magnetism and biology: the magnetotactic bacteria...

Gravitational and Space Biology Bulletin 17(2) June 2004 115

MAGNETISM AND BIOLOGY: THE MAGNETOTACTIC BACTERIA D.A. Bazylinski Department of Microbiology, Iowa State University, Ames, IA ABSTRACT Although the Earth’s geomagnetic field appears to influence the behavior and migration of a wide range of organisms, the most understood example of magnetoreception and magnetonavigation is that observed in the magnetotactic bacteria. Cells of this ubiquitous and diverse group of Gram-negative, motile, mainly aquatic microbes synthesize unique intracellular structures called magnetosomes which are membrane-bounded, single-magnetic-domain crystals of the magnetic minerals magnetite (Fe3O4) or greigite (Fe3S4). These crystals impart a permanent magnetic dipole moment to the cell causing it to align along magnetic field lines like a compass needle. This passive alignment of the cell while it actively swims is known as magnetotaxis. In many magnetotactic bacteria, magnetotaxis, in conjunction with aerotaxis, appears to function as a means for cells to locate and maintain an optimal position (the oxic-anoxic interface) in vertical oxygen gradients by reducing a 3-dimensional search problem to a 1-dimensional search problem. Although little is known about how the magnetosomes are formed, the narrow size (~35-120 nm) distributions, species-specific morphologies, and pure chemical compositions of the magnetosome crystals together with the fact that cells organize their magnetosomes in chains in which the cellular magnetic dipole moment is maximized, indicate that magnetotactic bacteria utilize a biologically-controlled mineralization process in synthesizing magnetosomes. Certain elongated Fe3O4 particle morphologies appear to be unique to the magnetotactic bacteria and have not been observed in abiotically-synthesized Fe3O4 particles. Hence, magnetosome crystals released by dead cells in their surrounding environment, have been used as evidence for the past presence of magnetotactic bacteria. Such crystals have been found in Martian meteorite ALH84001 where their presence has been used as evidence for life on ancient Mars. INTRODUCTION The chance discovery of the magnetotactic bacteria occurred recently about 30 years ago. Richard P. Blakemore, then a graduate student at the University of Massachusetts, microscopically noted large numbers of fast swimming, coccoid bacteria migrating persistently in one direction until a small bar magnet was brought in close proximity to the microscope (Blakemore, 1975, 1982). Blakemore, using magnetic manipulation and electron microscopy, found the magnetic behavior of the cells was due to the presence of unique, intracellular, electron - dense, magnetic mineral structures called magnetosomes (Balkwill et al., 1980). Although almost 3 decades have elapsed since their discovery, relatively few species of magnetotactic bacteria have been isolated and grown

in axenic culture. Because of this and the fastidiousness and difficulty of working with the existing strains available in pure culture, little is known about how these fascinating microorganisms biomineralize magnetosomes at the biochemical, chemical, and molecular levels. Despite this lack of understanding, the magnetotactic bacteria appear to be an environmentally important group of procaryotes based on their ubiquity and their presence in relatively high numbers in natural habitats and based on the geochemical transformations they catalyze (Bazylinski and Moskowitz, 1997; Bazylinski and Frankel, 2000). THE MAGNETOTACTIC BACTERIA: GENERAL FEATURES The magnetotactic bacteria represent a heterogeneous group of Gram-negative, mostly aquatic, motile procaryotes. Magnetotactic cocci, rods, vibrios, spirilla, and multicellular forms have been described. Those in pure culture display significant metabolic variation (Bazylinski and Frankel, 2000). Thus, the term “magnetotactic bacteria” lacks taxonomic significance and the group should be regarded as morphologically and metabolically diverse but share the trait of magnetotaxis. Despite this diversity, the magnetotactic bacteria share several important traits (Bazylinski and Frankel, 2000): (1) phylogenetically, all are Gram-negative members of the Domain Bacteria (magnetotactic Archaea may exist but none have been found to date); (2) all are motile by means of flagella (magnetotactic gliding bacteria or non-motile bacteria that produce magnetosomes might exist but would likely be overlooked during selection); (3) all demonstrate negative tactic and/or growth responses towards atmospheric levels of O2 and are microaerophiles or anaerobes or both; and (4) all possess a number of magnetosomes. A typical magnetotactic bacterium is shown in Figure 1.

Figure 1. Transmission electron micrograph of a negatively-stained magnetotactic bacterium. This cell is of a strain of a marine, magnetotactic spirillum (helically-shaped bacterium). The dark, electron-dense rectangular structures within the cell are the magnetosomes which, in this case, are arranged in a chain and consist of Fe3O4. The thread-like structures at each end of the cell are the flagella which the cell uses to swim.

____________________

* Correspondence to: D.A. Bazylinski Department of Microbiology, Iowa State University Ames, IA 50011 USA Email: [email protected] Phone: 515-294-2561; FAX: 515-294-6019

D.A. Bazylinski – Magnetism and Biology: The Magnetotactic Bacteria

116 Gravitational and Space Biology Bulletin 17(2) June 2004

Magnetotactic bacteria are cosmopolitan in distribution and ubiquitous in most aquatic habitats (Bazylinski, 1995). They are generally absent from well aerated or highly acidic waters. On a local basis, the highest numbers of magnetotactic bacteria are found at or just below the oxic-anoxic interface or transition zone (OATZ). In many freshwater systems, the OATZ occurs roughly at the sediment-water interface. In some brackish-to marine systems, the OATZ can be located permanently or seasonally in the water column due to the upward diffusion of hydrogen sulfide (H2S) resulting from the action of anaerobic sulfate-reducing bacteria (seawater contains approximately 28 mM sulfate) (Bazylinski et al., 1995, 2000). Thus these chemically-stratified systems are typified by reverse double gradients of O2 diffusing downward from the surface and H2S diffusing upward from the sediments as shown in Figure 2. The OATZ can occur at very small scales on the order or mm or µm in shallow salt marsh pools or at very large scales on the order of meters such as in the Black Sea, the largest anaerobic basin on Earth.

