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Magnetite: Structure, Properties and Applications: January 2011
Magnetite: Structure, Properties and Applications: January 2011
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ABSTRACT
Magnetic particles are of interest because they: occupy a unique position at the
interface of biology and chemistry, and hold high technological potential, i.e., they are
easily manipulated with only an external magnetic field. Many magnetic particles are
largely produced as a result of microbial iron metabolism, e.g., the low temperature
Banded Iron Formations – formed as a result of microbial activity in contrast to the
similar high temperature formations. The microbial origins of the Banded Iron
Formations are a fact that has only recently (in the last 30 years) been realized by
mainstream science. Particles of the mineral magnetite are among the most magnetic
that occur in nature. Magnetite is one of the most common products of microbial iron
metabolism, and it is, therefore, also a highly abundant mineral. In addition to being a
common end-product of microbial metabolism, magnetite is also known to be
incorporated into specialized organelles termed “magnetosomes.” These small magnets
are used for direction sensing by certain species of bacteria, i.e., magnetotactic
bacteria. The presence of magnetite in a Martian meteorite (ALH84001) was even
touted as evidence for life on Mars. Yet magnetite particles are also of interest in
biotechnology for everything from cell selection, e.g., stem cell tracking, differentiation
and biosensing, to a magnetic resonance imaging (MRI) contrast agent to drug
screening. Microbially-produced, nano-sized magnetite crystals are highly ordered
minerals consistent in size and morphology – characteristics that lend these particles
well to nano- and biotechnological applications. In this review, we examine various
forms of magnetite from its unique structures and properties to its many points of
relevance to biology and biotechnology.
INTRODUCTION
Over the past two decades there has been a marked increase in interest in biologically
mediated formation of iron (Fe) containing compounds and processes leading to the
biomineralization of iron minerals [1; 2; 3; 4]. This interest is in part due to the fact that
iron is a highly abundant element (the 2nd most abundant metal after aluminum and the
fourth most abundant element in the Earth’s crust) and also because many believe that
Fe(III) was the first external electron acceptor of global significance in microbial
respiration [5; 6; 7]. However, the role of iron in our planet’s natural history is far from
the only scientific appeal of iron and it mineral derivatives. From a biotechnological
perspective, magnetic iron oxide nanoparticles with appropriate surface chemistries are
ideal for use in numerous in vivo applications, such as: MRI contrast enhancement,
tissue repair, immunoassay, detoxification of biological fluids, hyperthermia, drug
delivery, and cell separation [8; 9]. One of the iron minerals of chief interest among all of
the entities composing the field of iron research is the naturally occurring iron oxide
magnetite. Magnetite is, as might be expected, 1) highly abundant, 2) a common by-
product/“secondary mineral” of metal metabolism/respiration, 3) utilized intracellularly by
a surprisingly large number of organisms, and 4) proposed for an ever-increasingly
large role in a number of biotechnological applications. The scope of this chapter is to
give a brief overview on various aspects of magnetite, especially its biologically-
mediated formation, and its applications.
What is Magnetite?
Iron (Fe), the first transition metal in group VIIIA of the periodic table, is one of the most
abundant elements on earth and is a major part (~4.7%) of the earth’s crust. Most iron-
containing minerals which form anaerobically contain iron in the Fe2+ oxidation state
(“ferro”). However, upon hydrolysis oxygen rapidly oxidizes the iron from its Fe2+ state to
Fe3+ (“ferric”) [3; 10]. Pure carbon-free metallic iron (the enantiotropic α-iron from) is
ferromagnetic, however, above 768oC it becomes paramagnetic and above 907oC it
converts to the enantiotropic γ-iron form [10; 11]. Carbon containing metallic iron can
also be made permanently magnetic, similar to steel. This form of magnetic iron is
different from magnetite, the focus of this chapter, and contains iron in both of its
oxidation states, i.e., Fe2+ and Fe3+ (which will from here be referred to as Fe(II) and
Fe(III), respectively). Iron can form a variety of oxide and oxyhydroxide phases leading
to varying, highly abundant mineral formations in terrestrial, aerobic habitats [12]. These
iron oxides exist in the form of minerals, some of the more common are: ferrihydrite,
lepidocrocite, maghemite, magnetite, hematite, and goethite [3; 13; 14; 15]. Although
iron can also exist in an amorphous iron oxyhydride form without a defined
stoichiometry of Fe(II)/Fe(III).
