Biomineralization is the process by which living organisms produce minerals, often to harden or stiffen existing tissues. Such tissues are called mineralized tissues. It is an extremely widespread phenomenon; all six taxonomic kingdoms contain members that are able to form minerals, and over 60 different minerals have been identified in organisms. Examples include silicates in algae and diatoms, carbonates in invertebrates, and calcium phosphates and carbonates in vertebrates. These minerals often form structural features such as sea shells and the bone in mammals and birds. Organisms have been producing mineralised skeletons for the past 550 million years. Other examples include copper, iron and gold deposits involving bacteria. Biologically-formed minerals often have special uses such as magnetic sensors in magnetotactic bacteria (Fe3O4), gravity sensing devices (CaCO3, CaSO4, BaSO4) and iron storage and mobilization (Fe2O3•H2O in the protein ferritin).
In terms of taxonomic distribution, the most common biominerals are the phosphate and carbonate salts of calcium that are used in conjunction with organic polymers such as collagen and chitin to give structural support to bones and shells. The structures of these biocomposite materials are highly controlled from the nanometer to the macroscopic level, resulting in complex architectures that provide multifunctional properties. Because this range of control over mineral growth is desirable for materials engineering applications, there is significant interest in understanding and elucidating the mechanisms of biologically controlled biomineralization.
Biominerals perform a variety of roles in organisms, the most important being support, defense and feeding.
If present on a super-cellular scale, biominerals are usually deposited by a dedicated organ, which is often defined very early in the embryological development. This organ will contain an organic matrix that facilitates and directs the deposition of crystals. The matrix may be collagen, as in deuterostomes, or based on chitin or other polysaccharides, as in molluscs.
Shell formation in molluscs
The mollusc shell is a biogenic composite material that has been the subject of much interest in materials science because of its unusual properties and its model character for biomineralization. Molluscan shells consist of 95–99% calcium carbonate by weight, while an organic component makes up the remaining 1–5%. The resulting composite has a fracture toughness ~3000 times greater than that of the crystals themselves. In the biomineralization of the mollusc shell, specialized proteins are responsible for directing crystal nucleation, phase, morphology, and growths dynamics and ultimately give the shell its remarkable mechanical strength. The application of biomimetic principles elucidated from mollusc shell assembly and structure may help in fabricating new composite materials with enhanced optical, electronic, or structural properties.
Because extracellular iron is strongly involved in inducing calcification, its control is essential in developing shells; the protein ferritin plays an important role in controlling the distribution of iron.
The first evidence of biomineralization dates to some  and sponge-grade organisms may have formed calcite skeletons . But in most lineages, biomineralization first occurred in the Cambrian or Ordovician periods. Organisms used whichever form of calcium carbonate was more stable in the water column at the point in time when they became biomineralized, and stuck with that form for the remainder of their biological history (but see  for a more detailed analysis). The stability is dependent on the Ca/Mg ratio of seawater, which is thought to be controlled primarily by the rate of sea floor spreading, although atmospheric CO
2 levels may also play a role.
Biomineralization evolved multiple times, independently, and most animal lineages first expressed biomineralized components in the Cambrian period. Interestingly, many of the same processes are used in unrelated lineages, which suggests that biomineralization machinery was assembled from pre-existing "off-the-shelf" components already used for other purposes in the organism. Although the biomachinery facilitating biomineralization is complex – involving signalling transmitters, inhibitors, and transcription factors – many elements of this 'toolkit' are shared between phyla as diverse as corals, molluscs, and vertebrates. The shared components tend to perform quite fundamental tasks, such as designating that cells will be used to create the minerals, whereas genes controlling more finely tuned aspects that occur later in the biomineralization process – such as the precise alignment and structure of the crystals produced – tend to be uniquely evolved in different lineages. This suggests that Precambrian organisms were employing the same elements, albeit for a different purpose — perhaps to avoid the inadvertent precipitation of calcium carbonate from the supersaturated Proterozoic oceans. Forms of mucus that are involved in inducing mineralization in most metazoan lineages appear to have performed such an anticalcifatory function in the ancestral state. Further, certain proteins that would originally have been involved in maintaining calcium concentrations within cells are homologous to all metazoans, and appear to have been co-opted into biomineralization after the divergence of the metazoan lineages. The galaxins are one probable example of a gene being co-opted from a different ancestral purpose into controlling biomineralization, in this case being 'switched' to this purpose in the Triassic scleractinian corals; the role performed appears to be functionally identical to the unrelated pearlin gene in molluscs. Carbonic anhydrase serves a role in mineralization in sponges, as well as metazoans, implying an ancestral role. Far from being a rare trait that evolved a few times and remained stagnant, biomineralization pathways in fact evolved many times and are still evolving rapidly today; even within a single genus it is possible to detect great variation within a single gene family.
