Magnetotactic bacteria
Encyclopedia
Magnetotactic bacteria are a polyphyletic group of bacteria
discovered by Richard P. Blakemore in 1975, that orient along the magnetic field lines
of Earth's magnetic field
. To perform this task, these bacteria have organelle
s called magnetosome
s that contain magnetic crystals. The biological phenomenon of microorganisms tending to move in response to the environment's magnetic characteristics is known as magnetotaxis
(although this term is misleading in that every other application of the term taxis
involves a stimulus-response mechanism). In contrast to the magnetoception
of animals, the bacteria contain fixed magnets that force the bacteria into alignment — even dead cells align, just like a compass needle. The alignment is believed to aid these organisms in reaching regions of optimal oxygen concentration.
written by Salvatore Bellini. While observing bog sediments under his microscope, he noticed a group of bacteria that evidently oriented themselves in a unique direction. He realised these microorganisms moved according to the direction of the North Pole
, and hence called them "magnetosensitive bacteria".
The first peer-reviewed article on magnetotactic bacteria appeared in a 1975 article in Science by Richard Blakemore, a microbiologist
at the Woods Hole Oceanographic Institution
, who had similarly observed bacteria capable of orienting themselves in a certain direction: Blakemore realised that these microorganisms were following the direction of Earth's magnetic field, from south to north, and thus coined the term "magnetotactic".
These bacteria have been the subject of many experiments: They have even been aboard the Space Shuttle
to examine their magnetotactic properties in the absence of gravity, but a definitive conclusion was not reached.
The sensitivity of magnetotactic bacteria to the Earth's magnetic field
arises from the fact these bacteria precipitate chains of crystals of magnetic minerals within their cells; to date, all magnetotactic bacteria are reported to precipitate either magnetite
or greigite
. These crystals, and sometimes the chains of crystals, can be preserved in the geological record as magnetofossils
. The oldest unambiguous magnetofossils come from the Cretaceous
chalk beds of southern England, though less certain reports of magnetofossils extend to 1.9 billion years old Gunflint Chert
. There have also been claims of their existence on Mars
based on the shape of magnetite
particles within the Martian meteorite ALH84001
, but these claims are highly contested.
(Fe3O4) or of greigite
(Fe3S4), although some species are capable of producing both. Magnetite possesses a magnetic moment
three times that of greigite.
Magnetite-producing magnetotactic bacteria are usually found in an oxic-anoxic transition zone (OATZ), the transition zone between oxygen-rich and oxygen-starved water or sediment. Many MTB are able to survive only in environments with very limited oxygen, and some can exist only in completely anaerobic environments. It has been postulated that the evolutionary advantage of possessing a system of magnetosomes is linked to the ability of efficiently navigating within this zone of sharp chemical gradients by simplifying a potential three-dimensional search for more favourable conditions to a single dimension (see the "Magnetism" subsection below for a description of this mechanism). Some types of magnetotactic bacteria can produce magnetite even in anaerobic
conditions, using nitric oxide
, nitrate
, or sulfate
as a final acceptor for electron
s. The greigite mineralising MTBs are usually strictly anaerobic.
It has been suggested MTB evolved in the early Proterozoic
Era, as the increase in atmospheric oxygen reduced the quantity of dissolved iron in the oceans. Organisms began to store iron in some form, and this intracellular iron was later adapted to form magnetosomes for magnetotaxis. These early MTB may have participated in the formation of the first eukaryotic cells. Biogenic magnetite not too different from that found in magnetotactic bacteria has been also found in higher organisms, from Euglenoid algae
, to salmon
, pigeons, and humans.
Magnetotactic bacteria produce their magnetic particles in chains. The magnetic dipole of the cell is therefore the sum of the dipoles of each BMP, which is then sufficient to passively orient the cell and overcome the casual thermal forces found in a water environment. In the presence of more than one chain, the inter-chain repulsive forces will push these structures to the edge of the cell, inducing turgor.
The diversity of MTB is reflected by the high number of different morphotypes found in environmental samples of water or sediment. Commonly observed morphotypes include spherical or ovoid cells (cocci
), rod-shaped (bacilli
), curved bacteria (vibrio
) and helical (spirillum
) of various dimensions. One of the more distinctive morphotypes is an apparently multicellular bacterium referred to as the many-celled magnetotactic prokaryote (MMP). Regardless of their morphology, all MTB studied so far are motile by means of flagella are Gram-negative
bacteria of various phyla: Despite the majority of known species' being proteobacteria
, e.g. Magnetospirillum magneticum an alphaproteobacterium, members of various phyla possess the magnetosome gene cluster, such as Candidatus Magnetobacterium bavaricum a Nitrospira. The arrangement of flagella differs and can be polar, bipolar, or in tufts. The first phylogenetic analysis on magnetotactic bacteria using 16SrRNA gene sequence comparisons was performed by P. Eden et al. in 1991.
Another trait that shows considerable diversity is the arrangement of magnetosomes inside the bacterial cell. In the majority of MTB, the magnetosomes are aligned in chains of various lengths and numbers along the cell's long axis, which is magnetically the most efficient orientation. However, dispersed aggregates or clusters of magnetosomes occur in some MTB, usually at one side of the cell, which often corresponds to the site of flagellar insertion. Besides magnetosomes, large inclusion bodies containing elemental sulfur
, polyphosphate
, or poly-β-hydroxybutyrate are common in MTB.
The most abundant type of MTB occurring in environmental samples, especially sediments, are coccoid cells possessing two flagellar bundles on a somewhat flattened side. This "bilophotrichous" type of flagellation gave rise to the tentative genus "Bilophococcus" for these bacteria. In contrast, two of the morphologically more conspicuous MTB, regularly observed in natural samples, but never isolated in pure culture, are the MMP and a large rod containing copious amounts of hook-shaped magnetosomes (Magnetobacterium bavaricum).
is governed by two factors: one is moving to align the magnetic force of the molecules in conjunction with the developing crystal, while the other reduces the magnetic force of the crystal, allowing an attachment of the molecule while experiencing an opposite magnetic force. In nature, this causes the existence of a magnetic domain, surrounding the perimeter of the domain, with a thickness of approximately 150 nm of magnetite, within which the molecules gradually change orientation. For this reason, the iron
is not magnetic in the absence of an applied field. Likewise, extremely small magnetic particles do not exhibit signs of magnetisation at room temperature; their magnetic force is continuously altered by the thermal motions inherent in their composition. Instead, individual magnetite crystals in MTB are of a size between 35 and 120 nm, that is, large enough to have a magnetic field and at the same time small enough to remain a single magnetic domain
.
