Biomineralization

(This text was somewhat edited from original manuscript. Illustrations removed and also formalia deleted to anonymize the text. This text was written as an exercise in writing review articles for a paleontology class I took spring of 2010. The format used was based on manuscript for Lethaia: An International Journal of Palaeontology and Stratigraphy.)

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Biomineralization – an overview of function and applications

Abstract

Micro-organisms reduce, immobilize and form many types of metal particles and also form more massive ore formations such as Banded Iron Formations (BIF). These processes are referred to as biomineralization and can be categorized in to Biologically Induced Mineralization (BIM) and Biologically Controlled Mineralization (BCM), that simply defines whether the process is intentional and intracellular (BCM) or a byproduct of metabolism (BIM). The importance of understanding the role and function of bacteria and other microbes and their use of minerals in its environment primarily relate to improving the production of metal for the industry (biomining and bioleaching), but also environmental issues where microbes can control and immobilize toxic elements in the environment. And finally, astrobiologists also use biominerals as indicators of life on other planets.

Keywords: Biomineral, bacteria, BIM, BCM, organomineral, biomining, bioleaching


Introduction

The topic of life and minerals contains interactions on many different aspects and levels. The important connections between the evolution of life and the role of minerals in this process has only been known for a couple of decades (Ochiai 1983, Smith 2005, Dove 2010). The science of studying ore forming microbes is basically even younger than this with little non-speculative material older than the 1980s. It is an expansive and still very young field of research where new important and basic level discoveries still are and probably will be made for a long time. Consequently, many rudimentary questions on how some important processes like the formation of some larger sedimentary ore deposits and their connection to microbial life still exist (Smith 2005, Défarge 2007). In the microbial world (i.e. bacteria, archaea and fungi), life interacts with minerals directly through metabolism and respiration and as a result of other indirect interactions. There are to date several hundred species of microbes known that interacts with around 64 known minerals (see Fig 1 for examples). These numbers continuously grow all the time when new associations and fossil evidence are found both in the field and in controlled laboratory environments. Most scientists within the field of biomineralization are confident that many more connections between microbial life and minerals are yet to be discovered (Défarge 2007). This paper focus on the connection between bacteria and ore minerals.

Biominerals and organominerals

Microbial associations and interactions with basic elements and minerals can be sub-divided into two major categories according to Frankel & Bazylinski (2003a). BIM, which stands for Biologically Induced Mineralization, and BCM, which stands for Biologically Controlled Mineralization. These two concepts then encompass all differentiating processes with regards to what taxa of microbes that are discussed, their use or interaction with minerals and what type of geological products are discussed (i.e. sulfates, sulfides, silicates and oxides). However, one can argue that this simple sub-division is problematic. First there exist several know examples of species of bacteria that can do both BIM and BCM, second and equally important, there exist a third concept called organominerals (Perry et al 2007, Défarge 2007). The concept of organominerals and what it encompass is debated (Défarge 2007). In some cases this third concept includes BIM but also refers to other related processes such as pyritization of fossils or the post-mortem incrustation of bacteria on other life forms. It can even include abiotic carbon. “Organomineral” must consequently be considered to be a too wide, vague and controversial term (Défarge 2007).

Biologically Induced Mineralization

BIM can be described as a mostly unintentional consequence of metabolic activities in the microbial organism. That means, the mineralization of ores or ore nano particles is unintentional and simply an extracellular by-product of the microbial metabolism. The bacteria or other type of microbe secrete organic products that attracts ions or compounds in its vicinity and with them, which subsequently results in either concentration, alteration, immobilization or depletion of these minerals. This means that the formation of elemental crystals is not directly controlled by the microbe. This leads to a poor and more random crystallization and a lack of specific crystal morphologies (Provencio & Polyak 2001). Ores formed in this manner also tend to be impure in the crystal lattice and full of inclusions of other minerals and compounds. (Frankel & Bazylinski 2003a).

All life on Earth respire, including all microbes. Bacterial respiration function is sometimes anaerobic and taking place in extreme environmental conditions with high temperatures and/or low solubility like for example inside siliciclastic bedrocks deep inside the earth crust. But also simply deep water settings or places where oxygen has been depleted by other organisms. This means that instead of oxygen, the anaerobic bacteria can use other elements or minerals as electron donors or acceptors in the electron transport chain, as long as they can receive or give an electron. The electron transport chain is then used to gain energy and function within the bacteria by generating a potential across its membrane (Newman 2001, Karp 2008). In respiration elements usually are in soluble form like oxygen, nitrates and sulphate, but several genera of bacteria can also respire on solid mineral states like the common examples hematite Fe2O3 and goethite α-FeO(OH) (Newman 2001, Lower et al 2001). The bacteria literally reside on and respire of the surface of these ore minerals. In solid state respiration it is generally thought that the bacteria generate an electron in a special protein (called 150-kD) in the outer membrane, which has direct contact with the minerals and transfers the electron directly to and from the minerals this way. The small electron charge that is formed has been proven through an experiment by Lower et al (2001) to exist and work on the bacteria Shewanella oneidensis and the solid state mineral goethite.