The homology of biomineralization pathways is underlined by a remarkable experiment whereby the nacreous layer of a molluscan shell was implanted into a human tooth, and rather than experiencing an immune response, the molluscan nacre was incorporated into the host bone matrix. This points to the exaptation of an original biomineralization pathway.
The most ancient example of biomineralization, dating back 2 billion years, is the deposition of magnetite, which is observed in some bacteria, as well as the teeth of chitons and the brains of vertebrates; it is possible that this pathway, which performed a magnetosensory role in the common ancestor of all bilaterians, was duplicated and modified in the Cambrian to form the basis for calcium-based biomineralization pathways. Iron is stored in close proximity to magnetite-coated chiton teeth, so that the teeth can be renewed as they wear. Not only is there a marked similarity between the magnetite deposition process and enamel deposition in vertebrates but some vertebrates even have comparable iron storage facilities near their teeth.
|Type of mineralization||Examples of organisms|
|Calcium carbonate (calcite or aragonite)|
|Apatite (phosphate carbonate)|
It has been suggested that biominerals could be important indicators of extraterrestrial life and thus could play an important role in the search for past or present life on Mars. Furthermore, organic components (biosignatures) that are often associated with biominerals are believed to play crucial roles in both pre-biotic and biotic reactions.
On January 24, 2014, NASA reported that current studies by the Curiosity and Opportunity rovers on the planet Mars will now be searching for evidence of ancient life, including a biosphere based on autotrophic, chemotrophic and/or chemolithoautotrophic microorganisms, as well as ancient water, including fluvio-lacustrine environments (plains related to ancient rivers or lakes) that may have been habitable. The search for evidence of habitability, taphonomy (related to fossils), and organic carbon on the planet Mars is now a primary NASA objective.
Most traditional approaches to synthesis of nanoscale materials are energy inefficient, requiring stringent conditions (e.g., high temperature, pressure or pH) and often produce toxic byproducts. Furthermore, the quantities produced are small, and the resultant material is usually irreproducible because of the difficulties in controlling agglomeration. In contrast, materials produced by organisms have properties that usually surpass those of analogous synthetically manufactured materials with similar phase composition. Biological materials are assembled in aqueous environments under mild conditions by using macromolecules. Organic macromolecules collect and transport raw materials and assemble these substrates and into short- and long-range ordered composites with consistency and uniformity. The aim of biomimetics is to mimic the natural way of producing minerals such as apatites. Many man-made crystals require elevated temperatures and strong chemical solutions, whereas the organisms have long been able to lay down elaborate mineral structures at ambient temperatures. Often, the mineral phases are not pure but are made as composites that entail an organic part, often protein, which takes part in and controls the biomineralisation. These composites are often not only as hard as the pure mineral but also tougher, as the micro-environment controls biomineralisation.
- Biomineralising polychaetes
- Bone mineral
- Diatomaceous earth
- Magnetotactic bacteria
- Mineralized tissues
- "Terminology for biorelated polymers and applications (IUPAC Recommendations 2012)". Pure and Applied Chemistry 84 (2): 377–410. 2012. doi:10.1351/PAC-REC-10-12-04.
- Astrid Sigel, Helmut Sigel and Roland K.O. Sigel, ed. (2008). Biomineralization: From Nature to Application. Metal Ions in Life Sciences 4. Wiley. ISBN 978-0-470-03525-2.
