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Springer Handbookoƒ Marine Biotechnology Kim Editor

123 1279 58.Biomineraliz in Marine Organisms a Ille C. Gebeshuber

58.2.5 Example of This chapter describes biominerals and the ma- Mineralization in Various rine organisms that produce them. The proteins Marine Organisms...... 1290 involved in biomineralization, as well as func- 58.2.6 Example of Biomineralization tions of the biomineralized structures, are treated. of the Unstable Calcium Current and future applications of bioinspired Carbonate Polymorph Vaterite .... 1290 material synthesis in engineering and medicine highlight the enormous potential of biominer- 58.3 Materials – Proteins Controlling alization in marine organisms and the status, Biomineralization...... 1290 challenges, and prospects regarding successful 58.4 Organisms and Structures marine biotechnology. That They Biomineralize...... 1290 58.4.1 Example: Molluscan Shells ...... 1293 58.4.2 Example: Coccolithophores...... 1293 58.1 Overview ...... 1279 58.1.1 Marine Biomining ...... 1280 58.5 Functions ...... 1294 58.2 Materials – Biominerals 1281 ...... 58.6 Applications ...... 1294 58.2.1 Biominerals Produced 58.6.1 Current Applications by Simple Precipitation of Bioinspired and Oxidation Reactions 1285 ...... Material Synthesis 58.2.2 Biological Production in Engineering and Medicine ..... 1294 of Perfectly Crystallized 58.6.2 Possible Future Applications Minerals ...... 1285 of Bioinspired Material Synthesis 58.2.3 Composite Biomaterials ...... 1287 in Engineering and Medicine – 58.2.4 Example of Uptake Outlook ...... 1297 and Conversion of a Very Rare atI|58.1 | I Part Element: Selenium ...... 1289 References...... 1298

58.1 Overview

Marine biotechnology has huge potential across a broad ences is that better tools should be developed for the spectrum of applications, ranging from biomedicine use of marine biotechnology to help solve environmen- to the environment. However, marine biotechnology tal problems such as biofouling, pollution, ecosystem has not yet matured into an economically significant degradation, and hazards to human health. field [58.1]: This chapter gives a functional approach to biomin- eralization in marine organisms. It presents the ma- Fundamental knowledge is lacking in areas that terials that are biomineralized (which include sim- are pivotal to the commercialization of biomedi- ple precipitated minerals, biologically produced per- cal products and to the commercial application of fect crystals, and composites of minerals and an or- biotechnology to solve marine environmental prob- ganic matrix with interesting new properties) and lems, such as pollution, ecosystem disease, and the proteins that are important in biomineralization, harmful algal blooms. gives an overview of some of the thousands of ma- One of the recommendations of the 2002 report of rine organisms that produce such materials, including the Ocean Studies Board and the Board on Life Sci- information on the respective biomineralized struc-

[email protected] in the oceans in- 2 f metallic and radionuclide ]. ]. All kinds of microbes contribute 7 ]. 8 58.1) [58. Biomineralization is characterized by interesting Solubility controls biomineralization. Organisms The number of marine biomineralizers is vast. Biomineralization describes the formation of or- interest to biologists and also toentists, engineers, and material sci- tissue engineers. chemical reactions involving proteins,perfect crystals, the the control creation ofbition of crystal depending growth on and the crystallographic inhi- axis,the as well production as of compositethat materials are with properties ofical high fluids value are toinorganic supersaturated engineering. minerals, Many with but biolog- neously. crystals respect An do to example of not certain is such form saliva; crystal it sponta- growth is inhibition supersaturatedpatite with formation, respect to yet hydroxya- The teeth overgrowth is do prevented by not phosphoprotein macro- molecules grow that continuously. bind to enamel crystals. produce hard parts bymineral exceeding component. the Increased solubility CO of the 58.1.1 Marine Biomining Current methods ofenvironmentally mining sustainable. are, It into might focus many on be cases,such bio-assisted not interesting ways as of Fe,(Table obtaining resources Al, andactively to Ti geological phenomena, from andsuch central marine geomicrobial to many environments processesmetals and are minerals. transformations Bioremediationological of is systems the for useorganic the of pollution, clean-up bi- with ofmost bacteria organic important and and organisms fungilization, in- for being or detoxification the reclamation, o pollutants immobi- [58. creases carbonate solubility, makingalization biominer- of structures moreMany difficult. of these calciumganisms are carbonate important biomineralizing parts of or- the marine food chain. There are 128 000 speciescalcareous of green, molluscs, red, 700 and speciesspecies brown of algae, of more deep-sea than benthic 300diatom , species [58.6 and 200 000 ganized mineral structurescellular and through molecular highly processes. Exampleseralized regulated of materials are biomin- enamel (97%(70% mineral) mineral), and as well asformation takes (70% mineral). place Crystal in(requires a two high degree of steps: saturation) and crystal(requires crystal lower growth nucleation degree of saturation). cheap ]. 3 [email protected] ]. ]. 4 4 ]. 2 ]. Biomineralization has implications on the 5 In the course of biomineralization, mineral products Biominerals have functional structures and shapes, In contrast to most other biological transforma- Minerals are usually stiff, brittle, and cheap energy One of the amazing properties of biomineralization Biotechnologists, material scientists, biologists, ge- (biominerals) are created intion organisms. has Biomineraliza- been around since the firstin Prokaryota appeared the Archaean,to the 2.5 billion geological years aeon ago. from Biomineralization about is of 4 high e.g., curved teeth andtrix acts light as baskets. a The meditatormodifier. Characteristics of organic of mineralization ma- materials and produced astrolled by crystal con- biomineralization arewell-defined structures and compositions, uniform high levels of particlespatial organization, complex sizes, morphologies, controlled aggregation and texture,orientation, preferential and higher-order crystallographic assembly into hierarchical structures. tions, biomineralization leaves far-reachingthe biosphere effects and on lithosphere,, including shells, traces and such , but as alsocliffs mountain [58. ranges and global scale, via thethe Earth global sciences. It cycling isfossilization of important (paleontology elements, in and in ),chemistry, and sedimentology, in in in marine geochemistry [58. wise. Organic materials areergistic soft combination and of pliable.amazing The both syn- functionalities, yields biomineralsframe with (which with saves metabolic a energy), filledinorganic with lightweight material organic (e.g., calciuminorganic-organic hybrids carbonate), (biocomposites) yielding withdefined mechanical well- properties [58. tures and their functions,and and possible finally future presentsrial applications current of synthesis bioinspired inmedicine. mate- engineering (including mining) and in organisms is that material, structure, andstrongly function correlated. are Biominerals arein highly structure, controlled composition, shape,can and organization, yield and new,ing. more The benign approaches complexexplained in shapes with engineer- simple ofgrowth mechanistic [58. biominerals models cannot of be crystal ologists, engineers, and medical doctors have longfascinated been by mineralwith highly structures developed measurement in devices atposal, organisms. our dis- we Now, canmaterials, investigate structures, and andproduce understand processes, related bioinspired biological and analogs [58. increasingly Biomedical Applications

Part I

Part I | 58.1 1280 Biomineralization in Marine Organisms 58.2 Materials – Biominerals 1281