The inclination of the Earth's magnetic field in the two respective hemispheres selects one of the two possible polarities of the magnetotactic cells (with respect to the flagellated pole of the cell), orienting the biomineralisation of the magnetosome
s. Various experiments have clearly shown that magnetotaxis
and aerotaxis work in conjunction in the magnetotactic bacteria. Aerotaxis is the response by which bacteria migrate to an optimal oxygen concentration in an oxygen gradient. It has been shown that, in water droplets, one-way swimming magnetotactic bacteria can reverse their swimming direction and swim backwards under reducing conditions (less than optimal oxygen concentration), as opposed to oxic conditions (greater than optimal oxygen concentration). The behaviour that has been observed in these bacterial strains has been referred to as magneto-aerotaxis.
Two different magneto-aerotactic mechanisms — known as polar and axial — are found in different MTB strains. Some strains that swim persistently in one direction along the magnetic field (either north-seeking [NS] or south-seeking [SS]) — mainly the magnetotactic cocci — are polar magneto-aerotactic. These magnetotactic bacteria will travel along the lines of the earth’s magnetic field according to their orientation, but will swerve as a group and reverse direction if exposed to a local, more powerful and oppositely-oriented magnetic field. In this way, they continue to travel in the same magnetic direction , but relative instead to the local field. Those MTB that swim in either direction along magnetic field lines with frequent, spontaneous reversals of swimming direction without turning around — for example, freshwater spirilla — are axial magneto-aerotactic and the distinction between NS and SS does not apply to these bacteria. The magnetic field provides both an axis and a direction of motility for polar magneto-aerotactic bacteria, whereas it only provides an axis of motility for axial types of bacteria. In both cases, magnetotaxis increases the efficiency of aerotaxis in vertical concentration gradients by reducing a three-dimensional search to a single dimension.
Scientists have also proposed an extension of the described model of magneto-aerotaxis to a more complex redoxtaxis. In this case, the unidirectional movement of MTB in a drop of water would be only one aspect of a sophisticated redox-controlled response. One hint for the possible function of polar magnetotaxis could be that most of the representative microorganisms are characterised by possessing either large sulfur inclusions or magnetosomes consisting of iron-sulfides. Therefore, it may be speculated the metabolism of these bacteria, being either chemolithoautotrophic or mixotrophic, is strongly dependent on the uptake of reduced sulfur compounds, which occurs in many habitats only in deeper regions at or below the OATZ due to the rapid chemical oxidation of these reduced chemical species by oxygen or other oxidants in the upper layers.
Microorganisms belonging to the genus Thioploca
, for example, use nitrate, which is stored intracellularly, to oxidize sulfide, and have developed vertical sheaths in which bundles of motile filaments are located. It is assumed that Thioploca uses these sheaths to efficiently move in a vertical direction in the sediment, thereby accumulating sulfide in deeper layers and nitrate in upper layers. For some MTB, it might also be necessary to perform excursions to anoxic zones of their habitat to accumulate reduced sulfur compounds.
of the magnetite requires regulating mechanisms to control the concentration of iron, the crystal nucleation
, the redox potential and the pH
. This is achieved by means of compartmentalisation in structures known as magnetosomes that allow the biochemical control of the above mentioned processes. After the genome
of several MTB species had been sequenced, a comparative analysis of the protein
s involved in the formation of the BMP became possible. Sequence homology with proteins belonging to the ubiquitous cation diffusion facilitator (CDF) family and the "Htr-like" serine protease
s has been found: While the first group is exclusively dedicated to the transport of heavy metals, the second group consists of heat shock protein
s (HSPs) involved in the degradation of badly folded
proteins. Other than the serine protease domain, some proteins found in the magnetosomial membrane (MM) also contain PDZ domains, while several other MM proteins contain tetratrico peptide repeat (TPR) domains.
and include a highly conserved consensus sequence
of 8 amino acid
s (of the 34 possible), which is the most common in nature. Apart from these amino acids, the remainder of the structure is found to be specialised in relation to its functional significance. The more notable compounds that comprise TPR domains include:
Examples of both the TPR-TPR interactions, as well as TPR-nonTPR interactions, have been reported.
, thus preventing interaction with the PDZ domain. The only conserved residues in these structures are those involved in the recognition of the carboxy terminal. PDZ domains are quite widespread in nature, since they constitute the basic structure upon which multiproteinic complexes are assembled: This is especially true for those associated with membrane proteins, such as the inward rectifier K+ channels
or the β2-adrenergic
receptors.
During the first formation of an invagination
in the cytoplasmic membrane is triggered by a GTPase
. It is supposed this process can take place amongst eukaryote
s, as well.
The second step requires the entrance of ferric ion
s into the newly formed vesicle
s from the external environment. Even when cultured in a Fe3+ deficient medium, MTB succeed at accumulating high intracellular concentrations of this ion. It has been suggested that they accomplish this by secreting, upon need, a siderophore
, a low-molecular-weight ligand displaying an elevated affinity for Fe3+ ions. The "Fe3+-siderophore" complex is subsequently moved in the cytoplasm
, where it is cleaved. The ferric ions must then be converted into the ferrous form (Fe2+), to be accumulated within the BMP; this is achieved by means of a transmembrane transporter, which exhibits sequence homology with a Na+/H+ antiporter
. Furthermore, the complex is a H+/Fe2+ antiporter, which transports ions via the proton gradient. These transmembrane transporters are localised both in the cytoplasmic membrane and in the MM, but with in an inverted orientation; this configuration allows them to generate an efflux of Fe2+ ions at the cytoplasmic membrane, and an influx of this same ion at the MM. This step is strictly controlled by a cytochrome
-dependent redox system, which is not yet fully explained and appears to be species-specific.
During the final stage of the process, the magnetite crystal nucleation is by action of transmembrane proteins with acidic and basic domains. One of these proteins, called Mms6, has also been employed for the artificial synthesis of magnetite, where its presence allows the production of crystals homogeneous in shape and size.