- Weiner, Stephen; Lowenstam, Heinz A. (1989). On biomineralization. Oxford [Oxfordshire]: Oxford University Press. ISBN 0-19-504977-2.
- Jean-Pierre Cuif, Yannicke Dauphin, James E. Sorauf (2011). Biominerals and fossils through time. Cambridge. ISBN 978-0-521-87473-1.
- Vinn, O. (2013). "Occurrence formation and function of organic sheets in the mineral tube structures of Serpulidae (Polychaeta Annelida)". PLoS ONE 8 (10): e75330. doi:10.1371/journal.pone.0075330. Retrieved 2013-10-27.
- Boskey, A. L. (1998). "Biomineralization: conflicts, challenges, and opportunities". Journal of cellular biochemistry. Supplement. 30-31: 83–91. PMID 9893259.
- Sarikaya, M. (1999). "Biomimetics: Materials fabrication through biology". Proceedings of the National Academy of Sciences of the United States of America 96 (25): 14183–14185. Bibcode:1999PNAS...9614183S. doi:10.1073/pnas.96.25.14183. PMC 33939. PMID 10588672.
- Livingston, B.; Killian, C.; Wilt, F.; Cameron, A.; Landrum, M.; Ermolaeva, O.; Sapojnikov, V.; Maglott, D.; Buchanan, A.; Ettensohn, C. A. (2006). "A genome-wide analysis of biomineralization-related proteins in the sea urchin Strongylocentrotus purpuratus". Developmental biology 300 (1): 335–348. doi:10.1016/j.ydbio.2006.07.047. PMID 16987510.
- Checa, A.; Ramírez-Rico, J.; González-Segura, A.; Sánchez-Navas, A. (2009). "Nacre and false nacre (foliated aragonite) in extant monoplacophorans (=Tryblidiida: Mollusca)". Die Naturwissenschaften 96 (1): 111–122. Bibcode:2009NW.....96..111C. doi:10.1007/s00114-008-0461-1. PMID 18843476.
- Currey, J. D. (1999). "The design of mineralised hard tissues for their mechanical functions". The Journal of experimental biology 202 (Pt 23): 3285–3294. PMID 10562511.
- Gabbiani G, Tuchweber B (1963). "The role of iron in the mechanism of experimental calcification". J Histochem Cytochem 11 ((6)): 799–803. doi:10.1177/11.6.799.
- Schulz, K.; Zondervan, I.; Gerringa, L.; Timmermans, K.; Veldhuis, M.; Riebesell, U. (2004). "Effect of trace metal availability on coccolithophorid calcification.". Nature 430 (7000): 673–676. Bibcode:2004Natur.430..673S. doi:10.1038/nature02631. PMID 15295599.
- Anghileri, L. J.; Maincent, P.; Cordova-Martinez, A. (1993). "On the mechanism of soft tissue calcification induced by complexed iron". Experimental and toxicologic pathology : official journal of the Gesellschaft fur Toxikologische Pathologie 45 (5–6): 365–368. doi:10.1016/S0940-2993(11)80429-X. PMID 8312724.
- Jackson, D. J.; Wörheide, G.; Degnan, B. M. (2007). "Dynamic expression of ancient and novel molluscan shell genes during ecological transitions". BMC Evolutionary Biology 7: 160. doi:10.1186/1471-2148-7-160. PMC 2034539. PMID 17845714.
- Porter, S. (2011). "The rise of predators". Geology 39 (6): 607–608. doi:10.1130/focus062011.1.
- Cohen, P. A.; Schopf, J. W.; Butterfield, N. J.; Kudryavtsev, A. B.; MacDonald, F. A. (2011). "Phosphate biomineralization in mid-Neoproterozoic protists". Geology. doi:10.1130/G31833.1.
- Maloof, A. C.; Rose, C. V.; Beach, R.; Samuels, B. M.; Calmet, C. C.; Erwin, D. H.; Poirier, G. R.; Yao, N.; Simons, F. J. (2010). "Possible animal-body fossils in pre-Marinoan limestones from South Australia". Nature Geoscience 3 (9): 653. doi:10.1038/ngeo934.