Table 58.1 Concentration of transition metals and zinc in eral-sulfide-oxidizing bacteria. Sulfurivirga caldicuralii seawater (after [58.11], original references after [58.12– is a microaerobic, thermophilic, thiosulfate-oxidizing 14]) chemolithoautotroph that is related to pyrite, arseni- Element Seawater (M)  108 cal pyrite, and chalcopyrite. The archaea Sulfolobus shibitae, Metallosphaera Acidianus infernus Fe 0.005–2 sp. and are related to chalcopyrite [58.18]. Zn 8.0 Cu 1.0 In low-temperature, aqueous habitats with oxygen, Mo 10.0 bacteria can affect the dissolution or precipitation Co 0.7 of minerals through their reduction or oxidation of Cr 0.4 compounds containing Mn, Fe, S, C, U, Cu, Mo, Hg, V 4.0 and Cr [58.10, p. 306]. Mn 0.7 Ni 0.5 Certain organisms are involved in the deposition of marine minerals, e.g., bacteria in deep-sea polymetal- Biomining is the use of microorganisms and plants lic nodules and coccoliths in seamount crusts [58.19]. (phytomining) to aid in the extraction and recovery of Biosynthesis and bioleaching, i. e., extraction of spe- metals from ores [58.9]. The microorganisms that grow cific metals from their ores through the use of in this aerobic, lithotrophic, and acidic environment are bacteria and further organisms, are of increasing usually chemolithoautotrophic, using reduced forms of importance. sulfur and iron, and acidophilic [58.10, p. 307]. Limestone and other fixed carbonates represent Microorganisms themselves might be very benefi- 1:8  1022 g carbon in the Earth’s lithosphere [58.20]. cial in this kind of approach or processes inspired by 40% of the Earth’s limestone deposits that were previ- biological processes that go on in biomineralizing or- ously thought to be of abiotic origin are, in fact, the con- ganisms [58.15, 16]. The usage of controlled microbial sequence of heterotrophic bacterial metabolism [58.21], cultures in order to concentrate certain minerals and which thus emphasizes the role of microbial mineraliza- ores was discussed already in 1972 [58.17]. It might tion (carbonation) in the process of locking atmospheric be worth reconsidering such ideas, with the increased and organic carbon as carbonate rocks back to the knowledge of biomineralization and environmental im- Earth’s lithosphere, a long-term carbon storage com- pact, as well as the novel methodologies that we now partment. While the precipitation of carbonate leads to have at our disposal. CO2 release in the ocean, this reaction must be consid- Bacteria that are active in marine microbial cor- ered in terms of final balance, as the buried sedimentary rosion are promising with respect to marine mining. layers of carbonate, which no longer interact with the 58.2 | I Part Acidithiobacillus ferrooxidans, for example, lives in ocean water, constitute a long-term carbon sink [58.22]. pyrite deposits, metabolizes iron and sulfur, and pro- The oceans absorb about half of the carbon dioxide duces sulfuric acid. Acidithiobacillus thiooxidans con- that is generated when burning fuels. As a conse- sumes sulfur and produces sulfuric acid. Both of these quence of this increased amount of carbon dioxide, the bacteria are already used as catalysts in bioleaching, oceans are becoming increasingly acidic, which is re- whereby metals are extracted from their ores through sulting in less calcium carbonate biomineralization and oxidation. Sulfobacillus sp. are ferrous-iron and min- a potential collapse of the marine ecosystem.

58.2 Materials – Biominerals

Many organisms build inorganic structures in var- ble with the modern methods that are now at the ious shapes and forms. The synthesis, as well as disposal of biologists. Many of the crystals and the size, morphology, composition, and location of composite materials made up of proteins and amor- these biogenic materials is genetically programmed phous inorganic parts are still unknown in cur- and controlled. Detailed investigations and descrip- rent inorganic chemistry. Nowadays we know more tions of biomineralization have only become possi- than 70 minerals that are produced by organ-

[email protected] Mytilus Tivela Aplysia , , and Tetrahymena Spiroloculina ]) and 27 leractinians, , in the radular apparatus of – 23 , 4 ous and hypercalcified , Hydrolithon onkodes Hydrolithon onkodes Codakia orbicularis sp. Rosalina leei Falcidens ), coccolithophorids, and mollusc Dental plaque Bacteria, embryos of the Mediterranean mussel Bacteria , bivalves, crustaceans, (teeth), gastropods (gizzard plates) Granules in the hymenostomatidian ciliate cyanobacteria Hypercalcified demosponges, sc molluscs, teleosteans, bryozoans, Serpulidae (tube-building annelid worms in the class Polychaeta),Ascidians algae, bacteria Sea urchin teeth (protodolomite: amagnesium crystalline carbonate calcium- with a disorderedthe lattice metallic in ions which occur ininstead the of same in crystallographic alternate layers layers as in the dolomite mineral) Vascular plants, crustaceans Tropical coralline alga teeth, embryos of the Nudibranchpunctata gastropod Marine snail shells, microbes, cyanobacteria Bacteria Vertebrates (bone/teeth precursor) bones, vertebrate teeth (enamel), brachiopods, (teeth), fish (scales), the mollusc Tropic bivalve species Linguliformea (brachiopods) Bones Bones, dental enamel, dentin galloprovincialis pyriformis Marine biomineralizers of the respective biomineral Foraminiferans (e.g., Foraminiferans, calcare calcareous spicules, octocorals, crustaceans, echinoderms, corals, bryozoans Tropical coralline alga mactroides hyaline shells, crustaceans, mammals, birds, corals,atha, Archaeocy- bryozoans, echinoderms (brittle star,fish,sanddollars,seacucumbers...),Serpulidae(tube- sea urchin, star building annelid worms in thecyanobacteria, class sponges, Polychaeta), algae barnacles, 14 / 4 3 O PO 2 . 2 O / 6H 2 OH/ 2  . F C  3 3 2 / 3 O O 3 8H / / 4 / 2 2 2  3 3 4 6 Fe [email protected] 2 2 OH/ ; F / 2 / / OorCaCO O . 6 CO 4 / 2H 2 3 2 3 2H 2 / x PO CO CO 4   / ; ; /.PO 4 H H Mg  7 3 4 4 4 4   . PO 1 CO CO 3 . 2 PO O 3 3 3 3 3 . . 3 PO 3 2 . 2 . H PO PO CO OHj. Ca NH P . . H Œ . x . C 2 10 5 5 18 8 5 3 3 2 Ca CaHPO Ca Ca Ca Ca Mg Fe Variable Pb CaCO CaMg SrCO FeCO Ca Ca Mg MgCO CaCO CaCO CaCO CaMg Chemical formula CaCO Non-exhaustive list of biominerals produced by marine organisms (after [58. Vivianite Amorphous calcium (at least six forms) Amorphous calcium pyrophosphate Francolite Carbonated Carbonated apatite (dahlite, dahllite) Whitlockite Struvite Octacalcium phosphate Hydroxyapatite Brushite Amorphous calcium carbonate (at least five forms) Dolomite Strontianite Siderite Vaterite Monohydrocalcite Protodolomite Hydrocerussite Magnesite Mg-calcite Biomineral Carbonates Table 58.2 Biomedical Applications

Part I

Part I | 58.2 1282 Biomineralization in Marine Organisms 58.2 Materials – Biominerals 1283

Table 58.2 (continued) Biomineral Chemical formula Marine biomineralizers of the respective biomineral Oxides and hydroxides

Magnetite Fe3O4 Eubacteria, Archaebacteria, teleosteans, polyplacophorans (chitons) C2 Amorphous ilmenite Fe TiO3 Foraminifera, snail radulae Maghemite -Fe2O3 Amorphous iron oxide Fe2O3 In the radular apparatus of the mollusc Falcidens sp. Amorphous manganese oxide Mn3O4 Bacteria Manganese(III) oxohydroxide MnOOH Bacterial spores of the marine Bacillus,strainSG-1 Goethite ˛-FeOOH Gastropods, teeth, marine sponges Akaganeite ˇ-FeOOH Bacteria Lepidocrocite -FeOOH Polyplacophorans (chitons), marine sponges 3C Ferrihydrite .Fe /2O3  0:5H2O Lamprey Geotria australis, chitons, snails Todorokite .Na;Ca;K;Ba;Sr/1x.Mn;Mg;Al/6O12 Hydrothermal vent microbes 34H2O 4C 3C Birnessite .Na0:3Ca0:1K0:1/.Mn ;Mn /2O4 Microbes 1:5H2O Sulfates

Gypsum CaSO4  2H2O Cnidarians, statoliths of certain medusae, Desmidae (algae), cyanobacteria

Bassanite CaSO4  0:5H2O Statoliths of certain medusae Barite BaSO4 Cyanobacteria, Spirogyra (alga), Loxididae (), Chara fragilis (higher alga), (large deep-sea protists), , foraminifera, Loxodes (gravity receptor)

Celestite SrSO4 Radiolarians, Acantharia, algae, foraminifera Rosalina leei and Spiroloculina hyaline,snailshell 3C. / . / Jarosite KFe3 SO4 2 OH 6 Purpureocillium lilacinum (an acidophilic ), Acidithiobacillus ferroxidans Sulfides atI|58.2 | I Part Pyrite FeS2 Magnetotactic bacteria Amorphous pyrrhotite Fe.1x/S(x D 0to0.2) Hydrotroilite FeS  nH2O Sulphate-reducing bacteria, Desulfovibrio spp. Sphalerite (Zn,Fe)S Magnetotactic bacteria Galena PbS Sulfate reducing bacteria

