Biomineralization

Part of a series related to
Biomineralization
General Mineralized tissues Remineralisation Biocrystallization Biointerface Biofilm
Exoskeletons (shells) Arthropod exoskeleton cuticle Brachiopod shell Cephalopod shell cirrate shell cuttlebone gladius Lorica Choanoflagellate lorica Protist shell coccosphere coccolith diatom frustule foraminifera test testate amoebae Seashell echinoderm stereom mollusc shell nacre chiton shell gastropod shell small shelly fauna scaly-foot snail shell estuary shells Sponge spicule Test
Endoskeletons (bones) Vertebrate skeleton Bone mineral Ossification
Teeth, scales, tusks etc Limpet teeth Otolith otolithic membrane Scale microfossils Tusk
Calcification amorphous calcium carbonate marine biogenic calcification calcareous nannofossils Aragonite oolitic aragonite sand aragonite sea Calcite microbial calcite precipitation calcite sea Great Calcite Belt
Silicification biogenic silica siliceous ooze diatomaceous earth
Other forms Bone bed Kerogen alginite oil shale Phosphate phosphorite Pyrena
Related Mineral evolution In soil mineralization immobilization Ballast minerals Magnetofossil Magnetosome Magnetotactic bacteria Magnetoreception Microfossils engrailed gene Druse Cupriavidus metallidurans Biomineralising polychaetes Mineral nutrients Microbial mat Fossilization permineralization petrifaction Burgess Shale preservation
Category
v t e

Biomineralization, also written biomineralisation, is the process by which living

Organisms have been producing mineralized skeletons for the past 550 million years. Calcium carbonates and calcium phosphates are usually crystalline, but silica organisms (sponges, diatoms...) are always non-crystalline minerals. 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

Mineralization can be subdivided into different categories depending on the following: the organisms or processes that create chemical conditions necessary for mineral formation, the origin of the substrate at the site of mineral precipitation, and the degree of control that the substrate has on crystal morphology, composition, and growth.[8] These subcategories include biomineralization, organomineralization, and inorganic mineralization, which can be subdivided further. However, the usage of these terms varies widely in the scientific literature because there are no standardized definitions. The following definitions are based largely on a paper written by Dupraz et al. (2009),^[8] which provided a framework for differentiating these terms.

Biomineralization

Biomineralization, biologically controlled mineralization, occurs when crystal morphology, growth, composition, and location are completely controlled by the cellular processes of a specific organism. Examples include the shells of invertebrates, such as molluscs and brachiopods. Additionally, the mineralization of collagen provides crucial compressive strength for the bones, cartilage, and teeth of vertebrates.^[9]

Organomineralization

This type of mineralization includes both biologically induced mineralization and biologically influenced mineralization.

• Biologically induced mineralization occurs when the metabolic activity of microbes (e.g. bacteria) produces chemical conditions favorable for mineral formation. The substrate for mineral growth is the organic matrix, secreted by the microbial community, and affects crystal morphology and composition. Examples of this type of mineralization include calcareous or siliceous stromatolites and other microbial mats. A more specific type of biologically induced mineralization, remote calcification or remote mineralization, takes place when calcifying microbes occupy a shell-secreting organism and alter the chemical environment surrounding the area of shell formation. The result is mineral formation not strongly controlled by the cellular processes of the animal host (i.e., remote mineralization); this may lead to unusual crystal morphologies.^[10]
• Biologically influenced mineralization takes place when chemical conditions surrounding the site of mineral formation are influenced by abiotic processes (e.g., evaporation or degassing). However, the organic matrix (secreted by microorganisms) is responsible for crystal morphology and composition. Examples include micro- to nanometer-scale crystals of various morphologies.^[11][12]

Biological mineralization can also take place as a result of fossilization. See also calcification.

Biological roles

Among animals, biominerals composed of

• 
  Many protists, like this coccolithophore, have protective mineralised shells
• 
  Forams

  from a beach
• 
  Many invertebrate animals have external exoskeletons or shells, which achieve rigidity by a variety of mineralisations
• 
  Vertebrate animals have internal

  hydroxylapatite

If present on a supracellular scale, biominerals are usually deposited by a dedicated organ, which is often defined very early in embryological development. This organ will contain an organic matrix that facilitates and directs the deposition of crystals.