- Zhuravlev, A. Y.; Wood, R. A. (2008). "Eve of biomineralization: Controls on skeletal mineralogy". Geology 36 (12): 923. doi:10.1130/G25094A.1.
- Porter, S. M. (Jun 2007). "Seawater chemistry and early carbonate biomineralization". Science 316 (5829): 1302–1301. Bibcode:2007Sci...316.1302P. doi:10.1126/science.1137284. ISSN 0036-8075. PMID 17540895.
- Maloof, A. C.; Porter, S. M.; Moore, J. L.; Dudas, F. O.; Bowring, S. A.; Higgins, J. A.; Fike, D. A.; Eddy, M. P. (2010). "The earliest Cambrian record of animals and ocean geochemical change". Geological Society of America Bulletin 122 (11–12): 1731–1774. doi:10.1130/B30346.1.
- Murdock, D. J. E.; Donoghue, P. C. J. (2011). "Evolutionary Origins of Animal Skeletal Biomineralization". Cells Tissues Organs 194 (2–4): 98–102. doi:10.1159/000324245. PMID 21625061.
- Kouchinsky, A.; Bengtson, S.; Runnegar, B.; Skovsted, C.; Steiner, M.; Vendrasco, M. (2011). "Chronology of early Cambrian biomineralization". Geological Magazine: 1. doi:10.1017/S0016756811000720.
- Knoll, A.H. (2004). "Biomineralization and evolutionary history". In P.M. Dove, J.J. DeYoreo and S. Weiner. Reviews in Mineralogy and Geochemistry.
- Westbroek, P.; Marin, F. (1998). "A marriage of bone and nacre.". Nature 392 (6679): 861–862. Bibcode:1998Natur.392..861W. doi:10.1038/31798. PMID 9582064.
- Jackson, D.; McDougall, C.; Woodcroft, B.; Moase, P.; Rose, R.; Kube, M.; Reinhardt, R.; Rokhsar, D.; Montagnani, C.; Joubert, C.; Piquemal, D.; Degnan, B. M. (2010). "Parallel evolution of nacre building gene sets in molluscs". Molecular Biology and Evolution 27 (3): 591–608. doi:10.1093/molbev/msp278. PMID 19915030.
- Marin, F; Smith, M; Isa, Y; Muyzer, G; Westbroek, P (1996). "Skeletal matrices, muci, and the origin of invertebrate calcification". Proceedings of the National Academy of Sciences of the United States of America 93 (4): 1554–9. Bibcode:1996PNAS...93.1554M. doi:10.1073/pnas.93.4.1554. PMC 39979. PMID 11607630.
- H. A. Lowenstam, L. Margulis, (1980). "Evolutionary prerequisites for early phanerozoic calcareous skeletons". BioSystems 12 (1–2): 27–41. doi:10.1016/0303-2647(80)90036-2. PMID 6991017.
- Lowenstam, H.; Margulis, L. (1980). "Evolutionary prerequisites for early phanerozoic calcareous skeletons". Biosystems 12 (1–2): 27–41. doi:10.1016/0303-2647(80)90036-2. PMID 6991017.
- Reyes-Bermudez, A.; Lin, Z.; Hayward, D.; Miller, D.; Ball, E. (2009). "Differential expression of three galaxin-related genes during settlement and metamorphosis in the scleractinian coral Acropora millepora". BMC Evolutionary Biology 9: 178. doi:10.1186/1471-2148-9-178. PMC 2726143. PMID 19638240.
- Jackson, D.; Macis, L.; Reitner, J.; Degnan, B.; Wörheide, G. (2007). "Sponge paleogenomics reveals an ancient role for carbonic anhydrase in skeletogenesis.". Science 316 (5833): 1893–1895. Bibcode:2007Sci...316.1893J. doi:10.1126/science.1141560. PMID 17540861.