Greigite Fe3S4 Magnetotactic bacteria Mackinawite .Fe;Ni/1CxS(x D 0to0.11) Wurtzite (Zn,Fe)S Cadmium sulfide CdS nanoparticles Marine cyanobacterium Phormidium tenue

Acanthite Ag2S Polychaete worm Pomatoceros triqueter Arsenates

Orpiment As2S3 Bacteria Native elements Sulfur S nanoparticles Gold Au nanoparticles Tropical marine yeast Yarrowia lipolytica, marine sponge Acanthella elongate, marine alga Sargassum wightii Silver Ag nanoparticles Marine fungus Penicillium fellutanum, Fusarium oxyspo- rum (a fungus that is reported to infect marine mammals)

[email protected] , ,Pb,Sr,and Pseudomonas spiders (silver color) and Glycera dibranchiata , a bacterium that builds , p. 25]. Some bacteria 23 Scaphander cylindrellus Tetragnatha (bacterium); reduction of Ura- (turtle grass), sea grass, vascular , molluscs (sea slug) spicules Sulfurospirillum barnesii Desulfovibrio vulgaris Vertebrate and invertebrate , fishshell, skin, gizzard mollusc plates of gastropods,mysid statoliths crustaceans of marine Gravity receptors Archidoris Jaws of the marine bloodworm Thalassia testudinum plants, Bornetella (marine alga) ,of gizzard the plates deep water gastropod renal sac of the ascidianMogula tunicate manhattensis (marine filter feeder) Fish scales (fish silver), Marine biomineralizers of the respective biomineral Bacteria Shewanella oneidensis nium by marine aerobic biofilms Radiolarians, diatoms, demosponges, hexactinellid sponges, most sponge spicules, Opaland teeth , in mollusc copepods penial structures,and heliozoan scales spines Microorganisms (?) marina Biomineralized products comprise metals and al- Ni loys, ceramics, polymers,areBa,Ca,Cu,Fe,K,Mn,Mg,Na, and composites. Examples Zn; as hydroxides, oxides, andbonates, sulfates or and sulfides, phosphates car- [58. DNA O / 2 O / 2 6H /  O H O 2 . 2 2 4 O  H O . 2 [email protected] / :4H 2 O OH/ 2 7 0 2 . Na   2H O Cl O 3 3 6 5 / 2H H  15 / 2 3 ) 5 4   O O O (one of the four main nucle- 2 O 4 4 O H H 4 4 5 4 4 4 O 6 O n C 6 6 O 2 N N CaO N O O H n 2  2 OH/ C 4 2 3 4 5 Si 2 2 4 C RNA 2 2 . . 2 C 4 . SiF 2 . H H H H H 3 58.2). Biomineralization 2 5 n 5 4 5 C C organic compounds that characteristi- cally consist of long alkyl chains Mg Cu C CaC CaC MnC CaC C Ca C SiO Mg CaF K CaF Cu Chemical formula Se nanoparticles U nanoparticles and obases found in the nucleic acids Continued Magnesium oxalate (glushin- skite) Copper oxalate (moolooite) Anhydrous ferric oxalate Sodium urate Earlandite Guanine Uric acid Paraffin hydrocarbon Wax Whewellite Manganese oxalate Calcium tartrate Calcium malate Hieratite Amorphous fluorite Atacamite Organic minerals Weddellite Sepiolite Halides Fluorite Selenium Uranium Silica (opal) Biomineral Native Elements isms in various ways (Table Table 58.2 takes placeboth at much normal lowersame temperatures mineralized than and structures by thosesynthesis. pressures, conventional required chemical to form the Biomedical Applications

Part I

Part I | 58.2 1284 Biomineralization in Marine Organisms 58.2 Materials – Biominerals 1285

(e.g., from the species Geobacter and Citrobacter) ac- in a variety of different aquatic habitats. It uses the en- 2C cumulate and passivate toxic metal ions, such as UO2 , ergy it obtains from oxidization, remains of its activities Pb2C,andCd2C. Bacteria have learnt to cope with most are drains clogged with iron depositions, iron(III)-oxide elements of the periodic table, e.g., with encoded resis- (Fe2O3) and iron(III) oxide-hydroxide (HFeO2). This tance systems for toxic metal ions. For many chemical bacterium or some of its biochemicals related to the elements, bacteria have found uses either in ultralow oxidization of iron might be of high interest for an al- concentrations in functional biomolecules (e.g., vana- ternative way of mining iron in the sea. dium), or in vast amounts (e.g., calcium for the forma- tion of shells) [58.28]. Gold, silver, uranium, palladium Manganese Dioxide MnO2 and CdS nanocrystals are produced by various organ- Manganese(IV)-oxide (MnO2) is precipitated via mi- isms [58.29], Chaps. 25 and 55. The size of nanocrys- croorganisms such as Leptothrix discophora [58.32]. tals strongly determines fundamental properties such The sheaths of the organisms of the Sphaerotilus- as their color or the external field required to switch Leptothrix group often are coated with Fe.OH/3 or a magnetized particle in hard disk drives. The perfect MnO2 [58.33]. control of the size of the biomineralized nanocrystals The Mn and Fe oxidizing/depositing bacteria in is one major reason why bioassisted nanocrystal pro- freshwater habitats belong to the genera Sphaerotilus, duction is widely viewed as highly promising regarding Gallionella,andLeptothrix [58.34, 35]. base materials for new man-made optical and electrical In marine environments, the direct evidence for Fe- materials. Zinc (Zn) is present in the jaws of the ma- oxidizing bacteria is not well documented. The one rine worm Nereis sp. [58.30], and copper (in the form notable exception was the finding of abundant Gal- of the biomineral atacamite, Cu .OH/ Cl) is present in 2 3 lionella-like stalk material and microscopic identifi- the jaws of the marine bloodworm Glycera dibranchi- cation of putative G. ferruginea cells from a shallow ate [58.31]. The metals reinforce protein fibres in worm water volcanic system near Santorini Island in the jaws. Mediterranean Sea. [58.36] The three different types of biominerals are either produced by simple precipitation, as perfect crystals,or Pyrite and Marcasite FeS as composites. 2 Sulfate reducing bacteria gain energy from the reduc- tion of sulfates. When iron(II) ions are present, FeS 58.2.1 Biominerals Produced 2 can be produced, by Simple Precipitation and Oxidation Reactions 2 C : C C C 2C 2SO4 3 5C 2H Fe Calcium carbonate, iron(III)-oxide hydrate (FeOOH), ! FeS2 C 3:5CO2 C H2O 58.2 | I Part manganese(IV)-oxide (MnO2), and pyrite, as well as marcasite (both FeS2) are generated in organisms by (the C comes from organic substances). precipitation and oxidation reactions, i. e., relatively simple reactions in which solved substances are trans- 58.2.2 Biological Production lated into insoluble ones via the metabolism of or- of Perfectly Crystallized Minerals ganisms. Example: CaCO2 in stromatolites that were built by autotrophic cyanobacteria as far back in time Ice H2O as 3:5 billion years ago. Ice is a mineral with a relatively low melting point. Organisms actively protect themselves against this un- Calcium Carbonate CaCO3 wanted mineral in their bodies via two strategies: either 2C C  ! [Ca 2HCO3 ] (carbonate) CaCO3 (stromato- they prevent freezing of their bodily fluids via freeze lite) C CO2 (insertion to the biomass) C H2O. protection proteins (Sect. 58.3) or they enrich ice nucle- The advantage for the cyanobacteria might be me- ation proteins in their blood, which promote and control chanical fixation of the biofilm in water. freezing so that their cells do not suffer. Some bacteria such as Pseudomonas syringae produce proteins that Iron(III)-Oxide-Hydroxide FeOOH Goethite promote freezing; they are used for the production of Gallionella ferruginea is a chemoautotrophic iron-oxi- artificial snow. Various organisms such as arctic fish, dizing chemolithotrophic bacterium that has been found plants, fungi, microorganisms, and bacteria build an-