Figure 2. Depiction of the oxic-anoxic transition zone (OATZ) in the water column of a chemically-stratified semi-anaerobic basin containing inverse concentration gradients of O2 diffusing from the surface and H2S diffusing from the anaerobic zone and sediments. Magnetite-producing magnetotactic bacteria are generally found at the OATZ proper whereas Fe3S4-producers appear to prefer the anaerobic just below the OATZ where H2S is present. Axial magnetotactic species (e.g., spirilla) align along the geomagnetic field lines (dashed lines) and swim bidirectionally upward and downward relying on a temporal sensory mechanism of aerotaxis to find and maintain position at the OATZ. Polarly magnetotactic species (e.g., cocci) also align along the geomagnetic field lines and appear to use a two-state aerotactic sensory mechanism to also locate and maintain position at the OATZ. When cocci are in the oxic zone, the [O2] is suboptimal (too high), and cells swim downward (small arrows above OATZ). When they venture into the anoxic zone, the [O2] is also suboptimal (too low), and cells “switch” to an alternate state where they reverse the direction of their flagella motors and swim upward (small arrows below OATZ) without turning around. Based on laboratory experiments, the magnetotactic bacteria show great potential for being important agents in the biochemical cycling of several important elements in natural habitats. While there is little doubt they play a significant role in iron cycling, they also are important in the biogeochemical cycling of: sulfur, either as sulfide-oxidizing lithotrophs, sulfate-reducing organisms, and/or

greigite (Fe3S4) producers (see next section); nitrogen, either as denitrifyers or nitrogen-fixers or both; and carbon, as autotrophs (primary producers) based on chemosynthesis (chemolithoautotrophy) rather than photosynthesis (Bazylinski and Frankel, 2000). THE BACTERIAL MAGNETOSOME Magnetosomes are defined as intracellular, membrane-bound, single-magnetic-domain crystals of a magnetic mineral (Balkwill et al., 1980), either the iron oxide magnetite, Fe3O4 (Frankel et al., 1979), or the iron sulfide greigite, Fe3S4 (Mann et al., 1990). Most magnetotactic bacteria only produce one mineral type although one uncultured magnetotactic bacterium was found to contain both minerals (Bazylinski et al., 1993). The chemical purity of Fe3O4 produced by the magnetotactic bacteria is very high (Thomas-Keprta et al., 2000, 2001). Despite the fact that cultured magnetotactic bacteria are routinely grown with a variety of metals as trace growth requirements, only iron is incorporated into the magnetosome. In only one report (Towe and Moench, 1981), were impurities, as trace amounts of titanium, found in Fe3O4 particles of a magnetotactic bacterium, in this case an uncultured freshwater magnetotactic coccus. Thus, the absence of transition metal ions other than iron is one of the hallmarks of Fe3O4 magnetosome crystals. Although all freshwater magnetotactic bacteria have been found to biomineralize Fe3O4 magnetosomes, many marine, estuarine, and salt marsh species produce magnetosomes with iron sulfide mineral crystals (Bazylinski and Moskowitz, 1997; Bazylinski and Frankel, 2000). These include an unusual multicellular bacterium referred to as MMP and a variety of relatively large rod-shaped bacteria (Pósfai et al., 1998a, 1998b). The iron sulfide minerals are either Fe3S4 or a mixture of Fe3S4 and transient non-magnetic iron sulfide phases that likely represent mineral precursors to Fe3S4 (Pósfai et al., 1998a, 1998b). These include non-magnetic mackinawite (tetragonal FeS) and possibly a sphalerite-type cubic FeS (Pósfai et al., 1998a, 1998b). Based on transmission electron microscopic observations, electron diffraction, and known iron sulfide chemistry (Berner, 1964, 1967), the reaction scheme for Fe3S4 formation in the magnetotactic bacteria appears to be: cubic FeS → mackinawite (tetragonal FeS) → greigite (Fe3S4) (Pósfai et al., 1998a, 1998b). Reports of iron pyrite (FeS2) (Mann et al., 1990) and pyrrhotite (Fe7S8) (Farina et al., 1990) in magnetotactic bacteria have not been confirmed and may reflect errors in electron diffraction determinations. No iron sulfide producing magnetotactic bacteria have been isolated and grown in axenic culture to date. But high mineral purity does not appear to be a feature of Fe3S4 crystals in magnetotactic bacteria. Significant amounts of copper but not other transition metal ions were found in Fe3S4 magnetosomes of some magnetotactic bacteria including the MMP (Bazylinski et al., 1993a). The amount of copper was dependent upon collection site and was variable from magnetosome to



magnetosome within an individual cell, ranging in one case from about 0.1 to 10 atomic % relative to iron. This suggests that copper incorporation is a consequence of environmental conditions. Copper appeared in some cases to be mostly concentrated on the surface of the crystals. These observations indicate that mineralization in these organisms is more susceptible to chemical conditions in the external environment, and suggest that the iron sulfide magnetosomes could function in transition metal detoxification (Bazylinski et al., 1993a). The morphology of the mineral crystals in magnetosomes varies but is generally consistent within cells of a single bacterial strain or species (Bazylinski et al., 1994, 1997). Three general crystal morphologies have been found in Fe3O4 and Fe3S4 magnetosomes and include: (1) roughly cuboidal; (2) parallelepipedal (rectangular in projection); and (3) tooth-, bullet-, or arrowhead-shaped (Bazylinski et al., 1994, 1997). Examples of these particular morphologies are shown in Figure 3.

Figure 3. Scanning transmission electron micrographs of different crystal morphologies of Fe3O4 particles in magnetotactic bacteria. (a) cubo-octahedra in Magnetospirillum magnetotacticum; (b-c) parallelepipeds within cells of strain MV-1 and MC-1, respectively; (d) parallelepipeds within cells of an unidentified, uncultured coccus that show a constriction (at arrows) in the middle of some of the crystals; (e-f) variations of bullet- and tooth-shaped Fe3O4 crystals in unidentified, uncultured magnetotactic bacteria. Magnetite and Fe3S4 are in the Fd3m space group. Macroscopic crystals of Fe3O4 display habits of the octahedral (111) form, more rarely dodecahedral (110), or cubic (100) forms (Palache et al., 1944). The habit of the isometric roughly cuboidal Fe3O4 crystals in all the freshwater magnetospirilla, e.g., Magnetospirillum

magnetotacticum, are cubooctahedra, composed of (100) + (111) forms (Mann et al., 1984), with isometric development of the six symmetry related faces of the (100) form and of the eight symmetry related faces of the (111) form as shown in Figure 4a. The cubo-octahedron is the equilibrium form of Fe3O4 and is commonly observed in synthetic chemically-produced Fe3O4.