It is likely that many other proteins associated with the MM could be involved in other roles, such as generation of supersaturated concentrations of iron, maintenance of reducing conditions, oxidisation of iron, and partial reduction and dehydration of hydrated iron compounds.
and sulfur are not interchangeable as nonmetallic substances of the magnetosome within the same species.
From a thermodynamic
point of view, in the presence of a neutral pH and a low redox potential, the inorganic synthesis of magnetite is favoured when compared to those of other iron oxide
s. It would thus appear microaerophilic
or anaerobic
conditions create a suitable potential for the formation of BMPs. Moreover, all iron absorbed by the bacteria is rapidly converted into magnetite, indicating the formation of crystals is not preceded by the accumulation of intermediate iron compounds; this also suggests the structures and the enzyme
s necessary for biomineralisation are already present within the bacteria. These conclusions are also supported by the fact that MTB cultured in aerobic conditions (and thus nonmagnetic) contain amounts of iron comparable to any other species of bacteria.
s. The magnetosome envelope allows for easy couplings of bioactive substances to its surface, a characteristic important for many applications.
Magnetotactic bacterial cells have been used to determine south magnetic poles in meteorites and rocks containing fine-grained magnetic minerals and for the separation of cells after the introduction of magnetotactic bacterial cells into granulocyte
s and monocyte
s by phagocytosis. Magnetotactic bacterial magnetite crystals have been used in studies of magnetic domain analysis and in many commercial applications including: the immobilisation of enzymes; the formation of magnetic antibodies, and the quantification of IgG; the detection and removal of Escherichia coli
cells with a fluorescein isothiocyanate
conjugated monoclonal antibody, immobilised on magnetotactic bacterial magnetite particles; and the introduction of genes into cells, a technology in which magnetosomes are coated with DNA and "shot" using a particle gun into cells that are difficult to transform using more standard methods.
However, the prerequisite for any large-scale commercial application is mass cultivation of magnetotactic bacteria or the introduction and expression of the genes responsible for magnetosome synthesis into a bacterium, e.g., E. coli, that can be grown relatively cheaply to extremely large yields. Although some progress has been made, the former has not been achieved with the available pure cultures.
Bacteria
Bacteria are a large domain of prokaryotic microorganisms. Typically a few micrometres in length, bacteria have a wide range of shapes, ranging from spheres to rods and spirals...
discovered by Richard P. Blakemore in 1975, that orient along the magnetic field lines
Magnetic field
A magnetic field is a mathematical description of the magnetic influence of electric currents and magnetic materials. The magnetic field at any given point is specified by both a direction and a magnitude ; as such it is a vector field.Technically, a magnetic field is a pseudo vector;...
of Earth's magnetic field
Earth's magnetic field
Earth's magnetic field is the magnetic field that extends from the Earth's inner core to where it meets the solar wind, a stream of energetic particles emanating from the Sun...
. To perform this task, these bacteria have organelle
Organelle
In cell biology, an organelle is a specialized subunit within a cell that has a specific function, and is usually separately enclosed within its own lipid bilayer....
s called magnetosome
Magnetosome
Magnetosome chains are membranous prokaryotic organelles present in magnetotactic bacteria. They contain 15 to 20 magnetite crystals that together act like a compass needle to orient magnetotactic bacteria in geomagnetic fields, thereby simplifying their search for their preferred microaerophilic...
s that contain magnetic crystals. The biological phenomenon of microorganisms tending to move in response to the environment's magnetic characteristics is known as magnetotaxis
Magnetotaxis
Logically, magnetotaxis describes an ability to sense a magnetic field and coordinate movement in response. It was applied to the behavior of certain motile, aquatic bacteria in 1975 by R. P. Blakemore....
(although this term is misleading in that every other application of the term taxis
Taxis
A taxis is an innate behavioral response by an organism to a directional stimulus or gradient of stimulus intensity. A taxis differs from a tropism in that the organism has motility and demonstrates guided movement towards or away from the stimulus source ...
involves a stimulus-response mechanism). In contrast to the magnetoception
Magnetoception
Magnetoception is the ability to detect a magnetic field to perceive direction, altitude or location. This sense plays a role in the navigational abilities of several animal species and has been postulated as a method for animals to develop regional maps.Magnetoception is most commonly observed in...
of animals, the bacteria contain fixed magnets that force the bacteria into alignment — even dead cells align, just like a compass needle. The alignment is believed to aid these organisms in reaching regions of optimal oxygen concentration.
Introduction
The first description of magnetotactic bacteria appeared in 1963 in a publication of the Microbiology Institute of the University of PaviaUniversity of Pavia
The University of Pavia is a university located in Pavia, Lombardy, Italy. It was founded in 1361 and is organized in 9 Faculties.-History:...
written by Salvatore Bellini. While observing bog sediments under his microscope, he noticed a group of bacteria that evidently oriented themselves in a unique direction. He realised these microorganisms moved according to the direction of the North Pole
North Pole
The North Pole, also known as the Geographic North Pole or Terrestrial North Pole, is, subject to the caveats explained below, defined as the point in the northern hemisphere where the Earth's axis of rotation meets its surface...
, and hence called them "magnetosensitive bacteria".
The first peer-reviewed article on magnetotactic bacteria appeared in a 1975 article in Science by Richard Blakemore, a microbiologist
Microbiology
Microbiology is the study of microorganisms, which are defined as any microscopic organism that comprises either a single cell , cell clusters or no cell at all . This includes eukaryotes, such as fungi and protists, and prokaryotes...
at the Woods Hole Oceanographic Institution
Woods Hole Oceanographic Institution
The Woods Hole Oceanographic Institution is a private, nonprofit research and higher education facility dedicated to the study of all aspects of marine science and engineering and to the education of marine researchers. Established in 1930, it is the largest independent oceanographic research...
, who had similarly observed bacteria capable of orienting themselves in a certain direction: Blakemore realised that these microorganisms were following the direction of Earth's magnetic field, from south to north, and thus coined the term "magnetotactic".
These bacteria have been the subject of many experiments: They have even been aboard the Space Shuttle
Space Shuttle
The Space Shuttle was a manned orbital rocket and spacecraft system operated by NASA on 135 missions from 1981 to 2011. The system combined rocket launch, orbital spacecraft, and re-entry spaceplane with modular add-ons...
to examine their magnetotactic properties in the absence of gravity, but a definitive conclusion was not reached.