The process of respiration in solubles is more complex, variable and is much more important in the formation of larger ore concentrations than solid state respiration. Here it is not simply the direct use of mineral grains, but more often an unintentional by-product of the respiration. The bacteria, depending on species can produce, for example OH, CO2, H+ and NH3 as a result of end-products of the metabolism and these elements and ions can, in turn, react to and attract various ore minerals and thereby form larger concentrations with time (Konhauser 1997). The principle of a charged surface, as shown above when discussing solids can also among solubles result in an attraction of ore atoms around the bacterial cell surface (Fig. 2), which in time and when the bacterial concentration is in high enough will lead to formation of ores. This process also continues to some extent long after the bacteria has perished due to electron charge build up (Konhauser 1997). As a result of creating low Ph substances and acids, but also by using certain proteins through their metabolism, bacteria can also dissolve or extract ions that then binds to these organic compounds through a process called chelation, where the organic compounds as ligands are formed around a metal ion.

This is also the principle process in how and why plants and fungi concentrate metals and toxic heavy metals around or within their cells. The molecules formed by chelation are very stable and therefore used for many purposes in the medical and agrarian industries (Fomina 2007). The most commonly occurring variation of BIM and probably economically most important is sulfate reduction to sulfides where bacteria generate sulfides through the metabolism of suftates. The sulfide ions can then bind to a large number of different types of metals, forming sedimentary sulfide ores.

Biologically Controlled Mineralization

BCM is a more specific and intentional use of minerals by micro-organisms that takes place at an intracellular level and is generally much less understood than BIM. In BCM the mineral crystals are formed and deposited within the organic matrices and vesicles for different purposes or possibly also in some cases unintentional as a result of uncontrolled uptake – making the line between BIM and BCM unclear. In general, however, BCM is defined by more distinct composition, size and shape of the intracellulary formed crystals in comparison to BIM crystals which shows that the organism has a significant degree of control of the crystallization of the minerals and the crystallization is thought to be under genetic and/or metabolic control (Frankel & Bazylinski 2003b).

The single most common and most well studied process of BCM is those of so the called magnetoactic bacteria (MTB) and their use of ferrimagnetic nanocrystals (Postfai & Dunin-Burkowsky 2009). With special organelles called magnetosomes the bacteria, like for example the Magnetospirillum gryphyswaldense generates crystals of magnetite Fe3O4 (or less commonly greigite Fe3S4) within their body, that readily visible in X-ray (Fig. 3). These crystals are just big enough to have their individual magnetic fields so that it can react to the Earth’s magnetic field, and orient the bacteria in its water habitats. It is thought that it aids the bacteria in movement and orientation of what is up and down in their habitat so that it can move to the preferred part of the oxic or anoxic habitat since it is here, at the interface between these habitats the magnetoactic bacteria lives. The use of magnetite or greigite grains have also been seen in many more groups of life such as algea, worms, lobsters, birds and fishes. Here it is thought that they use the magnetic crystals for more active navigation and not just orientation as in the case of bacteria (Postfai & Dunin-Burkowsky 2009). According to Frankel & Bazylinski (2003a) the process of BCM is not proven to occur on a large scale and therefore most likely does not lead to any significant ore formations in comparison to BIM. But both Ochiai (1983) and Konhauser (1997) hypothesize that larger concentration of ore (greigite Fe3S4 , pyrite FeS2 and sedimentary copper ) could be the result of BCM.

Examples of minerals and ores formed by BIM and BCM

Iron

Biologically formed iron ore is by far the most common and thoroughly studied process of biomineralization (Konhauser 1997, Frankel & Bazylinski 2003a, Perez-Gonzales et al. 2009, Johnston 2010). It is relatively important to start with iron as an example of how ores are formed by BIM since iron often is the primary choice (due to its abundance in nature) for many of the BIM-bacteria that exist. Iron in its various forms is their most common source of energy (but can be replaced by other types of minerals). There are five major variations on iron biomineralization that incorporates both BIM and BCM: Hydroxides & oxides, phosphates, silicates, sulfates and sulfides (Konhauser 1997).