Magnetite is composed of Fe(II) and Fe(III) oxide typically denoted by ‘Fe3O4’ but more
appropriately expressed by its full notation ‘Fe(II)Fe(III)2O4’. Magnetite is one of the
most commonly occurring, ferromagnetic minerals on Earth. It is a member of the class
of minerals known as the ‘spinels’. These minerals have the general formulation
‘A2+B23+O42-‘, A and B can be divalent, trivalent, or quadrivalent cations, including
magnesium, zinc, iron, manganese, aluminum, chromium, titanium, and silicon. The
anion is normally oxide, and A and B can also be the same metal under different
charges, such as the case of magnetite ‘Fe(II)Fe(III)2O4’ (described above). Spinels
form in the isometric/cubic crystal system [16]. Magnetite is typically found in natural
terrestrial environments ranging from igneous and metamorphic rocks to all varieties of
sedimentary environments [17]. Magnetite is also found intracellularly in multiple
lineages of life: the Bacteria, the Protozoa, and the Animals [18; 19; 20; 21].
Additionally, magnetite has also been found in materials believed to be of
extraterrestrial origin, e.g., the Martian meteorite ALH84001 [17].
Figure 1. A Model for the Proposed Evolution of Magnetite Biomineralization. Geologic
time is shown along the vertical axis in billions of years along with some of the major events in
history that may have influenced magnetite biomineralization. These include (a) the origin of the
Earth at ~ 4.5 billion years ago (bya); (b) the oldest sedimentary rocks from the Isua complex of
Greenland at 3.8 bya; (c) the major deposition of the banded iron formations at 2.5-2.0 bya,
which presumably corresponds to the time in which the bulk of the deep oceanic water mass
changed from anaerobic to more aerobic conditions; (d) the endosymbiotic origin of eukaryotic
cells at about 1.6 bya; (e) the diversification of metazoan phyla at ~0.9 bya; and (f) the
widespread appearance of diverse biomineralization at the Precambrian-Cambrian boundary at
~0.6 bya (see Chang and Kirschvink [22]).
Structure of Magnetite
Magnetite is the most strongly magnetic mineral occurring in nature. Small particles of
magnetite in single-domain (SD) or pseudo-SD magnetization states (sizes in the range
of 30–70 nm and 70 nm to 20 µm, respectively) are the dominant carriers of
magnetization in sediments and rocks. Larger, multidomain particles are less likely to
maintain strong and stable natural magnetization over geological time as compared to
SD particles [23].
The structure of magnetite is often revealed using X-ray scattering and/or electron
diffraction studies [24; 25; 26]. However electron diffraction studies alone are not
accurate enough to unambiguously identify a mineral of interest, for example magnetite
and maghemite only present slight differences in their electron diffraction parameters.
For the differentiation of magnetite/maghemite for example, 57Fe Mössbauer
spectroscopy would be used [27]. Another technique that can convincingly differentiate
minerals such as magnetite from maghemite without requiring large amounts of the
mineral of interest is electron energy-loss spectroscopy [28]. This technique is able to
unravel the oxidation state of iron in a sample analyzed by transmission electron
microscopy [28].
Origins of Magnetite
Prokaryotes (both archaea and bacteria) biomineralize iron oxides, including magnetite,
through two methods that differ mechanistically: biologically-induced mineralization
(BIM) and biologically-controlled mineralization (BCM). Magnetite nanocrystals
produced by BIM are 1) known to be synthesized by dissimilatory iron-reducing
microorganisms (DIRM), 2) are deposited external to the cell, and 3) are generally
physically indistinguishable from magnetite particles formed inorganically [24; 36; 37]. In
the past, BCM has been referred to as “organic matrix-mediated mineralization” [32],
and “boundary-organized biomineralization” -- implying membranes play an important
role in the biomineralization process [38]. BCM magnetite is synthesized by the
magnetotactic bacteria and is precipitated intracellularly as membrane-bound
structures called ‘magnetosomes’. Magnetosome magnetite appears to have a crystal
morphology and narrow size range unique to the bacterium producing it [26; 39; 40].
The magnetotactic bacteria will be discussed after the description of DIRM.