Figure 4. Idealized Fe3O4 (a-d) and Fe3S4 (e-f) crystal morphologies from high resolution electron microscope studies of magnetosomes in magnetotactic bacteria. Fe3O4 morphologies in magnetotactic bacteria: (a) cubo-octahedron as from Magnetospirillum magnetotacticum; (b-c) variations of hexagonal prisms (parallelepipeds in projection) as from cells of strains MV-1 and MC-1, respectively; (d) elongated cubo-octahedron (parallelepipeds in projection) from an unidentified coccus. Fe3S4 morphologies observed in magnetotactic bacteria: (e) cubo-octahedron; (b) elongated rectangular prism (parallelepipeds in projection). The habits of the unusual non-isometric parallelepipedal crystals in other strains (Figures 4b-4d), e.g., the marine vibrios MV-1 and MV-2 and the coccus MC-1, can be described as combinations of (100), (111) and (110) forms (Devouard et al., 1998). In these cases, the six, eight and twelve symmetry related faces of the respective forms that constitute the habits do not develop equally. For example, crystals of strains MV-1, MV-2 (Figure 4b) (Sparks et al., 1990; Meldrum et al., 1993b) and MC-1 (Figure 4c) (Meldrum et al., 1993a) have pseudo hexagonal habits elongated along a (111) axis, with six well developed (110) faces parallel to the elongation axis, and capped by (111) planes perpendicular to the elongation axis. In MV-1 and MV-2 crystals, the remaining six (111) faces form truncations of the end



caps, and the remaining six (110) faces are missing (Meldrum et al., 1993b). In MC-1 crystals, the truncations at each end consist of three (100) faces alternating with three (110) faces. Thus, six (110) faces are larger and six are smaller, and six (111) faces are absent in this habit. Only the six (100) faces are isometric (Meldrum et al., 1993a). The motif of six elongated (110) faces capped by (111) faces with differing truncation planes appears to be most common in magnetotactic bacteria with non-isometric magnetosome crystals. The elongated, parallelepipedal, prismatic habits, corresponding to the anisotropic development of symmetry related faces, are exotic enough to be used as biomarkers for the past presence of magnetotactic bacteria (see later sections) and could occur either because of anisotropy in the growth environment (such as, for example, concentration and/or temperature gradients) or anisotropy of the growth sites (Mann and Frankel, 1989). In the case of the non-isometric magnetosomes, the anisotropy of the environment could derive from an anisotropic flux of ions through the magnetosome membrane surrounding the crystal (Gorby et al., 1988), or from anisotropic interactions of the magnetosome membrane with the growing crystal (Mann and Frankel, 1989). Although Fe3O4 crystals produced by magnetotactic bacteria are considered to be of relatively high structural perfection, some defects occur. Twinned crystals are common in magnetotactic bacterially-produced Fe3O4 (ca. 10%) with individuals related by rotations of 180 degrees around the (111) direction parallel to the chain direction and with a common (111) contact plane. Multiple twins are less common (Devouard et al., 1998). As with Fe3O4, several Fe3S4 crystal morphologies, composed primarily of (111) and (100) forms, have been observed (Heywood et al., 1991). These include cubooctahedral and pseudo rectangular prismatic, as shown in Figures 4e-f, and tooth-shaped (Heywood et al., 1991; Pósfai et al., 1998a, 1998b). Like that of their Fe3O4 counterparts, the morphologies of the Fe3S4 particles in the rod-shaped bacteria appear to be species- and/or strain-specific. Magnetite and Fe3S4 crystals in magnetotactic bacteria fall into a very narrow size range, about 35 to 120 nm (Bazylinski et al., 1994), which has physical significance. In this size range, the crystals are uniformly magnetized, permanent single-magnetic-domains. Smaller particles, called superparamagnetic, would be of no use to the cell since they are not permanently magnetic at ambient temperature. Domain walls would form in larger particles, forming a multi-domain crystal, thereby reducing the magnetic remanence of the crystal. The cell has maximized the magnetic remanence of the individual crystals by synthesizing single-magnetic-domains (Bazylinski and Moskowitz, 1997). Statistical analyses of Fe3O4 crystal size distributions in cultured strains show narrow, asymmetric distributions and consistent width to length ratios within each strain (Devouard et al., 1998). The shapes of the magnetosome crystal size distributions are asymmetric with a sharp high

end cutoff, consistent with a transport-controlled Ostwald ripening process (Eberl et al., 1998). BIOMINERALIZATION As stated above, magnetotactic bacteria synthesize well-ordered crystals with narrow size distributions with asymmetric shapes and species- and/or strain-specific morphologies. These characteristics indicate that the organisms regulate the biomineralization process(es) involved in magnetosome synthesis to a high degree, exerting great crystallochemical control over the nucleation and growth of the crystals. This type of mineralization is referred to as biologically-controlled mineralization (BCM; Bazylinski and Frankel, 2000). Magnetite and Fe3S4 can also be formed by an indirect mineralization process mediated by organisms called biologically-induced mineralization (BIM; Lowenstam, 1981). In BIM, mineralization is not controlled by the organism and occurs indirectly as a result of metabolic activities of the organism. In the case of Fe3O4 and Fe3S4 mineralization, organisms secrete and/or produce metabolic products that react with specific ions or compounds in the local environment resulting in the production of extracellular mineral particles that are an unintended byproduct of metabolic activities. Unlike those produced by BCM, Fe3O4 and Fe3S4 particles formed by BIM are extracellular, poorly crystallized, have a broad size distribution and no defined morphology as shown in Figure 5. The lack of control over biomineralization in BIM can also result in decreased mineral specificity and/or the inclusion of impurities in the particles. Mineral particles produced by BIM share similar crystallochemical features as particles synthesized abiotically and are generally indistinguishable from those particles produced inorganically under similar conditions. Dissimilatory iron-reducing bacteria form Fe3O4 via BIM. They respire with Fe(III) as amorphous Fe(III) oxyhydroxide under anaerobic conditions and Fe(II) produced by the cells reacts with the excess Fe(III) oxyhydroxide in the environment forming Fe3O4 (Lovley, 1990). Magnetite particles formed by iron-reducing bacteria are: (1) extracellular; (2) irregularly shaped with a broad size distribution that is log-normal; and (3) poorly crystallized (Figure 5: Sparks et al., 1990). Some sulfate-reducing bacteria produce Fe3S4 through BIM. In this situation, sulfate-reducing bacteria respire with sulfate anaerobically producing hydrogen sulfide, the sulfide ions reacting with the excess iron in the growth medium forming particles of a variety of iron sulfides including Fe3S4 (Bazylinski and Moskowitz, 1997). Greigite particles produced by sulfate-reducing bacteria have not been examined in any detail but are thought to have characteristics similar to the Fe3O4 particles produced through BIM. In both BCM and BIM, mineral formation is dependent upon the conditions external to the cell, e.g., pH, Eh, etc., as it would be in abiotic reactions. The ability to distinguish between BCM and BIM as well as abiotically produced Fe3O4 and Fe3S4 particles has great environmental and paleobiological significance and will be discussed later.