Hydroxides & oxides. – Oxidization in nature of ferrihydrites is very common. Biologically it generally works on an extracellular level as BIM. In the active way, bacteria oxidizes Fe2+ or Fe3+ (or other forms of metal that can oxidize) as an energy source, precipitating iron hydroxides or iron hydroxysulfates (or other end products for other metals). Very little energy can be gained this way with regards to Fe2+, and therefore large quantities will be oxidized even by a small number of bacteria (Konhauser 1997). The by-products of the process are acidic, and the process also accelerates when Ph-levels drop. So the more oxidization, the more beneficial the environment will be for more oxidization. BIM-magnetite is the most common iron ore that forms through this process (Fig. 4). Both hematite and goethite are found associated with oxidizing bacteria as well. They are thought in some cases to have formed when the ferrihydrites dehydrate after bacterial precipitation. Magnetite can form under both BIM and BCM. As mentioned above, under BCM it is formed inside the organism to be a tool for orientation. Under BIM however its simply precipitated on the membrane as a end-product of metabolism, encrusting the bacteria (Konhauser 1997). In recent years, the most prevailing theory on Banded Iron Formation (BIF) in the Precambrian is that of cyanobacteria oxidizing free iron ions in the oceans, thus forming the BIF (Kappler et al. 2005).

Sulfides. – Following ores that are the result of oxidization, the sulfides, formed in anoxic environments are probably the most important ores for mining. Pyrite is one of the most common iron sulfides and has been connected in some cases to bacterial activities, both as BIM and BCM. Sulfides in these cases are the end-product of bacterial metabolism of the energy rich sulfates. Konhauser et al. (1997) described biomineralized pyrite as formed by the coupling of oxidization of organic molecules in the environment to the reduction of sulfate. The sulfide generated by the bacteria reacts with iron oxides or hydroxides and form monosulfide phases as FeS (and mackinawite (Fe,Ni)1 + xS) but also elemental sulfur. The latter then becomes the oxidant required to convert FeS to pyrite FeS2.

Sulfates. – As a result of oxidization in acidic conditions of ferrihydrates and also iron sulfides bacteria can produce ferric hydroxysulfates. This process is commonly used in biomining and bioleaching. But the exact process of this in detail on a bacterial level is a matter of debate (Konhauser 1997).

Phosphates. – Phosphates are a common source of energy for bacteria and occur in abundance in, for example anoxic water environments. Phosphate is often dissolved from underlaying apatite (Ca5(PO4)3(F,Cl,OH)) rich rocks or a product from the decay of organic material. The formation of iron phosphate minerals through microbes such as strengite (FePO4-2H2O), which is a hydrated iron phosphate created by organic acids, has been directly observed when analyzing biofilms growing on phosphorite sediments. Associations with simple iron oxides (FeO) and goethite has also been found in phosphorite sediments from Paleozoic to Cenozoic times. These biofilms, or lichens, which are symbiotical concentrations of bacteria and fungi concentrate and immobilize metals from the phosphates. Phosphorite sediments can sometime form banded layers of hundred of meters in thickness with thinner layers of phosphorous iron ores (Konhauser 1997).

Silicates. – Bacteria can also form iron rich silicates, primarily found in acidic hot spring sediments (Konhauser 1997). Examination of such sediments has revealed bacterial cells completely encrusted in these minerals. They are presumed to be formed as a result of iron binding to anionic cells and where dissolved silica in the spring then was subsequently added to the growing minerals in the process. Another process in which silicates form has been observed in biofilms in clays in freshwater environments. Here (Fe, Al)-silicates similar to chamonite ((Fe5Al)(Si3Al)10(OH)8) and kaolinite (Al4(Si4O10)(OH)4), but with a poor crystallinity, typical of BIM-biominerals, was found. These are therefore thought to have formed as a result of reaction between the silica, metals and possibly metals within the cell (BCM-generated) since it is well known that fresh water bacteria can bind and immobilize metals. The process of forming a silicate is then completed through diagenesis (Konhauser 1997).

Uranium

Uranium in all its variations and stages (flourides, oxides and metal) is deadly for all forms of life, including the radiation-resistant bacteria and fungi that use it for respiration. It is all a matter of time and concentration before life expires. So the keys to success in using this element for microbial life are the duration and amount of exposure. When the concentrations of uranium reach a certain level, life dies from the radiation (Alfa and Beta-radiation) and the process of crystal formation only continues abiotically because of the high concentrations. There are no uranium-specific bacteria that respire uranium, rather it is known to be the same species that use iron or manganese for respiration. They can use U(VI) (Uranium Hexafluoride) as an electron acceptor instead of for example Fe3+ (Min et al, 2005). S. putrefaciens and G. metallireducens are the most common species of bacteria that reduce U(VI) to Uranium dioxide U(IV)(UO2) through respiration and in the process economically interesting ores of uranite are created, which is a metal ore that largely consists of UO2.