Presently DIRM have been isolated from a relatively wide number of unique and
ubiquitous habitats (Table 1), including mesophilic and thermophilic (with isolates able
to grow above the boiling point of water [56; 57; 58]); anaerobic and aerobic soils and
sediments, soda lakes, thermal springs, etc. [2; 3; 59; 60; 61; 62; 63; 64; 65]. Magnetite
is produced by a number of iron-reducing microorganisms, including: several species of
Shewanella [64; 66; 67; 68] and Geobacter [37; 66; 69; 70], Ferribacterium limneticum
[61], Geoalkalibacter ferrihydriticus [59], Alkaliphilus metalliredigens [60], and
Thermolithobacter ferrireducens [2]. Unlike the BCM magnetite produced by the
magnetotactic bacteria, there does not appear to be any functional use that can be
ascribed to BIM particles.
Of particular interest are thermophilic, iron-reducing, chemolithoautotrophs, i.e.,
microorganisms capable of growth utilizing only CO2, H2, and amorphous iron oxides
alone [2; 36; 71; 72; 73]. These DIRM are likely to have been involved in the
precipitation of the Precambrian era, low temperature BIF [54; 55]. Thermophilic,
autotrophic, DIRM may also be much more prevalent than currently reported, and may
exist in biosphere pockets deep within the Earth (and possibly other planets, see
“Possible Extraterrestrial Origins? below”) [4; 74]. A number of groups [71; 72; 73; 75;
76; 77] have focused on the isolation and characterization of these chemolithotrophic
metal-reducing (specifically iron-reducing) strains from deep subsurface environments
over the past decade. From these studies and others, a number of novel
microorganisms have been isolated, characterized, and studied.
Table 1. Dissimilatory Iron-Reducing Microorganims which Biomineralize Magnetite.
*Several species, and strains of species, of Shewanella and Geobacter are known to produce
magnetite. NR = Not reported.
Magnetotactic Organisms. Magnetotactic bacteria synthesize intracellular magnetic
particles composed of iron oxides and/or iron sulfides, the most common examples
include magnetite (Fe3O4) and greigite (Fe3S4), respectively [1; 78]. The nano-sized
particles are actually highly specialized, membrane-enveloped organelles [79; 80].
Unlike the magnetite nanoparticles synthesized by the dissimilatory iron-reducing
microorganisms through BIM, the magnetite produced by the magnetotactic bacteria is
biomineralized intracellularly in vesicles which originate from invaginations of the cell
membrane [81; 82]. After the first report of magnetotactic bacteria by [30], X-ray and
electron diffraction, 57Fe Mössbauer spectroscopy, and direct lattice imaging studies
showed that the intracellular iron particles of these bacteria are invariably made of
magnetic iron-containing particles, i.e., magnetite, despite a wide range of biologically
unique crystal morphologies and sizes [1; 25; 26]. These magnetic organelles, or
magnetosomes as they are often referred, are aligned in chains within a bacterium and
are postulated to function as biological compasses that enable the bacterium to migrate
along oxygen gradients in aquatic environments under the influence of the Earth’s
magnetic field [1; 26; 30; 80; 83]. Not surprisingly, the features of BCM magnetite differ
greatly from those produced by the DIRM. BCM magnetite has both high chemical purity
and structural perfection coupled with magnetic properties that differ from those
produced through BIM [84; 85; 86; 87; 88]. It is interesting to note that in sediment
obtained from the Southern Hemisphere, the majority of the magnetotactic bacteria
swim to the South Pole [89]. Whereas in samples obtained from the Northern
Hemisphere, they swim in the direction of the North Pole [30; 31]. However, exceptions
to this North Pole vs. South Pole swimming bias are known (for an example see [90]).
Some of the best-developed techniques for the synthesis of inorganic magnetite involve
its synthesis as a primary mineral phase. The precipitation of magnetite from a bulk
solution is highly effective and large quantities of the mineral can be produced. A
number of different methods accomplish the precipitation of magnetite from bulk
solutions. These techniques differ mainly in how the Fe(II) is introduced into the
solution. But all of these methods are dependent on controlling the pH and
alkalinity/concentration of CO2, i.e., conditions required for the stability of magnetite, in
the solution [8].