[email protected] . 111 110 100 111 111 Magneto- 100 200 nm 001 111 101 ) b ( Elongated 111 001 {100}+{111} 111 111 010 111 010 111 111 100 110 ], with permission) 101 38 011 100 101 111 Elongated 001 {100}+{111} 001 111 111 010 010 110 Magnetospirillum magnetotacticum 111 111 111 110 111 101 A magnetotactic bacterium. 100 ) a ( 111 111 101 111 001 011 58.2), e.g., 58.3). Biogenic magnetite in the human brain may {100}+{111} {110}+{111} {110}+{111}+{100} {110}+{111}+{100} Cuboctohadron The formation of bacterial magnetite crystals is as 010 110 111 a) b) some crystal morphology.with atomic The precision (after [58. are built Fig. 58.2 (Fig. The anaerobic bacterium uses theself magnets along to orient the it- thereby magnetic determine field up and linesgravity, down of because (it the cannot as doat Earth, a this a and via small lowhoney bacterium Reynold’s – it number, which lives likenetosomes is a a were no life also piece way foundand of to in salmon. dust rely migratory Magnetite in on birds,cision particles trout, gravity). have with Mag- even molecular(Fig. been pre- identified in the human brain account for thein high-field magnetic saturation resonance effects imaging and, observed riety perhaps, of for a biological va- fields. effects of low-frequency magnetic follows: first, thethe environment. bacterium Then takes itduring reduces Fe(III) Fe(III) the ions to transport Fe(II) from across ions the cell membrane. Sub- 6584 : [email protected] Ophioma wentii ]. 37 3 4 O 58.1). 3 m  ]. 39 The calcite microlenses of the brittle star. Each 4864 (depending on the crystallographic axis). : Calcium Carbonate CaCO (Calcite, Aragonite, and Vaterite) Already 350 millions of years ago some trilobite Magnetite Fe Antifreeze proteins bind to ice crystals and prevent Calcite is the most stable polymorph ofate. calcium carbon- It is transparent, with a refractive index of 1 and 1 These properties make it a good materialtion for the of produc- optical lenses.has The calcite brittle eyes star ofover its optically body (Fig. corrected microlenses all species used calcite lenses; upup to one 15 single 000 eye! lenses Calciumthe carbonate making is ear: also zebra present fish in alize use aragonite Starmaker proteins for tosense hearing biominer- [58. and their vestibular of the lenses is onlyScale some bar tens of 100 micrometers in diameter. Fig. 58.1 Magnetite is a ferromagnetic blacke.g., iron be oxide found that can, ingle magnetic a chain crystals in of magnetotactic magnetosomes, bacteria i. e., sin- tifreeze and ice structuringthese proteins. proteins, With the the organismstures help below can the of survive freezing point in of tempera- water. their growth andthe recrystallization, cells thereby of the preventing crystals. organisms Due from to being their destroyedproteins ice by in binding ice properties, living antifreeze naturetions work (300–500 times at less very thanantifreeze conventional low man-made concentra- agents). Frost-tolerantfreezing of species their body survive fluids [58. the Biomedical Applications

Part I

Part I | 58.2 1286 Biomineralization in Marine Organisms 58.2 Materials – Biominerals 1287

{111} {022}

Fig. 58.4 Pearls 10 nm

Fig. 58.3 A magnetite particle from the human brain (af- layer organic layer • Aragonite polygonal ter [58.42], with permission) (conchiolin) on a pearl tablets (500 nm thick) • Protein/polysaccharide sequently, Fe(II) ions are transported to and across organic matrix the vesicle membrane (the membrane), (30 nm thick) amorphous hydrated Fe(III) oxide is precipitated within CaCO3 the vesicle, and the amorphous phase is transformed to (aragonite crystals) magnetite by surface reactions involving mixed-valence Fig. 58.5 Nacre layer on a pearl. The conchiolin pro- intermediates [58.40, 41]. tein/polysaccharide matrix is about 30 nm thick, the aragonite polygonal tablets are about 500 nm thick. The 58.2.3 Composite Biomaterials beautiful luster of the pearl comes from optical inter- ference effects of light on the thin tablets. Permission Composite materials combine two or more materi- pending als yielding new materials with interesting properties. 58.2 | I Part Many biomaterials are composites. In most cases, the organisms yielded whole mountain ranges. The calcium functionality of the biological composites is based on carbonate shell serves as mechanical protection for the nanoscale structures. Examples for such nanocompos- soft bodies of the organisms, be they foraminifers, other ites (also known as hybrid biomaterials) are nacre (the single-celled organisms, mussels, molluscs, or other beautifully iridescent layer in, e.g., abalone shells or animals. pearls, Figs. 58.4 and 58.5), bones and enamel, as Nacre is an iridescent form of aragonite (which is well as egg or mollusc shells. In many cases, the a calcium carbonate with orthorhombic symmetry as mechanical properties of such nanocomposites are out- opposed to the trigonal symmetry in calcite) that is standing: abalone nacre, for example, has a fracture made by certain marine animals. Its protein content is toughness that is 3000 times higher than that of calcite about 5%. crystals [58.43]. Sea urchins biomineralize calcium carbonate in their shells, teeth, and spines. Sea urchin spines can Calcium Carbonate CaCO3 Nanocomposites reach a length of 10 cm, with their toughness by far Calcium carbonate is an important ingredient in outnumbering the toughness of pure calcium carbonate. the nanocomposite that makes up the shells of Sea urchin teeth are single crystal calcites [58.45]. foraminifers [58.44], eggs of birds and mollusc shells. In corals, sensitive little animals (polyps) biomin- Calcium carbonate is the material that is biomineralized eralize with the help of algae, with whom they most: remnants of calcium carbonate biomineralizing live in symbiosis, an of calcium carbon-

[email protected] Monorhaphis ,someinstar ) b ( ]. Glass sponges are exclu- 58.7). One single species can , some ball-like m ) 50 a  ( Hexactinellida (glass sponge) spicules. Glass produces a silica needle of up to 3 m in length and a) b) Glass sponges are an important ecological factor in A second type of marine organisms that biominer- sponges consist of aa network thin of such layer spicules ofdefended covered living both by inside cells. and Inup to out. this 20 different Single way types glass of theyof spicules sponges are them in have various needle heavily shapes, like some shapes. Scale bars 10 Fig. 58.7a,b sively marine organisms; theyall comprise sponges about currently 7%from known. of amorphous Their hydrated skeleton silicaexquisite is needles shapes made (spicules) (Fig. of have up to 20 differentchuni types of needles. 8 mm in diameter, whichbottom it of uses the to Indian stabilize and itself Pacific at oceans. the the Antarctic; spicules of dead animalslayers can up build to woolly 2 m high.tric The layers single spicules of have concen- silica,canal. arranged The around spicules a areand hollow proteins a central and composite are in material many of cases highly silica elastic. remnant shellsnanostructured of shell of diatoms. the ,has Because diatomaceous huge earth surface area of and is, therefore,drinks the used such for filtering as porous beer andtion of apple explosives juice, such or as dynamite. for the produc- alize silica are the(Hexactinellida) about 500 [58. species of glass sponges , 3 47 from ) [58. ]. These ex- 2 [email protected] 46 MEMS and aid in CaCO 2 Solium exsculptum neralizing phytosynthetic b) is a zoom into the most left junction in ) a ( 58.6). Diatoms can serve as inspiring natural 58.6). Sometimes, single diatom cells are con- Diatoms are silica biomi Proteins that are involved in the biomineraliza- is a natural resource that is in Diatoms and Glass Sponges Nanostructured SiO ]. . The sample is from the Hustedt Collection in Bremer- tion of silica areSilicateins called silicatein, are silaffinstrengthen high and the silicase. silica molecular structure; silaffinslar weight are weight low molecu- proteins proteins that yieldminutes. that silica precipitation within mined in various places on the Earth. It contains the 48 Diatoms are unicellularsaltwater and algae on thattemperature and moist pressure live biomineralize surfaces, an in exoskeleton of and fresh that rigid, at or tough,oskeletons are normal and nanostructured and hard(Fig. of silica exquisite beauty [58. nected via hinges andvices. mechanical Such interconnecting linkages have de- eral a hundreds size on ofdiatoms the have nanometers. order ever of No beenfossilized sev- reported, signs not and even of were whenearlier wear they (as alive in is tensin the of Fig. case millions formicrosystems of the when years fossil itchanical diatom aspects comes of depicted microengineered to devices, especially 3D tribological microelectromechanical or systems me- ( ate. The algaeprecipitation. consume the CO ) Biomedical Applications b (

a) Part I haven, Germany, #haven). E1761 Image reproduced (Courtesy with kind of permission F. Hinz, AWI Bremer- single-celled organisms. The fossil diatom the island of Mors inlions Denmark of depicted years in ago. the It image beautifullyshell, lived shows 45 an reinforcement mil- expedient nanostructured ribs,structures. connections, Panel and primary mechanical Fig. 58.6a,b panel