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.^[15] 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.^{[citation needed]}

The most described arrangement in mollusc shells is the nacre, known in large shells such as Pinna or the pearl oyster (Pinctada). Not only does the structure of the layers differ, but so do their mineralogy and chemical composition. Both contain organic components (proteins, sugars, and lipids), and the organic components are characteristic of the layer and of the species.^[4] The structures and arrangements of mollusc shells are diverse, but they share some features: the main part of the shell is crystalline calcium carbonate (aragonite, calcite), though some amorphous calcium carbonate occurs as well; and although they react as crystals, they never show angles and facets.^[16]

In fungi

Fungi are a diverse group of organisms that belong to the eukaryotic domain. Studies of their significant roles in geological processes, "geomycology", have shown that fungi are involved with biomineralization, biodegradation, and metal-fungal interactions.^[18]

In studying fungi's roles in biomineralization, it has been found that fungi deposit minerals with the help of an organic matrix, such as a protein, that provides a nucleation site for the growth of biominerals.

Though minerals can be produced by fungi, they can also be degraded, mainly by oxalic acid–producing strains of fungi.^[21] Oxalic acid production is increased in the presence of glucose for three organic acid producing fungi: Aspergillus niger, Serpula himantioides, and Trametes versicolor.^[21] These fungi have been found to corrode apatite and galena minerals.^[21] Degradation of minerals by fungi is carried out through a process known as neogenesis.^[22] The order of most to least oxalic acid secreted by the fungi studied are Aspergillus niger, followed by Serpula himantioides, and finally Trametes versicolor.^[21]

In bacteria

It is less clear what purpose biominerals serve in bacteria. One hypothesis is that cells create them to avoid entombment by their own metabolic byproducts. Iron oxide particles may also enhance their metabolism.^[23]

Other roles

Biomineralization plays significant global roles

Most biominerals can be grouped by chemical composition into one of three distinct mineral classes: silicates, carbonates, or phosphates.[25]

Silicates

Silicates (glass) are common in marine biominerals, where diatoms and radiolaria form frustules from hydrated amorphous silica (opal).^[27]

Carbonates

The major carbonate in biominerals is CaCO₃. The most common polymorphs in biomineralization are calcite (e.g. foraminifera, coccolithophores) and aragonite (e.g. corals), although metastable vaterite and amorphous calcium carbonate can also be important, either structurally^[28][29] or as intermediate phases in biomineralization.^[30][31] Some biominerals include a mixture of these phases in distinct, organised structural components (e.g. bivalve shells). Carbonates are particularly prevalent in marine environments, but also present in freshwater and terrestrial organisms.^[32]

Phosphates

The most common biogenic phosphate is

Other minerals

Beyond these main three categories, there are a number of less common types of biominerals, usually resulting from a need for specific physical properties or the organism inhabiting an unusual environment. For example, teeth that are primarily used for scraping hard substrates may be reinforced with particularly tough minerals, such as the iron minerals magnetite in chitons^[39] or goethite in limpets.^[40] Gastropod molluscs living close to hydrothermal vents reinforce their carbonate shells with the iron-sulphur minerals pyrite and greigite.^[41] Magnetotactic bacteria also employ magnetic iron minerals magnetite and greigite to produce magnetosomes to aid orientation and distribution in the sediments.

Magnetotactic bacterium containing a chain of magnetosomes

Magnetosome chain with octahedral habits modelled lower right^[42]

• 
  Chitons have aragonite shells and aragonite-based eyes,^[43] as well as teeth coated with magnetite.
• 
  Limpets have carbonate shells and teeth reinforced with goethite

• 
  Acantharian

  radiolarians have celestine crystal shells
• 
  Celestine crystals, the heaviest mineral in the oceans