Figure 2. Electron micrographs of various magnetotactic bacteria and their
magnetosome chains. The images represent some of the diversity seen in the cell morphology
of the magnetosomes, and of the arrangement of the magnetosomes in the bacteria: (a)
spirillum with a single chain of cubooctahedral magnetosomes, (b) coccus with two double
chains of slightly elongated prismatic magnetosomes, (c) coccus with clustered, elongated
magnetosomes, (d) vibrio with elongated prismatic or cubooctahedral magnetosomes arranged
in a single chain, (e) vibrio with two chains, and (f) rod-shaped bacterium with bullet-shaped
magnetosomes arranged in a multitude of chains. Scale bars in (a-f) represent 1 μm. Part g
shows a chain from a similar type of MTB as in part a, and part h shows one from a bacterium
as in part b. Scale bars in parts g-h represent 100 nm. Images are reprinted from Faivre and
Schuler [26] with permission from the American Chemical Society.
For bulk solution “co-precipitation”, Fe(II) and Fe(III) mixtures are introduced in a
starting solution under anaerobic conditions. In order to maintain the appropriate
alkaline pH for the stability of the magnetite, NH3 [95; 96; 97], NaOH [95; 98; 99],
NH4OH [100], or N(CH3)4OH [95] are employed. Interestingly when employing this
technique it is not uncommon for magnetite crystals of several different morphologies
(dependent on the exact conditions employed) to form; including cubic, rounded,
octahedral and/or irregular [95]. When more uniform crystals of magnetite are required,
modifications of the bulk “co-precipitation” technique can be applied. These
modifications rely upon limiting the space available for crystal growth by performing the
precipitation of magnetite in microemulsions, vesicles, polymer solutions, or gels [101;
102; 103; 104].
Other methods for the inorganic precipitation of magnetite as a primary mineral are:
“reduction-precipitation”, the use of constant voltage (the “electrochemical” method),
and high temperature precipitation. The “reduction-precipitation” technique involves the
precipitation of magnetite by the addition of iron as an Fe(III) solution, i.e., FeCl3. The
ferric ions are reduced to ferrous ions, e.g., by Na2SO3, followed by an increase in pH
under strictly anaerobic conditions [105; 106; 107], or a constant voltage can applied to
reduce Fe(III) ions and to obtain the necessary conditions to produce magnetite [108].
Finally, magnetite can be precipitated at 90ºC using an Fe(II) solution (such as FeSO4)
and the addition of KNO3 or N2H4 [106; 109].
Magnetite formation as a secondary mineral phase, as might be assumed, involves
the transformation of iron-bearing, primary mineral phases to magnetite at high or low
temperatures. Low temperature (20- 30°C) magnetite forms by the transformation of
ferrihydrite and/or green rust [66]. Magnetite formation through reactions between
soluble iron hydroxides and amorphous iron oxyhyroxide has also been reported [110].
In addition, the thermal decomposition of siderite or other Fe-rich carbonate phases at
highly elevated temperatures (>400°C) has been shown to result in the formation of
magnetite [111; 112; 113]. This latter mechanism of magnetite formation has been
invoked in connection with the controversy over the origin of magnetite crystals
contained within the Martian meteorite ALH84001 [93].
Possible Extraterrestrial Origins?
The reported similarity of the nanometer-sized magnetite crystals of the Martian
meteorite ALH84001 [93; 114; 115; 116] to the biogenic magnetite incorporated into the
magnetosomes of magnetotactic bacteria has raised significant scientific debate. At the
center of this debate is whether 1) these Martian meteorite magnetite crystals are
evidence for the presence of life on ancient Mars, and 2) what criteria can and will be
used to distinguish between the biological and inorganic origins of magnetite crystals.
The use of six criteria, first proposed by [17], are used by many (but not all) researchers
for the determination of whether certain magnetite crystals possibly constitute a
biomarker for life. Collectively these criteria are referred to as the magnetite assay for
biogenicity (MAB) and include 1) a narrow crystal size range, 2) consistent width/length
ratios, 3) chemical purity, 4) crystallographic perfection, 5) unusual crystal morphology,
and 6) directional crystal elongation [17; 103; 117; 118]. Thomas-Keprta et al. [17]
further suggest that these criteria comprise a rather restrictive and robust biosignature
since >30% of magnetites produced by a magnetotactic bacterial strain would not
display all six of these properties, i.e., would not be confirmed as biogenic precipitates.