Part I | 58.2 1288 Biomineralization in Marine Organisms 58.2 Materials – Biominerals 1289

Hydroxyapatite Ca5[OH|(PO4)3] like arrangement. See Fig. 58.8 foradrawingofthe Animal bones consist of about 65% inorganic com- seven layers of hierarchy in bone. ponents, mainly hydroxyapatite (a calcium phosphate with the chemical formula Ca5ŒOHj.PO4/3), providing Fluorapatite Ca5(PO4)3F compressive strength, and about 35% inorganic compo- Enamel has 95% inorganic components, mainly hy- nents, mainly , providing high tensile strength. droxyapatite. In fluorapatite the OH group is replaced Further ingredients in bones are proteins and fats. The with F – this makes enamel more resistant against acids high strength of bone is due to the fact that hydroxy- and provides a better protection against caries. apatite crystals are ordered mainly along the lines of tension and compressive stress, which results in a strut- 58.2.4 Example of Uptake and Conversion of a Very Rare Element: Selenium Structure Spongy bone In 1983, Foda et al. [58.51] described uptake and con- version of the very rare element selenium by the Bone tissue marine bacterium Pseudomonas marina in seawater –50 cm Macro containing either selenite or selenate. Pseudomonas Compact bone marina bioconverts selenite into water-soluble non- Se(IV) metabolite(s) and subsequently releases them back into the medium. It is also capable of reducing Se(IV) to elemental Se; this pathway becomes increas- and ingly evident at higher concentrations of selenite. Haversian canals In 2011, selenium-reducing microorganisms that –100 mm produce elemental selenium nanoparticles were re- ported [58.52]. This study identified high-affinity pro- teins associated with such bionanominerals and with non-biogenic elemental selenium. Proteins with an an- ticipated functional role in selenium reduction, such as a metalloid reductase, were found to be associated Fiber patterns

–50 mm Micro atI|58.2 | I Part Fibril arrays –10 mm

Mineralized collagen fibrils –1 mm

Tropocollagen –300 nm

Amino acids –1 nm Nano

Fig. 58.8 The hierarchical levels of bone, a biomineral- ized structure with added functionality on each level of Fig. 58.9 An exoskeleton. These planktonic, hierarchy, resulting in a tough and strong, yet lightweight free living, exclusively marine protozoa range in size from material [58.49], with permission 0:055 mm in diameter

[email protected] , ]). 23 ]. ],andingastro- 23 55 58.9). 2 nm diameter, they have the  ]. 5 58 gives a non-exhaustive list of the pro- 5mm(Fig. ], in turtle eggshells [58. 05 54 : 58.3 of the Unstable CalciumPolymorph Carbonate Vaterite Table The three main organic structuring and scaffolding Certain proteins provide active organic matrices that Many biomineralized structures are built from In those circumstances, impurities suchorganic as metal matter ions may or stabilize thetransformation vaterite into and calcite prevent its or aragonite. pod (e.g., snail, abalone, limpet) shells (e.g.,56 [58. 58.2.6 Example of Biomineralization Vaterite is a polymorph of calcium carbonatestable and is than less calciterally or in aragonite. some Vaterite organisms,quirts such occurs [58. as natu- in the spicules of sea tance for strontium circles inbetween 0 the sea. Their sizes range eralized material andseem structures. to andbiomineralization. be collagen universal and alternativeteins templates involved in in biomineralizationbiomineralized material. and the respective polymers are chitin, cellulose,have and common collagen. All principlesform three nanofibrils in with 1: their organization: they ferent structures, materials,is processes, tremendous: 128 and 000 species functions, described, of 700 molluscs have species been brown of algae, calcareous more green, thanthic red, foraminifera, 300 and and species 200 000 of diatoms deep-sea species ben- [58. ability to self-assemble, they produce fibrillarlike and fiber- structures with hierarchicalnanolevel up organization to from macrolevels, they the haveas the scaffolds ability and to as act templatesthey for form biomineralization, rigid and skeletal structures [58. control the formation of specific mineral structures; oth- ers act as catalystscertain that metal ions facilitate [58. the crystallization of p. 26]. nanostructured, hierarchical materials,even and functional sometimes gradient materials. Bone, for example, 58.2 ], and in 53 [58. [email protected] ) and strontianite 4 ]. Proteins have sev- 57 . Spiroloculina hyaline and in Various Marine Organisms ). These two minerals also occur as biominer- 3 58.4); some specific crystals produced by living Acantharea are one of the four types of large amoe- Proteins ultimately contribute to the extraordinary als in radiolarians, acantharia,Rosalina algae, leei the foraminiferae snail shells. bae that occur in thehave marine a water very column. regular Acantharea exoskeleton and are of high impor- and 58.4 Organisms and Structures That TheyMarine vertebrates, Biomineralize invertebrates, andalize plants biominer- more than 70 different substances (Tables eral important activeinhibit roles spontaneous in mineral biomineralization:(e.g., formation they the from protein statherin solution taneous in precipitation the of mouth inhibits calciumhibit spon- phosphate), the they growth in- responsible for directing of crystal nucleation, phase, existing mor- phology, and crystals, growth and dynamics.for The they example, crystal affected are shapetures by is, proteins and withof specific sequences struc- the that crystal,tal adsorb leading faces to to haveatoms regulation different different of charges so faces shape and proteinsmore, (crys- arrangements proteins can of can selectivelythat self-assemble adsorb). guide into Further- orderedstructures. the arrays formation of organizedmechanical, mineralized optical, etc., properties of the biomin- 58.3 Materials – ProteinsWe Controlling are Biomineralization just beginningteins to in understand biomineralization the [58. role of pro- Strontium is an alkalinerally in earth the metal minerals that occurs (SrSO natu- with nanoparticles formedSulfurospirillum by barnesii one selenium respirer, 58.2.5 Example of Strontium Mineralization (SrSO nature cannot becal produced synthesis by (e.g.,magnetotactic bacteria conventional the or some chemi- defect-free crystalviously classes magnetosomes need that proteins ob- in forexist their in build-up geological – crystal they formations).marine biomineralizers, The do and number with not them of the range of dif- Biomedical Applications

Part I

Part I | 58.4 1290 Biomineralization in Marine Organisms 58.4 Organisms and Structures That They Biomineralize 1291

Table 58.3 Biominerals and the respective proteins involved in biomineralization (non-exhaustive list) Biomineral Proteins Apatite Collagen (controls apatite) (in Porifera, coelenterates, molluscs, echinoderms) Bone Biglycan (a small leucine-rich repeat proteoglycan (SLRP) found in a variety of extracellular matrix tissues, including bone, , and ; essential for the structure and function of mineralized tissue) (a bone-specific protein linking mineral to collagen) (an extracellular structural protein and, therefore, an organic component of bone) Sialoprotein (BSP) (a component of mineralized tissues such as bone, dentin, cementum, and calcified cartilage) , phosphophoryn, , proteoglycans, glycoproteins, glycosaminoglycans CdS nanoparticles C-phycoerythrin (from the marine cyanobacterium Phormidium tenue) Calcium carbonate Calcified cartilage sialoprotein (BSP) (a component of mineralized tissues such as bone, dentin, cementum, and calcified cartilage) Orchestin (a calcium-binding phosphoprotein in the calcified cuticle of a crustacean) Snail shells conchiolin (conchin) Calmodulin-like protein (from pearl oyster Pinctada fucata) Eggshell matrix proteins Otoconin (in octoconia, small crystals of calcium carbonate, also called statoconia, as gravity and acceleration sensors) Statherin (growth inhibiting protein, inhibits spontaneous precipitation of calcium phosphate in the mouth) Pancreatic stone protein (PSP) inhibits calcium carbonate precipitation in pancreatic fluid Starmaker proteins (in zebrafish, aragonite biomineralization) Calcium phosphate Serum protein fetuin-A (inhibition of calcium phosphate precipitation, inhibiting smooth muscle cell calcification) Dentin Dentin sialoprotein (BSP) (a component of mineralized tissues such as bone, dentin, cementum, and calcified cartilage) Enamel Amelogenin (a series of closely related proteins involved in amelogenesis, the development of Tuftelin) Enamelin and amelogenin ( proteins) atI|58.4 | I Part Tuftelin (enamel) Transcription factor FoxO1 (essential for enamel biomineralization) Phosphoprotein (inhibits hydroxyapatite formation) Goethite Chitin (in limpet teeth, as template for goethite growth) Gold Cytochrome C Lysosome Ice Antifreeze proteins (control of ice crystal growth) Ice interaction polypeptides Magnetite MamA (required for the activation of magnetosome vesicles) MamJ (directs the assembly and localization of magnetosomes) Mms6 (regulates magnetite crystal morphology) Nacre Nacre proteins (perlucin, n16N,...) Silica Polyamines, silicatein and silaffine (in diatoms) Frustulin, pleuralin (in diatoms) Uranium Cytochrome c3 (reduction of uranium, from Desulfovibrio vulgaris) Vaterite Eggshell pelovaterin (turtle eggshells, vaterite crystals)