Figure 5. Particles of Fe3O4 produced in the growth medium of the iron-reducing bacterium, Geobacter metallireducens, through biologically-induced mineralization (BIM) rather than through biologically-controlled mineralization as in the magnetotactic bacteria. These particles are not well-ordered (amorphous or poorly crystallized), are mostly in the superparamagnetic size range, and are produced external to the cell. Arrows denote particles in which some crystal lattice lines can be seen. THE FUNCTION OF MAGNETOTAXIS In most magnetotactic bacteria, the magnetosomes are arranged in one or more chains in which the magnetic interactions of the particles cause their magnetic dipole moments to orient parallel to each other along the chain length. In this chain motif, the magnetic dipole moment of the cell is the sum of the dipole moments of the individual magnetosome crystals and the chain acts like a single magnetic dipole (Bazylinski and Moskowitz, 1997). The cell has thereby maximized its magnetic dipole moment which is generally large enough so that its interaction with the Earth’s geomagnetic field overcomes the thermal (Brownian) forces tending to randomize the cell’s orientation in water (Frankel and Blakemore, 1980). Magnetotaxis is the result of the passive alignment of the cell along geomagnetic field lines as it swims. Thus, cells, live or dead, behave as miniature compass needles and are neither attracted nor repelled from either geomagnetic pole although dead cells cannot be magnetotactic, i.e., they cannot swim. The observation of the conspicuous persistent swimming of the bilophotrichous (having two bundles of flagella on one side of the cell) magnetotactic cocci in wet mounts towards geomagnetic north (in the northern hemisphere) led to the discovery of the magnetotactic bacteria. These cells show a polar “preference” and generally greater than 99.9% of these type of cells from pure cultures or natural habitats will swim in one direction. Cells of the magnetotactic spirilla that have a single polar flagellum at each end of the cell, show no polar preference and equal numbers of these cells swim in either direction in wet mounts (Frankel et al., 1997). Although the Earth’s geomagnetic field strength is relatively consistent over the planet at about 0.5 gauss, the overall directionality of the geomagnetic field lines

differs, depending upon the location on Earth. The vertical component of the geomagnetic field is responsible for this and causes the geomagnetic field lines to be inclined in both hemispheres. The vertical component at the Equator is zero and thus the geomagnetic field lines here are not inclined; the lines become inclined as one moves away from the equator in either direction and the deviation from the horizontal becomes larger as the distance from the Equator increases until the field lines become completely vertical at the geomagnetic poles. According to Blakemore (1975, 1982), the inclined geomagnetic field lines select for a polarity in the cocci in each hemisphere favoring those cells whose polarity leads them downward away from toxic concentrations of O2 in surface waters. In natural environments, north- (and downward-) seeking magnetic cocci predominate in the northern hemisphere while south-seeking cocci predominate in the southern hemisphere (Blakemore et al., 1980). At the equator, where no polarity is favored, equal numbers of both polarities exist (Frankel et al., 1981). Like most other free-swimming bacteria, magnetotactic bacteria propel themselves forward in their aqueous environment by rotating their helical flagella (Silverman and Simon, 1974). However, magnetotactic bacteria do not exhibit the typical “run and tumble” motility of Escherichia coli and other chemotactic bacteria and generally swim bidirectionally (they do not change direction by tumbling). Because of their magnetosomes, magnetotactic bacteria are oriented and migrate along the local magnetic field B. The magnetotactic spirilla, e.g., Magnetospirillum magnetotacticum, swim parallel or antiparallel to B and form aerotactic bands (Bazylinski and Frankel, 2000) at a preferred oxygen concentration [O2]. In a homogeneous medium, roughly equal numbers of cells swim in either direction along B (Bazylinski and Frankel, 2000). Most microaerophilic bacteria form aerotactic bands at a preferred or optimal [O2] where the proton motive force is maximal (Zhulin et al., 1996), using a temporal sensory mechanism (Segall et al., 1986) that samples the local environment as they swim and compares the present [O2] with that in the recent past (Taylor, 1983). The change in [O2] with time determines the sense of flagellar rotation (Manson, 1992). The behavior of individual cells of M. magnetotacticum in microaerophilic bands is consistent with the temporal sensory mechanism (Frankel et al., 1997). Cells in the band which are moving away from the optimal [O2], to either higher or lower [O2], eventually reverse their swimming direction and return to the band. In contrast, the bilophotrichously-flagellated, magnetotactic cocci swim persistently in a preferred direction relative to B when examined microscopically in wet mounts (Frankel et al., 1997). However, the cocci in oxygen gradients, like cells of Magnetospirillum magnetotacticum, swim in both directions along B without turning around (Frankel et al., 1997). The cocci also form microaerophilic, aerotactic bands, like cells of M. magnetotacticum, and seek a preferred [O2] along the concentration gradient (Frankel et al., 1997). However, while the aerotactic behavior of M. magnetotacticum is