Broadly, biomineralized structures evolve and diversify when the energetic cost of biomineral production is less than the expense of producing an equivalent organic structure.[57]^[58][59] The energetic costs of forming a silica structure from silicic acid are much less than forming the same volume from an organic structure (≈20-fold less than lignin or 10-fold less than polysaccharides like cellulose).^[60] Based on a structural model of biogenic silica,^[61] Lobel et al. (1996) identified by biochemical modeling a low-energy reaction pathway for nucleation and growth of silica.^[62] The combination of organic and inorganic components within biomineralized structures often results in enhanced properties compared to exclusively organic or inorganic materials. With respect to biogenic silica, this can result in the production of much stronger structures, such as siliceous diatom frustules having the highest strength per unit density of any known biological material,^[63][64] or sponge spicules being many times more flexible than an equivalent structure made of pure silica.^[65][66] As a result, biogenic silica structures are used for support,^[67] feeding,^[68] predation defense ^[69][70][71] and environmental protection as a component of cyst walls.^[53] Biogenic silica also has useful optical properties for light transmission and modulation in organisms as diverse as plants,^[72] diatoms,^[73][74][75] sponges,^[76] and molluscs.^[77] There is also evidence that silicification is used as a detoxification response in snails ^[78] and plants,^[79] biosilica has even been suggested to play a role as a pH buffer for the enzymatic activity of carbonic anhydrase, aiding the acquisition of inorganic carbon for photosynthesis.^[80][56]

• 
  Diversity of biomineralization across the eukaryotes ^[56]

  The phylogeny shown in this diagram is based on Adl et al. (2012),^[81] with major eukaryotic supergroups named in boxes. Letters next to taxon names denote the presence of biomineralization, with circled letters indicating the prominent and widespread use of that biomineral. S, silica; C, calcium carbonate; P, calcium phosphate; I, iron (magnetite/goethite); X, calcium oxalate; SO₄, sulfates (calcium/barium/strontium), ? denotes uncertainty in the report.^{[82][83][25][50][47][84]}

There are questions which have yet to be resolved, such as why some organisms biomineralize while others do not, and why is there such a diversity of biominerals besides silicon when silicon is so abundant, comprising 28% of the Earth's crust.^[56] The answer to these questions lies in the evolutionary interplay between biomineralization and geochemistry, and in the competitive interactions that have arisen from these dynamics. Fundamentally whether an organism produces silica or not involves evolutionary trade-offs and competition between silicifiers themselves, and non-silicifying organisms (both those which use other biominerals, and non-mineralizing groups). Mathematical models and controlled experiments of resource competition in phytoplankton have demonstrated the rise to dominance of different algal species based on nutrient backgrounds in defined media. These have been part of fundamental studies in ecology.^[85][86] However, the vast diversity of organisms that thrive in a complex array of biotic and abiotic interactions in oceanic ecosystems are a challenge to such minimal models and experimental designs, whose parameterization and possible combinations, respectively, limit the interpretations that can be built on them.^[56]

Evolution

The first evidence of biomineralization dates to some 750 million years ago,

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 biomineralisation capacity of brachiopods and molluscs has also been demonstrated to be homologous, building on a conserved set of genes.^[103] This indicates that biomineralisation is likely ancestral to all lophotrochozoans.

The most ancient example of biomineralization, dating back 2 billion years, is the deposition of

Most traditional approaches to the 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.[106] 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.^[107][108]

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 biomineralization. These composites are often not only as hard as the pure mineral but also tougher, as the micro-environment controls biomineralization.^[107][108]

Architecture

• 
  Bacillus megaterium
• 
  Bacillus subtilis

One biological system that might be of key importance in the future development of architecture is bacterial biofilm. The term biofilm refers to complex heterogeneous structures comprising different populations of microorganisms that attach and form a community on inert (e.g. rocks, glass, plastic) or organic (e.g. skin, cuticle, mucosa) surfaces.^[109]

The properties of the surface, such as charge,

• 
  Model for biomineralization‐mediated scaffolding
  of bacterial biofilms

  A directed growth of the calcium carbonate crystals allows mechanical support of the 3D structure. The bacterial extracellular matrix (brown) promotes the crystals' growth in specific directions.^[115][114]

Bacterially induced calcium carbonate precipitation can be used to produce "self‐healing" concrete. Bacillus megaterium spores and suitable dried nutrients are mixed and applied to steel‐reinforced concrete. When the concrete cracks, water ingress dissolves the nutrients and the bacteria germinate triggering calcium carbonate precipitation, resealing the crack and protecting the steel reinforcement from corrosion.^[116] This process can also be used to manufacture new hard materials, such as bio‐cement.^[117][114]

However, the full potential of bacteria‐driven biomineralization is yet to be realized, as it is currently used as a passive filling rather than as a smart designable material. A future challenge is to develop ways to control the timing and the location of mineral formation, as well as the physical properties of the mineral itself, by environmental input. Bacillus subtilis has already been shown to respond to its environment, by changing the production of its ECM. It uses the polymers produced by single cells during biofilm formation as a physical cue to coordinate ECM production by the bacterial community.^{[118][119][114]}