The sensitivity of magnetotactic bacteria to the Earth's magnetic field
Earth's magnetic field
Earth's magnetic field is the magnetic field that extends from the Earth's inner core to where it meets the solar wind, a stream of energetic particles emanating from the Sun...
arises from the fact these bacteria precipitate chains of crystals of magnetic minerals within their cells; to date, all magnetotactic bacteria are reported to precipitate either magnetite
Magnetite
Magnetite is a ferrimagnetic mineral with chemical formula Fe3O4, one of several iron oxides and a member of the spinel group. The chemical IUPAC name is iron oxide and the common chemical name is ferrous-ferric oxide. The formula for magnetite may also be written as FeO·Fe2O3, which is one part...
or greigite
Greigite
Greigite is an iron sulfide mineral with formula Fe3S4. It is the sulfur equivalent of the iron oxide magnetite . It was first described in 1964 for an occurrence in San Bernardino County, California, and named after the mineralogist and physical chemist Joseph W...
. These crystals, and sometimes the chains of crystals, can be preserved in the geological record as magnetofossils
Magnetofossils
Magnetofossils are the fossil remains of magnetic particles produced by magnetotactic bacteria and preserved in the geologic record. The oldest definitive magnetofossils formed of the mineral magnetite come from the Cretaceous chalk beds of southern England, while magnetofossil reports not...
. The oldest unambiguous magnetofossils come from the Cretaceous
Cretaceous
The Cretaceous , derived from the Latin "creta" , usually abbreviated K for its German translation Kreide , is a geologic period and system from circa to million years ago. In the geologic timescale, the Cretaceous follows the Jurassic period and is followed by the Paleogene period of the...
chalk beds of southern England, though less certain reports of magnetofossils extend to 1.9 billion years old Gunflint Chert
Gunflint Chert
The Gunflint chert is a sequence of banded iron formation rocks that are exposed in the Gunflint Range of northern Minnesota and northwestern Ontario along the north shore of Lake Superior. The black layers in the sequence contain microfossils that are 1.9 to 2.3 billion years in age. Stromatolite...
. There have also been claims of their existence on Mars
Mars
Mars is the fourth planet from the Sun in the Solar System. The planet is named after the Roman god of war, Mars. It is often described as the "Red Planet", as the iron oxide prevalent on its surface gives it a reddish appearance...
based on the shape of magnetite
Magnetite
Magnetite is a ferrimagnetic mineral with chemical formula Fe3O4, one of several iron oxides and a member of the spinel group. The chemical IUPAC name is iron oxide and the common chemical name is ferrous-ferric oxide. The formula for magnetite may also be written as FeO·Fe2O3, which is one part...
particles within the Martian meteorite ALH84001
ALH84001
Allan Hills 84001 is a meteorite that was found in Allan Hills, Antarctica on December 27, 1984 by a team of U.S. meteorite hunters from the ANSMET project. Like other members of the group of SNCs , ALH 84001 is thought to be from Mars. However, it does not fit into any of the previously...
, but these claims are highly contested.
Biology
Several different morphologies (shapes) of MTB exist, differing in number, layout and pattern of the bacterial magnetic particles (BMPs) they contain. The MTBs can be subdivided into two categories, according to whether they produce particles of magnetiteMagnetite
Magnetite is a ferrimagnetic mineral with chemical formula Fe3O4, one of several iron oxides and a member of the spinel group. The chemical IUPAC name is iron oxide and the common chemical name is ferrous-ferric oxide. The formula for magnetite may also be written as FeO·Fe2O3, which is one part...
(Fe3O4) or of greigite
Greigite
Greigite is an iron sulfide mineral with formula Fe3S4. It is the sulfur equivalent of the iron oxide magnetite . It was first described in 1964 for an occurrence in San Bernardino County, California, and named after the mineralogist and physical chemist Joseph W...
(Fe3S4), although some species are capable of producing both. Magnetite possesses a magnetic moment
Magnetic moment
The magnetic moment of a magnet is a quantity that determines the force that the magnet can exert on electric currents and the torque that a magnetic field will exert on it...
three times that of greigite.
Magnetite-producing magnetotactic bacteria are usually found in an oxic-anoxic transition zone (OATZ), the transition zone between oxygen-rich and oxygen-starved water or sediment. Many MTB are able to survive only in environments with very limited oxygen, and some can exist only in completely anaerobic environments. It has been postulated that the evolutionary advantage of possessing a system of magnetosomes is linked to the ability of efficiently navigating within this zone of sharp chemical gradients by simplifying a potential three-dimensional search for more favourable conditions to a single dimension (see the "Magnetism" subsection below for a description of this mechanism). Some types of magnetotactic bacteria can produce magnetite even in anaerobic
Hypoxia (environmental)
Hypoxia, or oxygen depletion, is a phenomenon that occurs in aquatic environments as dissolved oxygen becomes reduced in concentration to a point where it becomes detrimental to aquatic organisms living in the system...
conditions, using nitric oxide
Nitric oxide
Nitric oxide, also known as nitrogen monoxide, is a diatomic molecule with chemical formula NO. It is a free radical and is an important intermediate in the chemical industry...
, nitrate
Nitrate
The nitrate ion is a polyatomic ion with the molecular formula NO and a molecular mass of 62.0049 g/mol. It is the conjugate base of nitric acid, consisting of one central nitrogen atom surrounded by three identically-bonded oxygen atoms in a trigonal planar arrangement. The nitrate ion carries a...
, or sulfate
Sulfate
In inorganic chemistry, a sulfate is a salt of sulfuric acid.-Chemical properties:...
as a final acceptor for electron
Electron
The electron is a subatomic particle with a negative elementary electric charge. It has no known components or substructure; in other words, it is generally thought to be an elementary particle. An electron has a mass that is approximately 1/1836 that of the proton...
s. The greigite mineralising MTBs are usually strictly anaerobic.
It has been suggested MTB evolved in the early Proterozoic
Proterozoic
The Proterozoic is a geological eon representing a period before the first abundant complex life on Earth. The name Proterozoic comes from the Greek "earlier life"...