consistent with the temporal sensory mechanism, the aerotactic behavior of the cocci is not. Instead their behavior is consistent with a two-state aerotactic sensory model in which the [O2] determines the sense of the flagellar rotation and hence the swimming direction relative to B. Cells at [O2] higher than optimum swim persistently in one direction relative to B until they reach a low [O2] threshold at which they reverse flagellar rotation and hence swimming direction relative to B. They continue until they reach a high [O2] threshold at which they reverse again. In wet mounts, the [O2] is above optimal, and the cells swim persistently in one direction relative to B. This model accounts for the ability of the magnetotactic cocci to migrate to and maintain position at the preferred [O2] at the OATZ in natural environments and culture tubes. Based on the information above, two types of magneto-aerotaxis mechanisms, referred to as polar and axial magnetotaxis, used by the magnetotactic cocci and spirilla, respectively, have been described (Frankel et al, 1997). For the spirilla, the geomagnetic field provides an axis and not a direction for motility while the geomagnetic field provides both for motility of the cocci. The passive orientation of the cellular magnetic dipole in the geomagnetic field is necessary and involved in both mechanisms and both cell types use aerotaxis in conjunction with magnetotaxis to find and maintain an optimal position in vertical oxygen gradients. Magnetotaxis is especially advantageous to microorganisms in vertical concentration gradients because it increases the efficiency of locating and maintaining an optimal position relative to the gradient by reducing a 3-dimensional search problem to a 1-dimensional search problem (see Figure 2) (Frankel et al., 1997). MAGNETOTACTIC BACTERIA, “MAGNETOFOSSILS”, AND LIFE ON MARS Magnetite crystals presumably originating from magnetotactic bacteria have been found in many recent freshwater and marine sediments (e.g., Chang et al., 1989a) as well as from ancient sediments ~ 2 Ga years old (Chang et al., 1989b) and have been referred to as “magnetofossils”. The pertinent question is whether Fe3O4 and/or Fe3S4 crystals with specific morphologies can be used as “biomarkers”, indicators of the past presence of magnetotactic bacteria. In some cases where magnetotactic bacteria are still present, the use of these crystals appears justified but there are many sites particularly in ancient sediments where the organisms are no longer present. In addition, the biogeochemical processes involved in preserving and dissoluting these magnetofossils in sediments are not well understood. A number of researchers are convinced that specific morphological types of Fe3O4, particularly the anisotropic elongated prismatic crystals (also earlier referred to as parallelepipedal), can be used unequivocally in this way because there is currently no known means of synthesizing these particles, either by natural geological

processes or by chemical synthesis (Thomas-Keprta et al., 2000, 2001). However, others remain unconvinced. Intensive electron microscopy and chemical studies have been performed on Fe3O4 particles from magnetotactic bacteria, particularly those from strain MV-1, and, based on results from these studies, a series of 6 criteria have been established for the determination of whether Fe3O4 crystals are biogenic or not. These criteria are: (1) narrow size range (i.e., that of single-magnetic-domain crystals for uniform magnetization of the particle); (2) specific particle morphologies with restricted width-to-length ratios that have never been observed in chemically-synthesized Fe3O4 crystals; (3) high chemical purity; (4) the presence of few crystallographic defects; (5) unusual truncated hexa-octahedral geometry (referring to the geometry of strain MV-1 particles); and (6) elongation along a specific crystallographic axis, in strain MV-1, the (111) crystallographic axis (Thomas-Keprta et al., 2000, 2001). In 1996, McKay et al. (1996) described a number of mineralogical and other features from the Martian meteorite ALH84001 that may have resulted from biological processes on ancient Mars. This meteorite has a radiogenic Rb-Sr crystallization age of ~4.5 Ga (Nyquist et al., 2001), indicating it formed shortly after the planet Mars itself was formed. It was ejected into interplanetary space from the Martian surface ~16 Ma ago (Goswami et al., 1997), presumably as a consequence of a collision of an asteroid or comet with Mars, and ~13 Ka ago it was captured by the Earth’s gravity field, and fell as a meteorite in Antarctica (Jull et al., 1995). ALH84001 has experienced multiple shock events (Treiman and Romanek, 1998) and at least one, if not more, episodes of aqueous alteration (Wilde et al., 2001). Included in these features described by McKay et al. (1996) was the presence of ultrafine-grained Fe3O4, pyrrhotite (Fe7S8) and possibly Fe3S4 within ALH84001. The Fe3O4 crystals were reported to range from about 10 to 100 nm, were in the superparamagnetic and single-magnetic-domain size ranges, and were cuboid, teardrop and irregular in shape. The iron sulfide particles varied in size and shape, with the Fe7S8 particles ranging up to 100 nm. The mineral particles were embedded in carbonate globules, a significant feature of this meteorite, that consist of an optically golden-colored core concentrically zoned in calcium, manganese, iron, and magnesium carbonate (Valley et al., 1997) in which nanometer-sized Fe3O4 crystals are evenly distributed as a minor phase (Valley et al., 1997). Surrounding the core is an inner and outer rim composed mainly of tens-of-nanometer-sized magnetite crystals embedded in a magnesium-rich iron carbonate, which are separated by a band of nearly pure magnesium carbonate matrix (Thomas-Keprta et al., 2000, 2001). Optically this appears as a layered black-white-black colored rim. Since the carbonate globules are Martian, then the Fe3O4 crystals are assumed to also be of Martian origin. Magnetite crystals in ALH84001 carbonates have been extensively studied, both those in situ and those extracted from the carbonate globules, by high resolution