[email protected] vs. 58.9). ) Astrosclera Calcifibrospongia Petrobiona massiliana (Astroscleridae), (amorphous hydrated silica) Magnetospirillum magneticum , (iron, sulfur, uranium) / 3 (Ceratoporellidae: Porifera), Nature’s nanostructures are built by benign chem- CaCO On level 5 the osteons, cylindricalture, motifs in appear. bone Level struc- 6integrated brings into in the ascompact whole added bone, and functionality, bone level 7 is structure, the whole spongy bone (Fig. istry and viachemical synthesis self-assembly is slowly reaching and the efficiency templating. and Human . Goreauiella auriculata , Euplectella aspergillum Acidianus infernus / 3 tooth (up to 9 feet long) sp., / 3 Stromatospongia norae , / CaCO . 3 / [email protected] 3 ) Magnetospirillum gryphiswaldense CaCO 4 . ) 3 CaCO , Selenium nanoparticles) / Ceratoporella nicholsoni . ) CaCO 3 3 SrSO . 3 / (turtle grass), sea grass, vascular plants Pinctada fucata ; 3 3 Metallosphaera , CaCO . Monodon monoceros / CaCO 3 . Hispidopetra miniana , CaCO . Magnetotactic bacteria (e.g., Cynobacteria in stromatolithes Marine bacteria (CaCO Sulfolobus shibitae (Calcarea, Calcaronea), Coccolithophores (CaCO Diatoms, radiolarians and silicoflagellates (hydratedForaminifera silica) (CaCO Fungi in corals (pearl-like skeletons) Chemosynthetic marine organisms Shells, snail shell (strontium, calcium) Rhopaliophoran medusae (Cnidaria) statoliths (calciumDemosponges sulfate (silica) hemihydrate) Brittle star crystal eyes (Calcite) Most sponge spicules (silica) Hypercalcified sponge (calcium carbonate basal skeleton in addition to their spicules) Lanternshark (mineralized spines) such as the Giant PacificSea octopus urchins (beak) (needles, larval skeleton) Fanworms (Serpulidae) Vertebrate bone (apatite (phosphate carbonate)) Whale teeth Narwhal whale Enamel (vertebrate teeth) (apatite (phosphate carbonate)) Echinoderms Corals Glass sponges such as the Venus flower basket Crystal structures in the inner earJapanese in pearl zebrafish oyster Avian egg shell Archaeocyatha (CaCO Brachiopod and mollusc shells Sea-mats (Bryozoans) Calcareous sponge spicules Calcareous tunicate (marine filter feeders)Conodonts spicules (apatite (phosphate carbonate)) Examples Thalassia testudinum willeyana actinostromarioides Examples for biomineralizing organisms in all six biological kingdoms Archaea Protista Fungi Bacteria Animals Plants has seven layers of hierarchy,ponents spanning of from collagen the fibrils com- consists to of the the whole components bone. themselves,line Level including and 1 pro- hydroxyproline.size, On in level hierarchy, and 2, withthe one added mineralized step functionality, collagen. comes upof On in fibers, level which 3 on there level 4 are build arrays patterns, e.g., spirals. Table 58.4 Biomedical Applications

Part I

Part I | 58.4 1292 Biomineralization in Marine Organisms 58.4 Organisms and Structures That They Biomineralize 1293

Fig. 58.10a,b Concept for a self-repairing adhesive a) b) Force (nN) [58.43]. (a) Two ways to attach two particles: with a long molecule or with a long molecule with nodules. (b) When short molecule long molecule stretched, a short molecule can only be extended a little 1 and would then break. A long molecule would be stretched long molecule with modules much more and finally break. However, a long molecule with nodules, with sacrificial bonds that break before the backbone of the molecule breaks, increases the toughness of the adhesive. Such a strategy is applied in the abalone long molecule 0 shell and also in diatom adhesives (after [58.43], with per- long molecule 0 50 100 mission) I with modules Extension (nm) purity of natural biomineralized crystals, and in terms of controlling morphology and hierarchy, there is still a) a lot for us to learn [58.59]. From nanometer small crystals that serve as nucle- ation centers up to meter-long silica spicules in certain marine glass sponges – biomineralized structures span many orders of magnitude in length.

58.4.1 Example: Molluscan Shells

The main material in molluscan shells is calcium car- bonate: it amounts to about 9599% of the weight. The remaining 15% are made up of proteins. The b) complex biocomposite (Fig. 58.10) of molluscan shells is far more fracture resistant than a calcite crystal: in the case of the abalone shell, this factor amounts to 3000 [58.43]. The proteins controlling the biominer- alization (for an overview, see Sect. 58.3) allow for calcium carbonate (and/or strontianite, celestite, and

fluorite, see Sect. 58.2) synthesis at ambient conditions, 58.5 | I Part and control the crystal nucleation, phase, morphology, and growth dynamics. The abalone shell is an exam- ple of a biomineralized material with high fracture toughness. The blue-rayed limpet Ansates pellucida has Fig. 58.11a,b The coccolithophorid Rhabdosphaera clav- a shell that shows stripes of green-blue dynamic struc- igera. (a) Whole organism. (b) Detail of the tip of a single tural coloration (photonic structures). It exerts different spine showing spiral structure formed from consistently control over the calcium carbonate crystal phases in dif- aligned crystal units with rhombic faces (after [58.61], per- ferent parts of its shell, utilizing different proteins and mission pending) making different structures. Several phases of CaCO3 can exist locally next to each other, each containing its 110 m. These microscopic organisms control the characteristic proteins [58.60]. nucleation as well as the growth of the plates. Coc- colithophores form a significant proportion of total 58.4.2 Example: Coccolithophores marine primary production and carbon fixation; the biomineralized structures of dead coccolithophores Coccolithophores (Fig. 58.11) are small unicellular are the largest single component of deep-sea sedi- photosynthesizing protists that produce exoskele- ments and they also make up the white cliffs of tons of elaborate calcite plates with a size of about Dover [58.61, 62].

