman MD, Ding TT, Lansbury PT (2002) Molecular crowding accelerates fibrillization of α-synuclein: could an increase in the cytoplasmic protein concentration induce Parkinson’s disease? Biochemistry 41:3855–3860PubMedCrossRefGoogle Scholar
  136. Silvius JR (2003) Role of cholesterol in lipid raft formation: lessons from lipid model systems. Biochim Biophys Acta Biomembr 1610:174–183CrossRefGoogle Scholar
  137. Sottnik JL, Dai J, Zhang H, Campbell B, Keller ET (2015) Tumor-induced pressure in the bone microenvironment causes osteocytes to promote the growth of prostate cancer bone metastases. Cancer Res 75:2151–2158PubMedPubMedCentralCrossRefGoogle Scholar
  138. Spencer DS, Xu K, Logan TM, Zhou H-X (2005) Effects of pH, salt, and macromolecular crowding on the stability of FK506-binding protein: an integrated experimental and theoretical study. J Mol Biol 351:219–232PubMedCrossRefGoogle Scholar
  139. Spitzer J, Poolman B (2009) The role of biomacromolecular crowding, ionic strength, and physicochemical gradients in the complexities of life’s emergence. Microbiol Mol Biol Rev 73:371–388PubMedPubMedCentralCrossRefGoogle Scholar
  140. Spitzer J, Pielak GJ, Poolman B (2015) Emergence of life: physical chemistry changes the paradigm. Biol Direct 10:33PubMedPubMedCentralCrossRefGoogle Scholar
  141. Sudo S, Fujikawa T, Nagakura T, Ohkubo T, Sakaguchi K, Tanaka M, Nakashima K, Takahashi T (1997) Structures of mollusc shell framework proteins. Nature 387:563–564PubMedCrossRefGoogle Scholar
  142. Sumper M (2002) A phase separation model for the nanopatterning of diatom biosilica. Science 295:2430–2433PubMedCrossRefGoogle Scholar
  143. Sumper M (2004) Biomimetic patterning of silica by long-chain polyamines. Angew Chem Int Ed 43:2251–2254CrossRefGoogle Scholar
  144. Sun J, Bhushan B (2012) Hierarchical structure and mechanical properties of nacre: a review. RSC Adv 2:7617–7632CrossRefGoogle Scholar
  145. Tagliabracci VS, Engel JL, Wen J, Wiley SE, Worby CA, Kinch LN, Xiao J, Grishin NV, Dixon JE (2012) Secreted kinase phosphorylates extracellular proteins that regulate biomineralization. Science 336:1150–1153PubMedPubMedCentralCrossRefGoogle Scholar
  146. Tan BH, Tam KC, Lam YC, Tan CB (2005) Osmotic compressibility of soft colloidal systems. Langmuir 21:4283–4290PubMedCrossRefGoogle Scholar
  147. Tester CC, Brock RE, Wu C-H, Krejci MR, Weigand S, Joester D (2011) In vitro synthesis and stabilization of amorphous calcium carbonate (ACC) nanoparticles within liposomes. CrystEngComm 13:3975–3978CrossRefGoogle Scholar
  148. Thula TT, Rodriguez DE, Lee MH, Pendi L, Podschun J, Gower LB (2011) In vitro mineralization of dense collagen substrates: a biomimetic approach toward the development of bone-graft materials. Acta Biomater 7:3158–3169PubMedPubMedCentralCrossRefGoogle Scholar
  149. Toroian D, Lim JE, Price PA (2007) The size exclusion characteristics of type I collagen implications for the role of noncollagenous bone constituents in mineralization. J Biol Chem 282:22437–22447PubMedCrossRefGoogle Scholar
  150. Verch A, Gebauer D, Antonietti M, Cölfen H (2011) How to control the scaling of CaCO 3: A “fingerprinting technique” to classify additives. Phys Chem Chem Phys 13:16811–16820PubMedCrossRefGoogle Scholar
  151. Vidavsky N, Addadi S, Mahamid J, Shimoni E, Ben-Ezra D, Shpigel M, Weiner S, Addadi L (2014) Initial stages of calcium uptake and mineral deposition in sea urchin embryos. Proc Natl Acad Sci U S A 111:39–44PubMedCrossRefGoogle Scholar