Thomas-Keprta et al. propose that up to 25% of the magnetite crystals in the globular
carbonate globules of ALH84001 display all six of the properties with the remaining 75%
of the magnetites lacking sufficient characteristics to constrain their origin as either
biogenic and/or inorganic [17; 119]. However, there is an abiotic hypothesis, which has
been developed by a number groups, for the formation of the magnetite crystals within
ALH84001 [112; 120; 121].
More recently, Thomas-Keprta et al. [113] sought to resolve the debate between the
abiotic, i.e., thermal decomposition, and biotic origin of the ALH84001 magnetite
crystals. These authors performed a detailed characterization of the compositional and
structural relationships of the carbonate disks and associated magnetite crystals of
ALH84001. They then compared their observations with experimental thermal
decomposition studies [123; 124] under a range of plausible geological heating
scenarios. From their experiments, Thomas-Keprta et al. [113] concluded that the vast
majority of the nanocrystal magnetites present in the carbonate disks could not have
formed by any of the currently proposed thermal decomposition scenarios. They go on
to indicate their evidence supports an alternative allochthonous origin for this magnetite
unrelated to any shock or thermal processing of carbonates.
Evidence contrary to the biogenic origin of the ALH84001 magnetite has also been
produced that does not intrinsically invoke the abiotic, thermal decomposition origin as
an alternative. Weiss et al. [125] suggested that the ALH84001 magnetite fulfills only
two of the six criteria described by Thomas-Keprta et al. [17; 115]: high chemical purity
and an unusually fine-grained (single-domain to superparamagnetic) size
distribution/range. Weiss et al. [125] went on to indicate the magnetic measurements
they made show that no more than ~10% of the magnetite in ALH84001 can be in
isolated chains, one of the most distinctive properties of magnetosomes (BCM
magnetite) [126]. Therefore the results of Weiss et al. [125] suggest a difficulty in
definitively proving that ALH84001 magnetites are magnetosome in origin. However,
even these authors confess that in terrestrial sediments more than half of the
magnetosome chain structures present could have been disrupted [127]. The claim
made by Thomas-Keptra et al. [17] that ~27% of the ALH84001 magnetite crystals are
biogenic can not yet be ruled out.
Thus, there are credible arguments and supporters for both the biogenic and abiogenic
hypotheses for the origin of the crystals of magnetite in the ALH84001 meteorite. A
more definitive answer to the origin of these magnetite crystals will involve further
examination of the ALH84001 meteorite and other ancient Martian meteorites as well as
further study of BCM magnetite/magnetosomes.
.
Applications of Magnetite
Magnetic iron oxide particles, such as magnetite or maghemite (γ-Fe2O3), are widely
used in the development of medical and diagnostic applications such as magnetic
resonance imaging [128], cell separation [129], drug delivery [130] and hyperthermia
[131].
Conclusion
In the last two decades, there has been an increased focus on the study of magnetite
synthesis by prokaryotes, including both the dissimilatory iron-reducing microorganisms
(DIRM) and the magnetotactic bacteria. The magnetite crystals biomineralized by these
two classes of microorganisms, i.e., the DIRM: biologically-induced mineralization
(BIM) magnetite, and the magnetotactic bacteria: biologically-controlled
mineralization (BCM) magnetite, differ in a great number of ways, e.g., BCM
magnetite biomineralization is tightly regulated, in contrast to BIM magnetite
biomineralization, to produce crystals with a uniform crystal morphology and narrow
size range. Surprisingly magnetite crystals have even been found in the higher
organisms, from the Protozoa to even humans. The possible use of nanometer-sized
crystals of magnetite as magnetofossils, biosignatures for the past presence of life, is
intriguing and led to vigorous debates. Through all of these findings and studies, much
has been learned about how organisms biomineralize magnetite and how magnetite is
formed inorganically. However much remains to be discovered. Many parameters must
affect the chemical composition, crystal morphology and mineral structure of magnetite.
The studies of these parameters will lead to increased applications for magnetite in
industry and technology, a better understanding of how, and if, magnetite nanocrystals
can be studied as magnetofossils, and the full scope of iron metabolism by dissimilatory
iron-reducing microorganisms in the origin of life, e.g., the use of Fe(III) as a primordial
and relatively efficient external electron acceptor before the advent of the more efficient
electron acceptor oxygen at sufficient concentrations.
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