Era, as the increase in atmospheric oxygen reduced the quantity of dissolved iron in the oceans. Organisms began to store iron in some form, and this intracellular iron was later adapted to form magnetosomes for magnetotaxis. These early MTB may have participated in the formation of the first eukaryotic cells. Biogenic magnetite not too different from that found in magnetotactic bacteria has been also found in higher organisms, from Euglenoid algae
Algae
Algae are a large and diverse group of simple, typically autotrophic organisms, ranging from unicellular to multicellular forms, such as the giant kelps that grow to 65 meters in length. They are photosynthetic like plants, and "simple" because their tissues are not organized into the many...
, to salmon
Salmon
Salmon is the common name for several species of fish in the family Salmonidae. Several other fish in the same family are called trout; the difference is often said to be that salmon migrate and trout are resident, but this distinction does not strictly hold true...
, pigeons, and humans.
Magnetotactic bacteria produce their magnetic particles in chains. The magnetic dipole of the cell is therefore the sum of the dipoles of each BMP, which is then sufficient to passively orient the cell and overcome the casual thermal forces found in a water environment. In the presence of more than one chain, the inter-chain repulsive forces will push these structures to the edge of the cell, inducing turgor.
The diversity of MTB is reflected by the high number of different morphotypes found in environmental samples of water or sediment. Commonly observed morphotypes include spherical or ovoid cells (cocci
Coccus
Coccus can be used to describe any bacterium that has a spherical shape. It is one of the three distinct types of bacteria shapes, the other two being bacillus and spirillum cells...
), rod-shaped (bacilli
Bacilli
Bacilli refers to a taxonomic class of bacteria. It includes two orders, Bacillales and Lactobacillales, which contain several well-known pathogens like Bacillus anthracis .-Ambiguity:...
), curved bacteria (vibrio
Vibrio
Vibrio is a genus of Gram-negative bacteria possessing a curved rod shape, several species of which can cause foodborne infection, usually associated with eating undercooked seafood. Typically found in saltwater, Vibrio are facultative anaerobes that test positive for oxidase and do not form...
) and helical (spirillum
Spirillum
Spirillum in microbiology refers to a bacterium with a cell body that twists like a spiral. It is the third distinct bacterial cell shape type besides coccus and bacillus cells.-Taxonomic:...
) of various dimensions. One of the more distinctive morphotypes is an apparently multicellular bacterium referred to as the many-celled magnetotactic prokaryote (MMP). Regardless of their morphology, all MTB studied so far are motile by means of flagella are Gram-negative
Gram-negative
Gram-negative bacteria are bacteria that do not retain crystal violet dye in the Gram staining protocol. In a Gram stain test, a counterstain is added after the crystal violet, coloring all Gram-negative bacteria with a red or pink color...
bacteria of various phyla: Despite the majority of known species' being proteobacteria
Proteobacteria
The Proteobacteria are a major group of bacteria. They include a wide variety of pathogens, such as Escherichia, Salmonella, Vibrio, Helicobacter, and many other notable genera....
, e.g. Magnetospirillum magneticum an alphaproteobacterium, members of various phyla possess the magnetosome gene cluster, such as Candidatus Magnetobacterium bavaricum a Nitrospira. The arrangement of flagella differs and can be polar, bipolar, or in tufts. The first phylogenetic analysis on magnetotactic bacteria using 16SrRNA gene sequence comparisons was performed by P. Eden et al. in 1991.
Another trait that shows considerable diversity is the arrangement of magnetosomes inside the bacterial cell. In the majority of MTB, the magnetosomes are aligned in chains of various lengths and numbers along the cell's long axis, which is magnetically the most efficient orientation. However, dispersed aggregates or clusters of magnetosomes occur in some MTB, usually at one side of the cell, which often corresponds to the site of flagellar insertion. Besides magnetosomes, large inclusion bodies containing elemental sulfur
Sulfur
Sulfur or sulphur is the chemical element with atomic number 16. In the periodic table it is represented by the symbol S. It is an abundant, multivalent non-metal. Under normal conditions, sulfur atoms form cyclic octatomic molecules with chemical formula S8. Elemental sulfur is a bright yellow...
, polyphosphate
Polyphosphate
Triphosphates are salts or esters of polymeric oxyanions formed from tetrahedral PO4 structural units linked together by sharing oxygen atoms. When two corners are shared the polyphosphate may have a linear chain structure or a cyclic ring structure. In biology the polyphosphate esters AMP, ADP...
, or poly-β-hydroxybutyrate are common in MTB.
The most abundant type of MTB occurring in environmental samples, especially sediments, are coccoid cells possessing two flagellar bundles on a somewhat flattened side. This "bilophotrichous" type of flagellation gave rise to the tentative genus "Bilophococcus" for these bacteria. In contrast, two of the morphologically more conspicuous MTB, regularly observed in natural samples, but never isolated in pure culture, are the MMP and a large rod containing copious amounts of hook-shaped magnetosomes (Magnetobacterium bavaricum).
Magnetism
The physical development of a magnetic crystalCrystal
A crystal or crystalline solid is a solid material whose constituent atoms, molecules, or ions are arranged in an orderly repeating pattern extending in all three spatial dimensions. The scientific study of crystals and crystal formation is known as crystallography...
is governed by two factors: one is moving to align the magnetic force of the molecules in conjunction with the developing crystal, while the other reduces the magnetic force of the crystal, allowing an attachment of the molecule while experiencing an opposite magnetic force. In nature, this causes the existence of a magnetic domain, surrounding the perimeter of the domain, with a thickness of approximately 150 nm of magnetite, within which the molecules gradually change orientation. For this reason, the iron
Iron
Iron is a chemical element with the symbol Fe and atomic number 26. It is a metal in the first transition series. It is the most common element forming the planet Earth as a whole, forming much of Earth's outer and inner core. It is the fourth most common element in the Earth's crust...
is not magnetic in the absence of an applied field. Likewise, extremely small magnetic particles do not exhibit signs of magnetisation at room temperature; their magnetic force is continuously altered by the thermal motions inherent in their composition. Instead, individual magnetite crystals in MTB are of a size between 35 and 120 nm, that is, large enough to have a magnetic field and at the same time small enough to remain a single magnetic domain
Single domain (magnetic)
Single domain, in magnetism, refers to the state of a ferromagnet in which the magnetization does not vary across the magnet. A magnetic particle that stays in a single domain state for all magnetic fields is called a single domain particle . Such particles are very small...
.