  152. Volkmer D, Fricke M, Agena C, Mattay J (2004) Interfacial electrostatics guiding the crystallization of CaCO 3 underneath monolayers of calixarenes and resorcarenes. J Mater Chem 14:2249–2259CrossRefGoogle Scholar
  153. Wallace AF, Hedges LO, Fernandez-Martinez A, Raiteri P, Gale JD, Waychunas GA, Whitelam S, Banfield JF, De Yoreo JJ (2013) Microscopic evidence for liquid-liquid separation in supersaturated CaCO3 solutions. Science 341:885–889PubMedCrossRefGoogle Scholar
  154. Wang X, Sun H, Xia Y, Chen C, Xu H, Shan H, Lu JR (2009) Lysozyme mediated calcium carbonate mineralization. J Colloid Interface Sci 332:96–103PubMedCrossRefGoogle Scholar
  155. Wang X, Wu C, Tao K, Zhao K, Wang J, Xu H, Xia D, Shan H, Lu JR (2010) Influence of ovalbumin on CaCO3 precipitation during in vitro biomineralization. J Phys Chem B 114:5301–5308PubMedCrossRefGoogle Scholar
  156. Weiner S, Traub W (1980) X-ray diffraction study of the insoluble organic matrix of mollusk shells. FEBS Lett 111:311–316CrossRefGoogle Scholar
  157. Wills PR, Winzor DJ (2005) van der Waals phase transition in protein solutions. Acta Crystallogr Sect D 61(6):832–836CrossRefGoogle Scholar
  158. Wills PR, Comper WD, Winzor DJ (1993) Thermodynamic nonideality in macromolecular solutions: interpretation of virial coefficients. Arch Biochem Biophys 300:206–212PubMedCrossRefGoogle Scholar
  159. Wilson EK, Scrutton NS, Cölfen H, Harding SE, Jacobsen MP, Winzor DJ (1997) An ultracentrifugal approach to quantitative characterization of the molecular assembly of a physiological electron‐transfer complex. Eur J Biochem 243:393–399PubMedCrossRefGoogle Scholar
  160. Wingender B, Bradley P, Saxena N, Ruberti JW, Gower L (2016) Biomimetic organization of collagen matrices to template bone-like microstructures. Matrix Biol 52:384–396PubMedCrossRefGoogle Scholar
  161. Winzor DJ (1966) Detection of interaction in gluten extracts by gel filtration. Arch Biochem Biophys 113(2):421–426PubMedCrossRefGoogle Scholar
  162. Winzor DJ (2004) Determination of the net charge (valence) of a protein: a fundamental but elusive parameter. Anal Biochem 325:1–20PubMedCrossRefGoogle Scholar
  163. Winzor DJ, Wills PR (1986) Effects of thermodynamic nonideality on protein interactions: equivalence of interpretations based on excluded volume and preferential solvation. Biophys Chem 25:243–251PubMedCrossRefGoogle Scholar
  164. Winzor DJ, Wills PR (2006) Molecular crowding effects of linear polymers in protein solutions. Biophys Chem 119(2):186–195PubMedCrossRefGoogle Scholar
  165. Winzor CL, Winzor DJ, Paleg LG, Jones GP, Naidu BP (1992) Rationalization of the effects of compatible solutes on protein stability in terms of thermodynamic nonideality. Arch Biochem Biophys 296:102–107PubMedCrossRefGoogle Scholar
  166. Winzor DJ, Carrington LE, Deszczynski M, Harding SE (2004) Extent of charge screening in aqueous polysaccharide solutions. Biomacromolecules 5(6):2456–2460PubMedCrossRefGoogle Scholar
  167. Winzor DJ, Deszczynski M, Harding SE, Wills PR (2007) Nonequivalence of second virial coefficients from sedimentation equilibrium and static light scattering studies of protein solutions. Biophys Chem 128(1):46–55PubMedCrossRefGoogle Scholar