- Kirschvink J.L. & Hagadorn, J.W. (2000). "10 A Grand Unified theory of Biomineralization.". In Bäuerlein, E.,. The Biomineralisation of Nano- and Micro-Structures,. Weinheim, Germany: Wiley-VCH. pp. 139–150.
- Towe, K.; Lowenstam, H. (1967). "Ultrastructure and development of iron mineralization in the radular teeth of Cryptochiton stelleri (mollusca)". Journal of Ultrastructure Research 17 (1): 1–13. doi:10.1016/S0022-5320(67)80015-7. PMID 6017357.
- et al (September 26, 2006). "Final report of the MEPAG Astrobiology Field Laboratory Science Steering Group (AFL-SSG)" (.doc). In Steele, Andrew; Beaty, David. The Astrobiology Field Laboratory. U.S.A.: Mars Exploration Program Analysis Group (MEPAG) - NASA. p. 72. Retrieved 2009-07-22.
- Grotzinger, John P. (January 24, 2014). "Introduction to Special Issue - Habitability, Taphonomy, and the Search for Organic Carbon on Mars". Science 343 (6169): 386–387. doi:10.1126/science.1249944. Retrieved January 24, 2014.
- Various (January 24, 2014). "Special Issue - Table of Contents - Exploring Martian Habitability". Science 343 (6169): 345–452. Retrieved January 24, 2014.
- Various (January 24, 2014). "Special Collection - Curiosity - Exploring Martian Habitability". Science. Retrieved January 24, 2014.
- Grotzinger, J.P. et al. (January 24, 2014). "A Habitable Fluvio-Lacustrine Environment at Yellowknife Bay, Gale Crater, Mars". Science 343 (6169). doi:10.1126/science.1242777. Retrieved January 24, 2014.
- Thomas, George Brinton; Komarneni, Sridhar; Parker, John (1993). Nanophase and Nanocomposite Materials: Symposium Held December 1–3, 1992, Boston, Massachusetts, U.S.A. (Materials Research Society Symposium Proceedings). Pittsburgh, Pa: Materials Research Society. ISBN 1-55899-181-6.
- Lowenstam, H. A. (13 March 1981). "Minerals Formed by Organisms". Science 211 (4487): 1126–1131. Bibcode:1981Sci...211.1126L. doi:10.1126/science.7008198. ISSN 0036-8075. JSTOR 1685216. PMID 7008198.
- Addadi, L. and S. Weiner (1992). "Control And Design Principles In Biological Mineralization" (abstract). Angewandte Chemie International Edition in English 31 (2): 153–169. doi:10.1002/anie.199201531.
- Boskey, A.L. (2003). "Biomineralization: An overview". Connective Tissue Research 44 (Supplement 1): 5–9. doi:10.1080/713713622. PMID 12952166.
- McPhee, Joseph (2006). "The Little Workers of the Mining Industry". Science Creative Quarterly (2). Retrieved 2006-11-03.
- Schmittner, Karl-Erich and Giresse, Pierre (1999). "Micro-environmental controls on biomineralization: superficial processes of apatite and calcite precipitation in Quaternary soils, Roussillon, France". Sedimentology 46 (3): 463–476. doi:10.1046/j.1365-3091.1999.00224.x.
- Weiner, S. and L. Addadi (1997). "Design strategies in mineralized biological materials". Journal of Materials Chemistry 7 (5): 689–702. doi:10.1039/a604512j. Retrieved 2006-11-03.
- Dauphin, Y. (2005). "Biomineralization". Encyclopedia of Inorganic Chemistry (R.B. King ed)., Wiley & Sons 1: 391–404. ISBN 0-521-87473-4.
- Cuif, J.P. and Sorauf, J.E. (2001). "Biomineralization and diagenesis in the Scleractinia : part I, biomineralization". Bull. Tohoku Univ. Museum, 1: 144–151.
- Dauphin, Y. (2002). "Structures, organo mineral compositions and diagenetic changes in biominerals". Current Opinion in Colloid & Interface Science 7: 133–138. doi:10.1016/S1359-0294(02)00013-4.