Uranium contaminants

• 
  Autunite crystal

Biomineralization may be used to remediate groundwater contaminated with uranium.^[120] The biomineralization of uranium primarily involves the precipitation of uranium phosphate minerals associated with the release of phosphate by microorganisms. Negatively charged ligands at the surface of the cells attract the positively charged uranyl ion (UO₂²⁺). If the concentrations of phosphate and UO₂²⁺ are sufficiently high, minerals such as autunite (Ca(UO₂)₂(PO₄)₂•10-12H₂O) or polycrystalline HUO₂PO₄ may form thus reducing the mobility of UO₂²⁺. Compared to the direct addition of inorganic phosphate to contaminated groundwater, biomineralization has the advantage that the ligands produced by microbes will target uranium compounds more specifically rather than react actively with all aqueous metals. Stimulating bacterial phosphatase activity to liberate phosphate under controlled conditions limits the rate of bacterial hydrolysis of organophosphate and the release of phosphate to the system, thus avoiding clogging of the injection location with metal phosphate minerals.^[120] The high concentration of ligands near the cell surface also provides nucleation foci for precipitation, which leads to higher efficiency than chemical precipitation.^[121]

Biogenic mineral controversy

The geological definition of mineral normally excludes compounds that occur only in living beings. However, some minerals are often

The International Mineralogical Association (IMA) is the generally recognized standard body for the definition and nomenclature of mineral species. As of December 2020^[update], the IMA recognizes 5,650 official mineral species^[122] out of 5,862 proposed or traditional ones.^[123]

A topic of contention among geologists and mineralogists has been the IMA's decision to exclude biogenic crystalline substances. For example, Lowenstam (1981) stated that "organisms are capable of forming a diverse array of minerals, some of which cannot be formed inorganically in the biosphere."^[124]

Skinner (2005) views all solids as potential minerals and includes biominerals in the mineral kingdom, which are those that are created by the metabolic activities of organisms. Skinner expanded the previous definition of a mineral to classify "element or compound, amorphous or crystalline, formed through biogeochemical processes," as a mineral.^[125]

Recent advances in high-resolution genetics and X-ray absorption spectroscopy are providing revelations on the biogeochemical relations between microorganisms and minerals that may shed new light on this question.^[126][125] For example, the IMA-commissioned "Working Group on Environmental Mineralogy and Geochemistry " deals with minerals in the hydrosphere, atmosphere, and biosphere.^[127] The group's scope includes mineral-forming microorganisms, which exist on nearly every rock, soil, and particle surface spanning the globe to depths of at least 1,600 metres below the sea floor and 70 kilometres into the stratosphere (possibly entering the mesosphere).^{[128][129][130]}

Prior to the International Mineralogical Association's listing, over 60 biominerals had been discovered, named, and published.[134] These minerals (a sub-set tabulated in Lowenstam (1981)^[124]) are considered minerals proper according to Skinner's (2005) definition.^[125] These biominerals are not listed in the International Mineral Association official list of mineral names,^[135] however, many of these biomineral representatives are distributed amongst the 78 mineral classes listed in the Dana classification scheme.^[125]

Skinner's (2005) definition of a mineral takes this matter into account by stating that a mineral can be crystalline or amorphous.^[125] Although biominerals are not the most common form of minerals,^[136] they help to define the limits of what constitutes a mineral properly. Nickel's (1995) formal definition explicitly mentioned crystallinity as a key to defining a substance as a mineral.^[126] A 2011 article defined icosahedrite, an aluminium-iron-copper alloy as mineral; named for its unique natural icosahedral symmetry, it is a quasicrystal. Unlike a true crystal, quasicrystals are ordered but not periodic.^[137][138]

List of minerals

Examples of biogenic minerals include:^[139]

• Apatite in bones and teeth.
• Aragonite, calcite, fluorite in vestibular systems (part of the inner ear) of vertebrates.
• algal
  action.
• mitochondria
  .
• Magnetite and greigite formed by magnetotactic bacteria.
• Pyrite and marcasite in sedimentary rocks deposited by sulfate-reducing bacteria.
• Quartz formed from bacterial action on fossil fuels (gas, oil, coal).
• Goethite found as filaments in limpet teeth.

Astrobiology

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

Notes

References