Magnetosome
Magnetosome chains are membranous prokaryotic organelles present in magnetotactic bacteria. They contain 15 to 20 magnetite crystals that together act like a compass needle to orient magnetotactic bacteria in geomagnetic fields, thereby simplifying their search for their preferred microaerophilic...
s. Various experiments have clearly shown that magnetotaxis
Magnetotaxis
Logically, magnetotaxis describes an ability to sense a magnetic field and coordinate movement in response. It was applied to the behavior of certain motile, aquatic bacteria in 1975 by R. P. Blakemore....
and aerotaxis work in conjunction in the magnetotactic bacteria. Aerotaxis is the response by which bacteria migrate to an optimal oxygen concentration in an oxygen gradient. It has been shown that, in water droplets, one-way swimming magnetotactic bacteria can reverse their swimming direction and swim backwards under reducing conditions (less than optimal oxygen concentration), as opposed to oxic conditions (greater than optimal oxygen concentration). The behaviour that has been observed in these bacterial strains has been referred to as magneto-aerotaxis.
Two different magneto-aerotactic mechanisms — known as polar and axial — are found in different MTB strains. Some strains that swim persistently in one direction along the magnetic field (either north-seeking [NS] or south-seeking [SS]) — mainly the magnetotactic cocci — are polar magneto-aerotactic. These magnetotactic bacteria will travel along the lines of the earth’s magnetic field according to their orientation, but will swerve as a group and reverse direction if exposed to a local, more powerful and oppositely-oriented magnetic field. In this way, they continue to travel in the same magnetic direction , but relative instead to the local field. Those MTB that swim in either direction along magnetic field lines with frequent, spontaneous reversals of swimming direction without turning around — for example, freshwater spirilla — are axial magneto-aerotactic and the distinction between NS and SS does not apply to these bacteria. The magnetic field provides both an axis and a direction of motility for polar magneto-aerotactic bacteria, whereas it only provides an axis of motility for axial types of bacteria. In both cases, magnetotaxis increases the efficiency of aerotaxis in vertical concentration gradients by reducing a three-dimensional search to a single dimension.
Scientists have also proposed an extension of the described model of magneto-aerotaxis to a more complex redoxtaxis. In this case, the unidirectional movement of MTB in a drop of water would be only one aspect of a sophisticated redox-controlled response. One hint for the possible function of polar magnetotaxis could be that most of the representative microorganisms are characterised by possessing either large sulfur inclusions or magnetosomes consisting of iron-sulfides. Therefore, it may be speculated the metabolism of these bacteria, being either chemolithoautotrophic or mixotrophic, is strongly dependent on the uptake of reduced sulfur compounds, which occurs in many habitats only in deeper regions at or below the OATZ due to the rapid chemical oxidation of these reduced chemical species by oxygen or other oxidants in the upper layers.
Microorganisms belonging to the genus Thioploca
Thioploca
Thioploca is a genus of filamentous sulfur bacteria which occurs along of coast off the west of South America. A large vacuole occupies more than 80% of their cell volume and contains sulfide and nitrate which they use to make energy for their metabolism by oxidising sulfate with nitrate...
, for example, use nitrate, which is stored intracellularly, to oxidize sulfide, and have developed vertical sheaths in which bundles of motile filaments are located. It is assumed that Thioploca uses these sheaths to efficiently move in a vertical direction in the sediment, thereby accumulating sulfide in deeper layers and nitrate in upper layers. For some MTB, it might also be necessary to perform excursions to anoxic zones of their habitat to accumulate reduced sulfur compounds.
Magnetosomes
The biomineralisationBiomineralisation
Biomineralization is the process by which living organisms produce minerals, often to harden or stiffen existing tissues. Such tissues are called mineralized tissues. It is an extremely widespread phenomenon; all six taxonomic kingdoms contain members that are able to form minerals, and over 60...
of the magnetite requires regulating mechanisms to control the concentration of iron, the crystal nucleation
Nucleation
Nucleation is the extremely localized budding of a distinct thermodynamic phase. Some examples of phases that may form by way of nucleation in liquids are gaseous bubbles, crystals or glassy regions. Creation of liquid droplets in saturated vapor is also characterized by nucleation...
, the redox potential and the pH
PH
In chemistry, pH is a measure of the acidity or basicity of an aqueous solution. Pure water is said to be neutral, with a pH close to 7.0 at . Solutions with a pH less than 7 are said to be acidic and solutions with a pH greater than 7 are basic or alkaline...
. This is achieved by means of compartmentalisation in structures known as magnetosomes that allow the biochemical control of the above mentioned processes. After the genome
Genome
In modern molecular biology and genetics, the genome is the entirety of an organism's hereditary information. It is encoded either in DNA or, for many types of virus, in RNA. The genome includes both the genes and the non-coding sequences of the DNA/RNA....
of several MTB species had been sequenced, a comparative analysis of the protein
Protein
Proteins are biochemical compounds consisting of one or more polypeptides typically folded into a globular or fibrous form, facilitating a biological function. A polypeptide is a single linear polymer chain of amino acids bonded together by peptide bonds between the carboxyl and amino groups of...
s involved in the formation of the BMP became possible. Sequence homology with proteins belonging to the ubiquitous cation diffusion facilitator (CDF) family and the "Htr-like" serine protease
Serine protease
Serine proteases are enzymes that cleave peptide bonds in proteins, in which serine serves as the nucleophilic amino acid at the active site.They are found ubiquitously in both eukaryotes and prokaryotes...
s has been found: While the first group is exclusively dedicated to the transport of heavy metals, the second group consists of heat shock protein
Heat shock protein
Heat shock proteins are a class of functionally related proteins involved in the folding and unfolding of other proteins. Their expression is increased when cells are exposed to elevated temperatures or other stress. This increase in expression is transcriptionally regulated...
s (HSPs) involved in the degradation of badly folded
Protein folding
Protein folding is the process by which a protein structure assumes its functional shape or conformation. It is the physical process by which a polypeptide folds into its characteristic and functional three-dimensional structure from random coil....
proteins. Other than the serine protease domain, some proteins found in the magnetosomial membrane (MM) also contain PDZ domains, while several other MM proteins contain tetratrico peptide repeat (TPR) domains.