[email protected] 58.12). An- ]. 48 , 47 elemental composition of ]. and contain, for example, the 65 58.5 screen [58. UV can be envisaged [58. 58.12). Potential future marine biotechnology The abundance and distribution of chemical ele- Examples of functions of biomineralized structures ments in seawater is ativity, function and of involvement their in solubility, biotic reac- as and well abiotic processes, asthe oceanic composition circulation; of the it human shows body similarity (Fig. to imals have afour similar most composition; abundant elements inple are plants or the animals the sameabundant (O, as first element in C, is peo- H, P.the The and cell N), phone but (whichtation shall the of serve fifth a here(Fig. most as technical a device) represen- might is provide completely materials andnologies different that structures are for less newFor focused tech- each on plastics suchful and marine considerations metals. regarding biotechnology the attempt, potential care- benefit of calcite cell wallused scales as in exoskeleton, the coccolithophoridsand calcite that molluscs, shells are the of aragonite foraminifera corals, cell aragonite walls of molluscpod scleractinian shells, (e.g., and snail,used vaterite abalone, for gastro- limpet) optical(it shells. imaging constituted in Calcite their the was cal now eye strength extinct lens), to trilobites the and cuticleeggshells provides of it provides crustaceans, mechani- mechanical e.g., protection. crabs.provides Mg-calcite In mechanical strength to therals, spicules and of strength octoco- as wellspines as of protection echinoderms to (marine the invertebratesfeet shell with and and tube five-part radially symmetricalsea bodies, stars such and as seapoison urchins). dart in Chitin certain marine is gastropods. the Aragonite pro- vides material buoyancy of devices the inshells, as (e.g., well octopus) terite as spicules gravity provide receptors protectioncoral-looking in for animals, e.g., fish ascidians sea squirts), (sessile and heads. amorphous calcium Va- carbonate incrustaceans the with crab mechanical cuticleleaves strength, provides of whereas these marine inIron-silica plants the biominerals it provide serves cyanobacteriaeffective as with calcium an storage. straightforward biomimetic principle transferMEMS to novel are given in Table ]. 31 , in one 30 designer . [email protected] MEMS MEMS use structure rather than design (where only a handful ]. Further examples of tribo- 63 MEMS ], and the jaws of certain marine worms that 64 can be identified in various organisms. Espe- Material Synthesis in Engineering and Medicine The generalized principle of base materials can be used, and the therefore has to workrial), with and will structure be rather even morewe than relevant finally in mate- mass-produce the various 3D future when Micro- and nanoengineersin biological profit systems frommaterial very often is the structure used factmany rather to cases, that the than achieve structures are certain solelyrespective responsible functionalities. for functions, the In allowingtransfer for of principles simple from biomimetic therespective inspiring application structure to in the vance engineering. in This current is of rele- 58.6 Applications 58.6.1 Current Applications of Bioinspired 58.5 Functions Most structures intional. biological Their systems integrated arecompact, cheap solutions approach multifunc- to various chemical, allows dynamic, structural, for mechanical, highly or physical demands go. Structures inengineers organisms can and be inspiretionary, great novel, teachers new sometimes for approaches. evenintrinsic However, revolu- multifunctionality, not because alwaysaspect of can of one their an single organismform be successfully for isolated man-made inconcept-wise. applications, pure sometimes One not fascinatingfunctionality even example of of living thetures nature multi- is and biomineralized theircomplex struc- respective arrangements, functions. such Especiallynanostructures as more in the silica diatoms,substantial micro- are inspiration and in envisaged micro-especially to and tribology provide nanotechnology, (regarding friction,brication, adhesion, and lu- wear ofrelative small motion) rigid [58. interacting parts in material cially for micro-interacting and parts in nanoscale relative motion organisms (e.g., with some diatoms) rigid logical optimization inchitons, biomineralized where iron structures iscoated are teeth, stored and close the teeth to canwear easily their [58. be magnetite- renewed as they contain copper and zinc-reinforced proteins [58. Biomedical Applications

Part I

Part I | 58.6 1294 Biomineralization in Marine Organisms 58.6 Applications 1295

Table 58.5 Non-exhaustive list of already identified functions in biomineralized structures of marine organisms, sorted by chemical, dynamic, mechanical, physical, and structural functions Chemical functions Dynamic functions Structural functions Calcium storage Lubrication (bearing-like struc- Sclerites (a component section of High performance nanocomposites tures) an exoskeleton, especially each of Molecular glue in composite struc- Mobility the plates forming the skeleton of tures Motion an arthropod) Storage (biominerals are ion reser- Movable rigid parts (ensuring a Spicules voir for cellular functions) certain maximum and minimum Structure building (corals) Mineralized holdfast (byssus of the distance) Surface texturing for optimized jingle shell Anomia) Pumps mechanical properties Underwater adhesives Waste disposal (inside, like some nanocrystals or pearls, perhaps also outside) Mechanical Functions Physical Functions Click-stop mechanism Buoyancy Crack redirection Co-orientation mechanisms in biominerals (control of Distance holder crystal orientation) Fixation (e.g., click stop in diatoms) Dynamic colors (diatoms, polychaete worms) Fracture resistance Electrically conductive bacterial nanowires Hinges (nanowiring in microbial communities) Injection Energy dissipation Interlocking devices Gravity sensing (otoconia, statoliths) Mechanical connection Lenses (optical) Mechanical fixation Magnets (for navigation, location) Mechanical protection Optical components (antireflective layers, lenses, Mechanical strength transparent containers for photosynthesizing organ- Protection isms) Reinforcement Ossicles Scaffolds Photonic components (e.g., light guiding in deep-sea Skeleton (, exoskeleton) organisms) 58.6 | I Part Springs Photoprotective coatings Stability Reflectivity (fish silver) Strength and Integrity Gravity sensing Teeth for cutting, rasping and grinding (e.g., iron in Magnetic sensing the teeth of chitons) Optical sensing Toughness (abalone) Balance sensing Weapons (defensive: e.g., sea urchin needles, ag- UV protection gressive: e.g., pistol shrimp dactyl club, conch snail Whiteness harpoons) Wear protection (addition of zinc or copper for rein- forcement)

biomimetic and biomineralization approaches need to rial as soon as they start using it. Examples are SrSO4 be made, taking energy and other factors into account. in the exoskeleton of Acantharea (Sect. 58.2.5), or One of the advantages of technology as opposed to SiO2 in diatoms (Sect. 58.2.3) – with the abundance functional entities in organisms is the freedom of choice of Sr and Si in ocean water being about 8 and 2 ppm, in materials. Organisms are stuck with a certain mate- respectively [58.66].

[email protected] O 65.07% . elemental composition Mg 0.1% Cl 0.2% Na 0.2% S 0.3% P 1% K 0.4% stress shielding Ca 1.5% and very different from the composition ) N 3.2% b ( H 9.51% ) might in the future yield marine biotechnology an body, and a cell phone. The Composition of the human body (wt%) Composition C 18.52%

b) enough to resistthesize fragmentation their own before extracellular matrix. theelasticity The (i. e., cells modulus the of syn- stiffness) mustsist be high compressive enough forces to re- thatmust would transmit collapse the stress pores, range (and to strain) surrounding tissues, in andtrated must the prevent loading concen- physiological and n of the human body . Novel disruptive engineering approaches that learn from living ) c ( C 39.51% l compositio [email protected] O 85.85% 53). Important fac- use structure rather than material Br 0.01% K 0.04% Ca 0.04% Pb 0.5% S 0.09% Cu 15% Cd 0.5% Ta 0.5% Ta Cr 0.5% Ag 0.5% Mg 0.13% Na 1.08% Zn 0.5% is similar to the elementa Cl 1.94% Sn 1% N 0.83% ) Ni 2% a ( The elemental compositions of ocean water, the hum Others 3% H 10.82% H 3.29% Co 4% O 5.32% Ferrous metal 3% Composition of ocean water (wt%) of ocean water Composition Cl 5.05% Composition of a cell phone (wt%) Bioinspired material synthesis is also of increasing

Glass/ceramics 15% c) a) of ocean water inspired machines and devices that needtheir less structure metal (e.g., and a plastics, navigation but device rather inspired achieve by the homing needed sea functionality turtles, mainly with from no dependence on satellites or metal parts) importance in tissue engineering,applications especially for regarding scaffolding (Chap. tors are similar inrelate a to scaffold the and chemicaland in composition, architecture, a the the biomineral, pore degradationproperties. and structure The rate strength and of mechanical the scaffold must be high Fig. 58.12a–c of current engineering devices such as a cell phone nature (e.g., by using the principle Biomedical Applications

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Part I | 58.6 1296 Biomineralization in Marine Organisms 58.6 Applications 1297