transmission electron microscopy (Thomas-Keprta, 2000, 2001). A chemically and physically diverse distribution of Fe3O4 crystals are present in ALH84001, ranging in size from ~10 to 500 nm, with aspect (width/length) ratios from ~0.1 to 1.0, exhibiting poorly defined to well-faceted geometries, and vary from chemically impure to pure, and with and without defects. Approximately 75% of the ALH84001 Fe3O4 particles have been discounted as biogenic precipitates because they are either: (1) irregularly shaped showing two-dimensional projections that can be described as semi-circular, convex irregular, concave irregular, and teardrop-shaped; (2) have a whisker/platelet shape; or, (3) have an octahedral or cubo-octahedral geometry consistent with that observed in inorganically-produced Fe3O4 crystals (Thomas-Keprta et al., 2000, 2001). Most of these Fe3O4 crystals also do not show a consistent chemical purity, some containing minor amounts of aluminum and/or chromium (Thomas-Keprta et al., 2000, 2001). The origin(s) of these particles is (are) unknown but may be ascribed to processes such as in situ thermal/shock decomposition of Fe-carbonate (Golden et al., 2001), the allochthonous accumulation of Fe3O4 during the growth of the carbonate from hydrothermal fluids, the hydrothermal precipitation of Fe3O4 from a Fe-rich fluid, or the formation of BIM Fe3O4 by dissimilatory Fe-reducing bacteria. The remaining ~ 25% of the ALH84001 Fe3O4 crystals appear to be morphologically identical to those produced by a marine magnetotactic bacterium called strain MV-1 and generally meet the 6 criteria described above for biogenic Fe3O4 (Thomas-Keprta et al., 2000, 2001). On Earth, the observation of this type of Fe3O4 crystals would be interpreted by many as a biosignature indicative of the past presence of magnetotactic bacteria. Thus in ALH84001 carbonates, the presence of these type of Fe3O4 particles are also interpreted by some to be biosignatures of Martian magnetotactic bacteria. An alternative explanation is that the Fe3O4 crystals are the products of an unknown inorganic geochemical process that has not yet to been recreated in the laboratory. The fact that only ~25% of the ALH84001 Fe3O4 crystals meet the criteria for a biosignature is not surprising because: (1) terrestrial magnetofossils are typically found in environments abundant in inorganically-produced Fe3O4 resulting in an intimate mixture of biogenic and inorganic Fe3O4; (2) most of the information on ALH84001 Fe3O4 particles has come from those extracted by acid dissolution of the carbonate which destroys the distribution and spatial relationship between the crystals resulting in a homogenized sample; (3) other strains of terrestrial magnetotactic bacteria and dissimilatory Fe-reducing organisms do not produce Fe3O4 crystals like those of strain MV-1 that are easily distinguishable from those produced inorganically; and (4) even in strain MV-1 only ~70% of the Fe3O4 particles fulfill all of the 6 criteria (in other words, not all particles produced by a given strain of magnetotactic bacterium show the same morphology exactly) (Thomas-Keprta et al., 2000, 2001). An additional criterion for distinguishing biogenic Fe3O4 crystals is the presence of chains of Fe3O4 particles as they are found within most cells of magnetotactic

bacteria. This criterion has not been accepted by many researchers in the field since chain formation can be induced by high magnetic fields similar to those used in collecting magnetic particles from sediments. It is noteworthy that there is some evidence that chain formation of Fe3O4 particles occurs in ALH84001 as if magnetotactic bacteria were somehow trapped within the meteorite (Friedmann et al., 2001). However, the structures presumably found to be arranged in chains in ALH84001 were not proven unequivocally to be Fe3O4. In a recent study, Golden et al. (2001) synthesized ALH84001-like carbonate globules containing single-magnetic-domain, chemically pure, and lattice defect-free Fe3O4 particles in the globule rim regions by precipitating zones of siderite (FeCO3) from CO2-rich fluids under hydrothermal conditions and then heating the carbonate globules to ~470˚C under 13.3 kPa CO2 pressure simulating a thermal event. The morphology of the Fe3O4 crystals was not described. Whether magnetotactic bacteria like those on Earth could have lived or live on Mars is unknown and beyond the scope of this paper. The arguments presented briefly above have been reviewed extensively (e.g., Frankel and Buseck, 2000) and there is no doubt the debate will continue (Buseck et al., 2001). It seems likely it will take more than evidence from a single Martian meteorite to convince the majority of the scientific community that life existed or exists on Mars. CONCLUSIONS AND FINAL REMARKS The crystal size, crystallographic orientation, and the assembly of magnetosomes in chains in magnetotactic bacteria are all extremely important for the function of magnetotaxis in the geomagnetic field. The magnetosome chain is a masterpiece of permanent magnetic engineering that causes each cell to be a self-propelled magnetic dipole that is sufficiently magnetic to be oriented in the geomagnetic field overcoming thermal (Brownian) forces tending to randomize the orientation of the cell, yet fits into cells that are generally only several microns in diameter and can be assembled in situ. The cells swim along geomagnetic field lines and use chemotaxis (aerotaxis) to efficiently locate and generally remain at their optimal O2 concentration in vertical oxygen concentration gradients in chemically stratified water columns or sediments. A large number of organisms other than bacteria have been reported to be influenced by the Earth’s geomagnetic field including invertebrates such as protists (Torres de Araujo et al., 1986; Bazylinski et al., 2000), insects (Walker and Bitterman, 199), and mollusks (Lohmann and Willows, 1987) and vertebrates such as fish (Walker et al., 1997), amphibians (Phillips, 1986), reptiles (Lohmann, 1991) , birds (Walcott and Green, 1974; Walcott et al., 1979), and mammals (Walker et al., 1992) including humans (Kirschvink et al., 1992; Kobayashi and Kirschvink, 1995). Magnetite crystals virtually morphologically indistinguishable from those produced by the magnetotactic bacteria have been found in a number of different protist (Torres de Araujo et al., 1986;



Bazylinski et al., 2000), in the ethmoid tissues of tuna and salmon and other animals (Sparks, 1990), and in the human brain (Kirschvink et al., 1992; Kobayashi and Kirschvink, 1995). Honeybees (Kuterbach et al., 1982) and pigeons (Walcott et al., 1979) appear to contain particles of Fe3O4 or hydrous iron oxides that could be precursors to Fe3O4. The fact that many higher creatures biomineralize single-magnetic-domain Fe3O4 crystals of similar morphologies suggests the intriguing idea that that all these organisms share the same or a similar set of genes responsible for Fe3O4 biomineralization that would likely have originated in the magnetotactic bacteria. Taking the above into consideration and the fact that the same types of Fe3O4 crystals are found in at least some Martian meteorites, these particles are indeed promiscuous as to their presence. Whether or not they will prove to be an effective biomarker remains to be seen. ACKNOWLEDGEMENTS