TPR domain
The TPR domains are characterized by a folding consisting of two α-helicesAlpha helix
A common motif in the secondary structure of proteins, the alpha helix is a right-handed coiled or spiral conformation, in which every backbone N-H group donates a hydrogen bond to the backbone C=O group of the amino acid four residues earlier...
and include a highly conserved consensus sequence
Consensus sequence
In molecular biology and bioinformatics, consensus sequence refers to the most common nucleotide or amino acid at a particular position after multiple sequences are aligned. A consensus sequence is a way of representing the results of a multiple sequence alignment, where related sequences are...
of 8 amino acid
Amino acid
Amino acids are molecules containing an amine group, a carboxylic acid group and a side-chain that varies between different amino acids. The key elements of an amino acid are carbon, hydrogen, oxygen, and nitrogen...
s (of the 34 possible), which is the most common in nature. Apart from these amino acids, the remainder of the structure is found to be specialised in relation to its functional significance. The more notable compounds that comprise TPR domains include:
- membrane-bound transport complexes conveying proteins within mitochondriaMitochondrionIn cell biology, a mitochondrion is a membrane-enclosed organelle found in most eukaryotic cells. These organelles range from 0.5 to 1.0 micrometers in diameter...
and/or peroxisomePeroxisomePeroxisomes are organelles found in virtually all eukaryotic cells. They are involved in the catabolism of very long chain fatty acids, branched chain fatty acids, D-amino acids, polyamines, and biosynthesis of plasmalogens, etherphospholipids critical for the normal function of mammalian brains...
s - complexes that recognise DNA-binding proteins and repress DNA transcriptionTranscription (genetics)Transcription is the process of creating a complementary RNA copy of a sequence of DNA. Both RNA and DNA are nucleic acids, which use base pairs of nucleotides as a complementary language that can be converted back and forth from DNA to RNA by the action of the correct enzymes...
- the anaphase-promoting complexAnaphase-promoting complexAnaphase-Promoting Complex, also called cyclosome , is an E3 ubiquitin ligase that marks target cell cycle proteins for degradation by the 26S proteasome. The APC/C is a large complex of 11–13 subunit proteins, including a cullin and RING subunit much like SCF...
(APC).
Examples of both the TPR-TPR interactions, as well as TPR-nonTPR interactions, have been reported.
PDZ domain
The PDZ domains are structures that consist of 6 β-filaments and 2 α-helices that recognise the C terminal aminoacids of proteins in a sequence-specific manner. Usually, the third residue from the C terminal is phosphorylatedPhosphorylation
Phosphorylation is the addition of a phosphate group to a protein or other organic molecule. Phosphorylation activates or deactivates many protein enzymes....
, thus preventing interaction with the PDZ domain. The only conserved residues in these structures are those involved in the recognition of the carboxy terminal. PDZ domains are quite widespread in nature, since they constitute the basic structure upon which multiproteinic complexes are assembled: This is especially true for those associated with membrane proteins, such as the inward rectifier K+ channels
Ion channel
Ion channels are pore-forming proteins that help establish and control the small voltage gradient across the plasma membrane of cells by allowing the flow of ions down their electrochemical gradient. They are present in the membranes that surround all biological cells...
or the β2-adrenergic
Adrenergic
An adrenergic agent is a drug, or other substance, which has effects similar to, or the same as, epinephrine . Thus, it is a kind of sympathomimetic agent...
receptors.
Membrane and proteins
The formation of the magnetosome requires at least three steps.- 1. The invagination of the magnetosome membrane (MM)
- 2. The entrance of magnetite precursors into the newly formed vesicle
- 3. The nucleation and growth of the magnetite crystal.
During the first formation of an invagination
Invagination
Invagination means to fold inward or to sheath. In biology, this can refer to a number of processes.* Invagination is the morphogenetic processes by which an embryo takes form, and is the initial step of gastrulation, the massive reorganization of the embryo from a simple spherical ball of cells,...
in the cytoplasmic membrane is triggered by a GTPase
GTPase
GTPases are a large family of hydrolase enzymes that can bind and hydrolyze guanosine triphosphate . The GTP binding and hydrolysis takes place in the highly conserved G domain common to all GTPases.-Functions:...
. It is supposed this process can take place amongst eukaryote
Eukaryote
A eukaryote is an organism whose cells contain complex structures enclosed within membranes. Eukaryotes may more formally be referred to as the taxon Eukarya or Eukaryota. The defining membrane-bound structure that sets eukaryotic cells apart from prokaryotic cells is the nucleus, or nuclear...
s, as well.
The second step requires the entrance of ferric ion
Ion
An ion is an atom or molecule in which the total number of electrons is not equal to the total number of protons, giving it a net positive or negative electrical charge. The name was given by physicist Michael Faraday for the substances that allow a current to pass between electrodes in a...
s into the newly formed vesicle
Vesicle (biology)
A vesicle is a bubble of liquid within another liquid, a supramolecular assembly made up of many different molecules. More technically, a vesicle is a small membrane-enclosed sack that can store or transport substances. Vesicles can form naturally because of the properties of lipid membranes , or...
s from the external environment. Even when cultured in a Fe3+ deficient medium, MTB succeed at accumulating high intracellular concentrations of this ion. It has been suggested that they accomplish this by secreting, upon need, a siderophore
Siderophore
Siderophores are small, high-affinity iron chelating compounds secreted by grasses and microorganisms such as bacteria and fungi...
, a low-molecular-weight ligand displaying an elevated affinity for Fe3+ ions. The "Fe3+-siderophore" complex is subsequently moved in the cytoplasm
Cytoplasm
The cytoplasm is a small gel-like substance residing between the cell membrane holding all the cell's internal sub-structures , except for the nucleus. All the contents of the cells of prokaryote organisms are contained within the cytoplasm...
, where it is cleaved. The ferric ions must then be converted into the ferrous form (Fe2+), to be accumulated within the BMP; this is achieved by means of a transmembrane transporter, which exhibits sequence homology with a Na+/H+ antiporter
Antiporter
An antiporter is an integral membrane protein involved in secondary active transport of two or more different molecules or ions across a phospholipid membrane such as the plasma membrane in opposite directions.In secondary active transport, one species of solute moves along its electrochemical...
. Furthermore, the complex is a H+/Fe2+ antiporter, which transports ions via the proton gradient. These transmembrane transporters are localised both in the cytoplasmic membrane and in the MM, but with in an inverted orientation; this configuration allows them to generate an efflux of Fe2+ ions at the cytoplasmic membrane, and an influx of this same ion at the MM. This step is strictly controlled by a cytochrome
Cytochrome
Cytochromes are, in general, membrane-bound hemoproteins that contain heme groups and carry out electron transport.They are found either as monomeric proteins or as subunits of bigger enzymatic complexes that catalyze redox reactions....