Moreover fungi can absorb uranium that has been dissolved by bacteria, and possibly also dissolve uranium by itself. Therefore both fungi and bacteria can be found working and benefiting directly and indirectly from each other in the same ore environments (Chabalala & Chirwa 2009).

Uranium is relatively abundant in all parts of the Earths pedosphere and litosphere, but the richest concentrations are found in sand deposits. Min et al. (2005) proved an abundance of fossil pseudomorph bacterial structures in large sandstone hosted uranium roll-front deposits in the YL-basin of eastern China. Such pseudomorphic structures are usually poorly preserved, but in this case an associated feature that preserved the structures was found. High concentrations of uranite ore was recorded in association with petrified pieces of wood where uranite and the uranium silicate coffinite (U(SiO4)1-x(OH)4x ) had replaced the wood structure on a cellular level. Much of the fossilized wood-structure was also replaced by fossilized fungi and bacterial structures. This clearly shows the importance of uranium-reducing bacteria and fungi in connection with the formation of economically important uranium ores.

Copper

The formation of sedimentary copper ores through biomineralization is still controversial and unambiguous reports on these proven biomineralized ores are rare. Copper, an element that is essential in the cellular electron control, is deadly for all life when found as a free ion since it can catalyze the production of damaging free radicals (Manceau et al. 2007). Because free copper ions are common in nature all life basically have evolved ways to control excess copper ions, but some better than others, and few as well as fungi and bacteria. Some copper-resistant plants and fungi have developed methods to place excess copper in root systems and/or leaves and many types of copper-resistant bacteria seem to eject it to its membrane so that it eventually forms a crust around its surface (Manceau et al 2007).

Some cyanobacteria have have special enzymes and proteins that use copper (azurin and plastocyanin), and this could possibly explain some sedimentary banded formations of copper formed in marine environments, making these formations BCM since the copper is built up and formed intracellular. However this hypothesis has not been verified (Ochai 1983).

Gold

Determining whether an ore of gold is of biogenetic origin has recently been a matter of debate. Observations of what appears to be bacterial pseudomorfic structures on secondary gold deposits have been made, but there is no real consensus on its origin (Southam et al. 2009, Reith et al. 2009). The theories on bacterial origin started to appear when studies on gold grain in placer deposits revealed that the grains found there where larger than those found in the bedrock of that was the source of the primary gold. Somehow the gold accumulated and the grains grew in size and this led to the idea of bacterial involvement (Southam et al. 2009).

The problem is that since gold also catalyzes the production of free radicals, it is just as deadly as copper for microbial life. So basically, just as in the case of copper, bacteria living in a gold rich environment will metabolize the gold bearing mineral (usually a sulfate like thiosulfate) and then precipitate the reduced gold and finally shredding this gold off the membrane to immobilize it (Rainbow 2006). However there are recent findings by Reith et al. (2009) that indicate a direct and intentional use of gold by bacteria. Laboratory experiments and observations on the bacteria Cupriavidus metallidurans actually confirmed its ability to directly respire on the gold complexes and precipitate reduced variations of gold without it being fatal for the bacteria.

Applications

Biomining & control of toxic minerals

The use of mineral reducing bacteria in the ore industry has two major applications today. Firstly, the bacteria can leach desired products by reducing them. By allowing the bacteria to metabolize on sulfides in a stirring tank or reactor, they can produce ferric iron and sulfuric acids. This acid can then be used to convert insoluble sulfides of for example copper, nickel and zinc to soluble metal sulfates that can be recovered from the solution (Rawlings et al. 2002). This process is referred to as biomining or bioleaching. Secondly, similar processes can be used to control pollutions of both soils and water where free ions that tend to acidify and pollute its environment can be bound. Bacteria can even be used to control and immobilize radioactive elements or minerals by reduction making them more difficult for other life forms to absorb (Frankel & Bazylinski 2003a).

Finding life

The different ways microbial life respires and also concentrate various forms of minerals provides science with an in depth understanding on how life evolved on Earth and how certain biominerals found in the strata can point to the indications of past life in Earth’s history (Frankel & Bazylinski 2003a). This gives rise to the possibility of connecting certain types of minerals found on other planets to biotic activity (especially oxides and sulfides). A growing number of scientists involved in studies of astrobiology today think that if detected on other planets, comets or asteroids, certain minerals and ores can point to the existence of life since they are deeply associated with bacterial activity (Blanco et al. 2006, Défarge 2007, Perry et al. 2007, Perez-Gonzales et al. 2009, Mandeville 2010). However, since most of these minerals can form abiotically in thermal vents and other chemically reactive environments (Kesler 2005), there is no definitive proof of life when detecting these minerals and ores here on Earth or on other planets.

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