I thank my many collaborators over the years for their participation in much of the work described herein, particularly P.R. Buseck, R.B. Frankel, D.S. McKay, B.M. Moskowitz, and K.L. Thomas-Keprta. I also thank B. Dubbels for help with figures and P. Gould, R. Gould, M. King, and M. Lindup for inspiration. I am grateful for support from U.S. National Science Foundation grant CHE-9714101 and NASA Johnson Space Center grant NAG 9-1115. REFERENCES Balkwill, D.L., Maratea, D. and Blakemore, R.P. 1980. Ultrastructure of a magnetic spirillum. Journal of Bacteriology 141:1399-1408. Bazylinski, D.A. 1995. Structure and function of the bacterial magnetosome. ASM News 61:337-343. Bazylinski, D.A. and Frankel, R.B. 2000. Biologically-controlled mineralization of magnetic iron minerals by magnetotactic bacteria. In: Environmental Microbe-Mineral Interactions. (Lovley, D.R., Ed.), Washington, D.C.: ASM Press, pp. 109-144. Bazylinski, D.A., Frankel, R.B., Heywood, B.R., Mann, S., King, J.W., Donaghay, P.L. and Hanson, A.K. 1995. Controlled biomineralization of magnetite (Fe3O4) and greigite (Fe3S4) in a magnetotactic bacterium. Applied Environmental Microbiology 61:3232-3239. Bazylinski, D.A., Garratt-Reed, A.J. and Frankel, R.B. 1994. Electron microscopic studies of magnetosomes in magnetotactic bacteria. Microscopy Research and Technique 27:389-401. Bazylinski, D.A., Garratt-Reed, A.J., Abedi, A. and Frankel, R.B. 1993a. Copper association with iron sulfide magnetosomes in a magnetotactic bacterium. Archives of Microbiology 160:35-42.

Bazylinski, D.A., Heywood, B.R., Mann, S. and Frankel, R.B. 1993b. Fe3O4 and Fe3S4 in a bacterium. Nature 366:218. Bazylinski, D.A. and Moskowitz, B.M. 1997. Microbial biomineralization of magnetic iron minerals: microbiology, magnetism and environmental significance. In: Geomicrobiology: Interactions Between Microbes and Minerals. (Banfield, J.F. and Nealson, K.H., Eds.) Washington, D.C.: Mineralogical Society of America. Reviews in Mineralogy 35:181-223. Bazylinski, D.A., Schlezinger, D.R., Howes, B.L., Frankel, R.B. and Epstein, S.S. 2000. Occurrence and distribution of diverse populations of magnetic protists in a chemically-stratified coastal salt pond. Chemical Geology 169:319-328. Berner, R.A. 1964. Iron sulfides formed from aqueous solution at low temperatures and atmospheric pressure. Journal of Geology 72:293-306. Berner, R.A. 1967. Thermodynamic stability of sedimentary iron sulfides. American Journal of Science 265:773-785. Blakemore, R.P. 1975. Magnetotactic bacteria. Science 190:377-379. Blakemore, R.P. 1982. Magnetotactic bacteria. Annual Reviews of Microbiology 36:217-238.

Blakemore, R.P., Frankel, R.B. and Kalmijn, A.J. 1980. South-seeking magnetotactic bacteria in the southern hemisphere. Nature 236:384-385. Bradley, J.P., Harvey, R.P. and McSween Jr., H.Y. 1996. Magnetite whiskers and platelets in the ALH84001 martian meteorite: evidence for vapor phase growth. Geochimica et Cosmochimica Acta 60:5149-5155. Buseck, P.R., Dunin-Borkowski, R.E., Devouard, B., Frankel, R.B., McCartney, M.R., Midgley, P.A., Posfai, M. and Weyland, M. 2001. Magnetite morphology and life on Mars. Proceedings of the National Academy of Sciences of the United States of America 98:13490-13495. Chang, S.-B.R. and Kirschvink, J.L. 1989a. Magnetofossils, the magnetization of sediments, and the evolution of magnetite biomineralization. Annual Review of Earth and Planetary Sciences 17:169-195. Chang, S.-B.R., Stolz, J.F., Kirschvink, J.L. and Awramik, S.M. 1989b. Biogenic magnetite in stromatolites. 2. Occurrence in ancient sedimentary environments. Precambrian Research 43:305-312.



Devouard, B., Pósfai, M., Hua, X., Bazylinski, D.A., Frankel, R.B. and Buseck, P.R. 1998. Magnetite from magnetotactic bacteria: size distributions and twinning. American Mineralogist 83:1387-1398. Eberl, D.D., Drits, V.A. and Srodon, J. 1998. Deducing growth mechanisms for minerals from the shapes of crystal size distributions. American Journal of Science 298:499-533. Farina, M., Esquivel, D.M.S., Lins de Barros, H.G.P. 1990. Magnetic iron-sulphur crystals from a magnetotactic microorganism. Nature 343:256-258. Frankel, R.B., Bazylinski, D.A., Johnson, M. and Taylor, B.L. 1997. Magneto-aerotaxis in marine, coccoid bacteria. Biophysical Journal 73:994-1000. Frankel, R.B. and Blakemore, R.P. 1980. Navigational compass in magnetic bacteria. Journal of Magnetism and Magnetic Materials 15-18:1562-1564. Frankel, R.B., Blakemore, R.P., Torres de Araujo, F.F., Esquivel, D.M.S. and Danon, J. 1981. Magnetotactic bacteria at the geomagnetic equator. Science 212:1269-1270. Frankel, R.B., Blakemore, R.P. and Wolfe, R.S. 1979. Magnetite in freshwater magnetotactic bacteria. Science 203:1355-1356. Frankel, R.B. and Buseck, P.R. 2000. Magnetite biomineralization and ancient life on Mars. Current Opinion in Chemical Biology 4:171-176, 2000. Friedmann, E.I., Wierzchos, J., Ascaso, C. and Winklhofer, M. 2001. Chains of magnetite crystals in the meteorite ALH84001: evidence of biological origin. Proceedings of the National Academy of Sciences of the United States of America 98:2176-2181. Golden, D.C., Ming, D.W., Schwandt, C.S., Lauer Jr., H.V., Socki, R.V., Morris, R.A., Lofgren, G.E. and McKay, G.A. 2001. A simple inorganic process for formation of carbonates, magnetite, and sulfides in Martian meteorite ALH84001. American Mineralogist 86:370-375. Gorby, Y.A., Beveridge, T.J. and Blakemore, R.P. 1988. Characterization of the bacterial magnetosome membrane. Journal of Bacteriology 170:834-841. Goswami, J.N., Sinha, N., Murty, S.V.S., Mohapatra, R.K. and Clement, C.J. 1997. Nuclear tracks and light noble gases in ALH84001: Preatmospheric size, fall characteristics, cosmic ray exposure duration and formation age. Meteoritics and Planetary Science 32:91-96. Heywood, B.R., Mann, S. and Frankel, R.B. 1991. Structure, morphology and growth of biogenic greigite