Also the synthesis of scaffold materials using prin- macroscale, perfectly integrating nanotechnology and ciples and processes underlying biomineralization is of biology. high interest. Biomineralized materials can be used as Higher-order organization by mesoscale self-as- biomaterial scaffolds, either as they occur naturally or sembly and transformation of hybrid nanostructures after treatment for modification. Further applications as proposed by Cölfen and Mann [58.70]isakey are bioinert and biodegradable materials, in medical challenge in the design of integrated materials with devices, for tissue engineering, and for the coating of advanced functions. Macromolecules and surfactants implants. could be used to significantly increase the scope for We have already started to initiate chemical reac- controlled materials synthesis. tions by printing reagents directly into a 3D reaction- Biomimetic silica biosynthesis opens a new route ware matrix (i. e., printing of molecules and tissues with to semiconductor nanofabrication [58.71, 72]. In 2008, a commercially available 3D printing platform), and Jeffryes and coworkers succeeded in metabolically in- time will tell how far we can get with printing whole or- serting nanostructured Ge into a patterned silica matrix gans or machines, from basic ingredients, simple base of the diatom Pinnularia sp. at levels ranging from 0:24 materials, in our homes [58.67, 68]. to 0:97 wt % Ge [58.72]. Embedding nanoscale germa- Current biotechnology allows the usage of pro- nium (Ge) into dielectric silica is of high importance for teins that are important in biomineralization across optoelectronic applications. The same group succeeded species. Natalio and coworkers used silicatein-˛ (from in incorporating amorphous titania into the , sponges) to guide the self-assembly of calcite spicules which maintained its native structure even when local similar to the spicules of calcareous sponges. As op- TiO2 concentrations within the nanopores approached posed to the rather brittle natural spicules, the synthetic 60 wt %. Similar to germanium-silica nanocomposites, spicules show greatly enhanced bending strength, and titanium dioxide nanocomposites are of high inter- furthermore waveguiding properties even when they are est for optoelectronic, photocatalytic, and solar cell bent [58.69]. applications. Genetic approaches to engineering hierarchical 58.6.2 Possible Future Applications scale materials, engineered virus and protein cage archi- of Bioinspired Material Synthesis tectures for biomimetic material synthesis, and bone- in Engineering and Medicine – like materials by mineralization of hydrogels are further Outlook promising areas of research and development. Biomineralization processes will play increasingly The future of marine biotechnology is dependent important roles in biology, biotechnology, medicine, upon the development of an enhanced understand- chemistry, interfacial science, materials science, and ing of the physical, chemical, and biological proper- nanotechnology [58.73]. With cellular and genetic 58.6 | I Part ties of marine organisms and ecosystems. Materials, controls of mineral formation, we could shape the structures and processes related to marine environ- minerals exactly as we need them. In vitro mod- ments can provide valuable contributions to engineer- els of mineralization would allow us to understand ing, resource management, medicine, and various other in great detail the interactions and molecular con- fields. A prerequisite for this is the understanding of tacts between macromolecular and mineral compo- the connection between functionalities of biomineral- nents. Macromolecular scaffolds for materials synthesis ized materials and structures from the nanoscale to and organization would open up new directions in tis- the macroscale, including the effect of hierarchy and sue engineering. A detailed understanding of the com- structuring. Especially interesting are models where plex matrix–mineral relationships from the molecular macroscale properties can be understood from dis- level to the skeletal tissue, its properties and structure– tinct functionalities at various length scales and sub- function relations will open completely new approaches sequent implementation in technological processes. in engineering and medicine. For jewelery applica- Efficient successful synthesis of biomineralized ma- tions, we might even think about growing facetted terials and structures, where form follows function, crystals by spatially controlling growth inhibition and will pave the way towards tailored multiscale ma- promoting proteins (control of crystal orientation and rine biotechnology, which starts at the molecular level shape by interface engineering). Just imagine crys- and incorporates the hierarchical functionalities of bi- tals grown in gels, with exactly the shape and size ological materials through the length scales up to the needed!

[email protected] , ]. 50 The 75 ,21– 19 1, 393–416 Bioinorganic , 2nd edn., ed. , 177–196 (1988) 35 ] and ultimately yield a new ity?, Aquaculture 77 ]. , ed. by I. Bertini, H.B. Gray, S.J. Lippard, 76 (2), 113–120 (1974) 4 transport, and biomineralization. In: Chemistry J.S. Valentine (University Science1994) Books, Mill pp. Valley 1–35 distributions in relation to phytoplanktontivity, produc- Deep-Sea Res. Evol. membrane transport of cobalaminand in eukaryotic prokaryotic 1053–1086 cells, (1981) Annu. Rev. Biochem. for the recovery of metals, Int. Metall. Rev. dissolved chemicals, Proc. 144thSoc. Meet., Natl. Washington Am. (1963) pp. Chem. 122–131 tures, a(1972) possibil Desk Encyclopedia of Microbiologyby M. Schaechter (Academia, Oxford 2009) pp. 346– 31 (1974) 356 Marine invertebrate cell cultures are currently not and development isable still to needed replicateexquisite mechanical before both properties we of thethetic natural will structure bone. biomimetic be Syn- asbiological materials well principles fabricated as andand according the processes self-organization to of arefor self-assembly promising a new newrelated generation approaches bone of analogs biologicallyCurrent for and strategies structurally tissue for boneitations. engineering repair [58. Marine have organisms acceptedporous structures as lim- with templates for bone naturally growthan might be inspiration for occurring novel ex vivoapproaches bone [58. tissue engineering well established. They could serveeralization as tools studies for [58. biomin- generation of advanced, high-performance composites required for new construction materials, new microelec- tronic, optoelectronic and catalyticand devices, biological chemical sensors,vesters, smart energy medical transducers implants,capacity and and biochips. Marine faster har- biotechnology and regarding ap- plications higher of bioinspired material synthesis ining engineer- and medicine has enormous potential. 58.11 E.C. Theil, K.N. Raymond: Transition-Metal Storage, 58.12 J.H. Martin, R.M. Gordon: Northeast58.13 Pacificiron F. Egami: Minor58.14 elements and evolution, C. J. Sennett, Mol. L.E. Rosenberg, I.S. Mellman: Trans- 58.15 O.H. Tuovinen, D.P. Kelly: Use of micro-organisms 58.16 W.F. McIlhenny, D.A. Ballard: The sea as a source of 58.17 J.C. Deelman:58.18 Microbial A. mineral Teske: Deep sea maricul- hydrothermal vents. In: Ma- (Oxford (Wiley- )), and ,ed.by (Elsevier, ]. (The National 74 [email protected] (3), 241–250 (1986) 12 (5700), 1301–1302 (2004) Microbial Ecology nd Sustainability 306 Advanced Topics in Biomineralization Biomineralization: Principles and Con- The Mineral Resources of the Sea , pp. 195–199]. The high content of cal- 23 proposed bamboo corals as living bone Element Recovery a MISS) and stromatolites, banded iron for- (1–3), 19–32 (1996) (3), 609–643 (2010) raphy and conservation of336 diatoms, Hydrobiologia rine BiotechnologyProblems, in Promise, theAcademic, and Twenty-First Washington 2002) century: Products biomolecules, Science cepts in BioinorganicUniv. Materials Press, Chemistry Oxford 2001) biomineralize?, Paleobiology Amsterdam 1965) omicrobiology and bioremediation,156 Microbiology In: A.J. Hunt (Royal2013) Society pp. 114–139 of Chemistry, Cambridge Blackwell, Hoboken 2011) (InTech, Rijeka, Shanghai 2012) Ehrlich Microbe–mineral interactions that lead to sedimen- Although synthetic bone replacement materials Nature can furthermore serve as a teacher con- tary structures such as microbially inducedstructures sedimentary ( mations, cherts, sandstones, and carbonateone rocks might day be reproduced inand the allow laboratory a or more benign, in environmentally the friendlyof way field, mining. are now widely used in orthopaedics, much research References 58.6 D.G. Mann, S.J.M. Droop: 3. Biodiversity,58.7 biogeog- J.L. Mero: 58.1 Ocean Studies Board, Board on Life Sciences: 58.2 J.J. De Yoreo, P.M. Dove: Shaping crystals with 58.5 M. Brasier: Why do lower plants and animals 58.8 G.M. Gadd: Metals, minerals58.9 and microbes: Ge- W.N.C. Anderson: Hyperaccumulation by plants. 58.10 L.L. Barton, D.E. Northup: 58.3 J. Seto (Ed.): 58.4 S. Mann: dynamic and hierarchical structures [58. implants [58. cium carbonate scaffolds ofresembles the commonly bone used in coral cal terms properties. of Theble, structure coral osteoconductive, and exoskeleton and mechani- for is biodegradable, attachment, biocompati- and growth, allows of spreading, and bone differentiation cells.ufactured Coralline by hydroxyapatite hydrothermal can conversioncarbonate of coral be skeleton. the man- calcium cerning the nanofabricationoptical structures, nanoscale of attenuators (for micro- crystalline and nanoelectromechanical systems materials, (MEMS/NEMS Biomedical Applications

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