-dependent redox system, which is not yet fully explained and appears to be species-specific.
During the final stage of the process, the magnetite crystal nucleation is by action of transmembrane proteins with acidic and basic domains. One of these proteins, called Mms6, has also been employed for the artificial synthesis of magnetite, where its presence allows the production of crystals homogeneous in shape and size.
It is likely that many other proteins associated with the MM could be involved in other roles, such as generation of supersaturated concentrations of iron, maintenance of reducing conditions, oxidisation of iron, and partial reduction and dehydration of hydrated iron compounds.
Biomineralisation
Several clues led to the hypothesis that different genetic sets exist for the biomineralisation of magnetite and greigite. In cultures of Magnetospirillum magnetotacticum, iron can not be replaced with other transition metals (Ti, Cr, Co, Cu, Ni, Hg, Pb) commonly found in the soil. In a similar manner, oxygenOxygen
Oxygen is the element with atomic number 8 and represented by the symbol O. Its name derives from the Greek roots ὀξύς and -γενής , because at the time of naming, it was mistakenly thought that all acids required oxygen in their composition...
and sulfur are not interchangeable as nonmetallic substances of the magnetosome within the same species.
From a thermodynamic
Thermodynamics
Thermodynamics is a physical science that studies the effects on material bodies, and on radiation in regions of space, of transfer of heat and of work done on or by the bodies or radiation...
point of view, in the presence of a neutral pH and a low redox potential, the inorganic synthesis of magnetite is favoured when compared to those of other iron oxide
Iron oxide
Iron oxides are chemical compounds composed of iron and oxygen. All together, there are sixteen known iron oxides and oxyhydroxides.Iron oxides and oxide-hydroxides are widespread in nature, play an important role in many geological and biological processes, and are widely utilized by humans, e.g.,...
s. It would thus appear microaerophilic
Microaerophile
A microaerophile is a microorganism that requires oxygen to survive, but requires environments containing lower levels of oxygen than are present in the atmosphere . Many microphiles are also capnophiles, as they require an elevated concentration of carbon dioxide. In the laboratory they can be...
or anaerobic
Hypoxia (environmental)
Hypoxia, or oxygen depletion, is a phenomenon that occurs in aquatic environments as dissolved oxygen becomes reduced in concentration to a point where it becomes detrimental to aquatic organisms living in the system...
conditions create a suitable potential for the formation of BMPs. Moreover, all iron absorbed by the bacteria is rapidly converted into magnetite, indicating the formation of crystals is not preceded by the accumulation of intermediate iron compounds; this also suggests the structures and the enzyme
Enzyme
Enzymes are proteins that catalyze chemical reactions. In enzymatic reactions, the molecules at the beginning of the process, called substrates, are converted into different molecules, called products. Almost all chemical reactions in a biological cell need enzymes in order to occur at rates...
s necessary for biomineralisation are already present within the bacteria. These conclusions are also supported by the fact that MTB cultured in aerobic conditions (and thus nonmagnetic) contain amounts of iron comparable to any other species of bacteria.
Biotechnology applications
In certain types of applications, bacterial magnetite offers several advantages compared to chemically synthesized magnetite. Bacterial magnetosome particles, unlike those produced chemically, have a consistent shape, a narrow size distribution within the single magnetic domain range, and a membrane coating consisting of lipids and proteinProtein
Proteins are biochemical compounds consisting of one or more polypeptides typically folded into a globular or fibrous form, facilitating a biological function. A polypeptide is a single linear polymer chain of amino acids bonded together by peptide bonds between the carboxyl and amino groups of...
s. The magnetosome envelope allows for easy couplings of bioactive substances to its surface, a characteristic important for many applications.
Magnetotactic bacterial cells have been used to determine south magnetic poles in meteorites and rocks containing fine-grained magnetic minerals and for the separation of cells after the introduction of magnetotactic bacterial cells into granulocyte
Granulocyte
Granulocytes are a category of white blood cells characterized by the presence of granules in their cytoplasm. They are also called polymorphonuclear leukocytes because of the varying shapes of the nucleus, which is usually lobed into three segments...
s and monocyte
Monocyte
Monocytes are a type of white blood cell and are part of the innate immune system of vertebrates including all mammals , birds, reptiles, and fish. Monocytes play multiple roles in immune function...
s by phagocytosis. Magnetotactic bacterial magnetite crystals have been used in studies of magnetic domain analysis and in many commercial applications including: the immobilisation of enzymes; the formation of magnetic antibodies, and the quantification of IgG; the detection and removal of Escherichia coli
Escherichia coli
Escherichia coli is a Gram-negative, rod-shaped bacterium that is commonly found in the lower intestine of warm-blooded organisms . Most E. coli strains are harmless, but some serotypes can cause serious food poisoning in humans, and are occasionally responsible for product recalls...
cells with a fluorescein isothiocyanate
Isothiocyanate
Isothiocyanate is the chemical group –N=C=S, formed by substituting sulfur for oxygen in the isocyanate group. Many natural isothiocyanates from plants are produced by enzymatic conversion of metabolites called glucosinolates. These natural isothiocyanates, such as allyl isothiocyanate, are also...
conjugated monoclonal antibody, immobilised on magnetotactic bacterial magnetite particles; and the introduction of genes into cells, a technology in which magnetosomes are coated with DNA and "shot" using a particle gun into cells that are difficult to transform using more standard methods.
However, the prerequisite for any large-scale commercial application is mass cultivation of magnetotactic bacteria or the introduction and expression of the genes responsible for magnetosome synthesis into a bacterium, e.g., E. coli, that can be grown relatively cheaply to extremely large yields. Although some progress has been made, the former has not been achieved with the available pure cultures.
External links
- http://www.gps.caltech.edu/~jkirschvink/magnetofossil.html
- http://www.calpoly.edu/~rfrankel/mtbcalpoly.html
- http://www.agu.org/revgeophys/moskow01/moskow01.html
- Comparative Genome Analysis of Four Magnetotactic Bacteria Reveals a Complex Set of Group-Specific Genes Implicated in Magnetosome Biomineralization and Function Journal of Bacteriology, July 2007