  168. Wohlrab S, Cölfen H, Antonietti M (2005) Crystalline, porous microspheres made from amino acids by using polymer-induced liquid precursor phases. Angew Chem Int Ed 44:4087–4092CrossRefGoogle Scholar
  169. Wolf SE, Leiterer J, Pipich V, Barrea R, Emmerling F, Tremel W (2011) Strong stabilization of amorphous calcium carbonate emulsion by ovalbumin: gaining insight into the mechanism of ‘polymer-induced liquid precursor’ processes. J Am Chem Soc 133:12642–12649PubMedPubMedCentralCrossRefGoogle Scholar
  170. Woo E, Huh J, Jeong YG, Shin K (2007) From homogeneous to heterogeneous nucleation of chain molecules under nanoscopic cylindrical confinement. Phys Rev Lett 98:136103PubMedCrossRefGoogle Scholar
  171. Xia Y, Gu Y, Zhou X, Xu H, Zhao X, Yaseen M, Lu JR (2012) Controllable stabilization of poly (N-isopropylacrylamide)-based microgel films through biomimetic mineralization of calcium carbonate. Biomacromolecules 13:2299–2308PubMedCrossRefGoogle Scholar
  172. Xiang S, Kato M, Wu LC, Lin Y, Ding M, Zhang Y, Yu Y, McKnight SL (2015) The LC domain of hnRNPA2 adopts similar conformations in hydrogel polymers, liquid-like droplets, and nuclei. Cell 163:829–839PubMedPubMedCentralCrossRefGoogle Scholar
  173. Xie AJ, Zhang CY, Shen YH, Qiu LG, Xiao PP, Hu ZY (2006) Morphologies of calcium carbonate crystallites grown from aqueous solutions containing polyethylene glycol. Cryst Res Technol 41:967–971CrossRefGoogle Scholar
  174. Xie J, Zheng Y, Ying JY (2009) Protein-directed synthesis of highly fluorescent gold nanoclusters. J Am Chem Soc 131:888–889PubMedCrossRefGoogle Scholar
  175. Xu G, Evans JS (1999) Model peptide studies of sequence repeats derived from the intracrystalline biomineralization protein, SM50. I. GVGGR and GMGGQ repeats. Biopolymers 49:303–312Google Scholar
  176. Xu AW, Dong WF, Antonietti M, Cölfen H (2008) Polymorph switching of calcium carbonate crystals by polymer-controlled crystallization. Adv Funct Mater 18:1307–1313CrossRefGoogle Scholar
  177. Xu Z, Hirtz M, Yuan S, Liu C, Chi L (2011) Selective deposition of organic molecules onto different densely packed self-assembled monolayers: a molecular dynamics study. Chem Phys Lett 507:138–143CrossRefGoogle Scholar
  178. Yang L, Killian CE, Kunz M, Tamura N, Gilbert P (2011) Biomineral nanoparticles are space-filling. Nanoscale 3:603–609PubMedCrossRefGoogle Scholar
  179. Zhou H-X, Dill KA (2001) Stabilization of proteins in confined spaces. Biochemistry 40:11289–11293PubMedCrossRefGoogle Scholar
  180. Zhou H-X, Rivas G, Minton AP (2008) Macromolecular crowding and confinement: biochemical, biophysical, and potential physiological consequences. Annu Rev Biophys 37:375PubMedPubMedCentralCrossRefGoogle Scholar
  181. Zimmerman SB, Minton AP (1993) Macromolecular crowding: biochemical, biophysical, and physiological consequences. Annu Rev Biophys Biomol Struct 22:27–65PubMedCrossRefGoogle Scholar
  182. Zimmerman SB, Trach SO (1991) Estimation of macromolecule concentrations and excluded volume effects for the cytoplasm of Escherichia coli. J Mol Biol 222:599–620PubMedCrossRefGoogle Scholar

Copyright information

© International Union for Pure and Applied Biophysics (IUPAB) and Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Freiburg Institute for Advanced StudiesAlbert Ludwigs University of FreiburgFreiburg im BreisgauGermany
  2. 2.Physical Chemistry, Department of ChemistryUniversity of KonstanzKonstanzGermany

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