(Fe3S4). In: Materials Synthesis Based on Biological Processes. (Alpert, M., Calvert, P., Frankel, R.B., Rieke, P. and Tirrell, D., Eds.), Pittsburgh: Materials Research Society, pp. 93-108. Jull, A.J.T., Eastoe, C.J., Xue, S. and Herzog, G.F. 1995. Isotopic composition of carbonates in the SNC meteorites Allan Hills 84001 and Nakhla. Meteoritics 30:311-318. Kirschvink, J.L., Kobayashi-Kirschvink, A. and Woodford, B.J. 1992. Magnetite biomineralization in the human brain. Proceedings of the National Academy of Sciences of the United States of America 89:7683-7687. Kobayashi, A. and Kirschvink, J.L. 1995. Magnetoreception and electromagnetic field effects: sensory perception of the geomagnetic field in animals and humans. In Electromagnetic Fields: Biological Interactions and Mechanisms. (Blank, M., Ed.) Washington, DC: American Chemical Society, pp. 367-394. Kuterbach, D.A., Walcott, B., Reeder, R.J. and Frankel, R.B. 1982. Iron-containing cells in the honeybee (Apis mellifera). Science 218:695-697. Lohmann, K.J. 1991. Magnetic orientation by hatchling loggerhead sea turtles (Caretta caretta). Journal of Experimental Biology 155:37-49. Lohmann, K.J., and Willows, A.O.D. 1987. Lunar-modulated geomagnetic orientation by a marine mollusk. Science 235:331-334. Lovley, D.R. 1990. Magnetite formation during microbial dissimilatory iron reduction. In: Iron Biominerals. (Frankel, R.B. and Blakemore, R.P., Eds.) New York: Plenum Press, pp. 151-166. Lowenstam, H.A. 1981. Minerals formed by organisms. Science 211:1126-1131. Mann, S. and Frankel, R.B. 1989. Magnetite biomineralization in unicellular organisms. In: Biomineralization: Chemical and Biochemical Perspectives. (Mann, S., Webb, J. and Williams, R.J.P., Eds.) New York: VCH Publishers, pp. 389-426. Mann, S., Frankel, R.B. and Blakemore, R.P. 1984. Structure, morphology and crystal growth of bacterial magnetite. Nature 310:405-407. Mann, S., Sparks, N.H.C., Frankel, R.B., Bazylinski, D.A. and Jannasch, H.W. 1990. Biomineralization of ferrimagnetic greigite (Fe3O4) and iron pyrite (FeS2) in a magnetotactic bacterium. Nature 343:258-260. Manson, M.D. 1992. Bacterial chemotaxis and motility. Advances in Microbial Physiology 33:277-346.



McKay, D.S., Gibson Jr., E.K., Thomas-Keprta, K.L., Vali, H., Romanek, C.S., Clemett, S.J., Chillier, X.D.F., Maechling, C.R. and Zare, R.N. 1996. Search for past life on Mars: possible relic biogenic activity in Martian meteorite ALH84001. Science 273:924-930. Meldrum, F.C., Heywood, B.R., Mann, S., Frankel, R.B. and Bazylinski, D.A. 1993a. Electron microscopy study of magnetosomes in a cultures coccoid magnetotactic bacterium. Proceedings of the Royal Society of London, Series B 251:231-236. Meldrum, F.C., Heywood, B.R., Mann, S., Frankel, R.B. and Bazylinski, D.A. 1993b. Electron microscopy study of magnetosomes in two cultured vibriod magnetotactic bacteria. Proceedings of the Royal Society of London, Series B 251:237-242. Nyquist, L.E., Bogard, D.D., Shih, C-Y., Greshake, A., Stoffler, D. and Eugster, O. 2001. Ages and geologic histories of Martian meteorites. Space Science Reviews 96:105-164. Palache, C., Berman, H. and Frondel, C. 1944. Dana's System of Mineralogy. New York: Wiley, 384 p. Phillips, J.B. 1986. Two magnetoreception pathways in a migratory salamander. Science 233:765-767. Pósfai, M., Buseck, P.R., Bazylinski, D.A. and Frankel, R.B. 1998a. Reaction sequence of iron sulfide minerals in bacteria and their use as biomarkers. Science 280:880-883. Pósfai, M., Buseck, P.R., Bazylinski, D.A. and Frankel, R.B. 1998b. Iron sulfides from magnetotactic bacteria: structure, compositions, and phase transitions. American Mineralogist 83:1469-1481. Segall, J.E., Block, S.M. and Berg, H.C. 1986. Temporal comparisons in bacterial chemotaxis. Proceedings of the National Academy of Sciences of the United States of America 83:8987-8991. Silverman, M. and Simon, M. 1974. Flagellar rotation and the mechanism of bacterial motility. Nature 249:73-74.

Sparks, N.H.C. 1990. Structural and morphological characterization of biogenic magnetite crystals. In: Iron Biominerals. (Frankel, R.B. and Blakemore, R.P., Eds.) New York: Plenum Press, pp.167-177. Sparks, N.H.C., Mann, S., Bazylinski, D.A., Lovley, D.R., Jannasch, H.W. and Frankel, R.B. 1990. Structure and morphology of magnetite anaerobically-produced by a marine magnetotactic bacterium and a dissimilatory

iron-reducing bacterium. Earth and Planetary Science Letters 98:14-22. Taylor, B.L. 1983. How do bacteria find the optimal concentration of oxygen? Trends in Biochemical Sciences 8:438-441. Thomas-Keprta, K.L., Bazylinski, D.A., Kirschvink, J.L., Clemett, S.J., McKay, D.S., Wentworth, S.J., Vali, H., Gibson Jr., E.K. and Romanek, C.S. 2000. Elongated prismatic magnetite (Fe3O4) crystals in ALH84001 carbonate globules: potential martian magnetofossils. Geochimica et Cosmochimica Acta 64:4049-4081. Thomas-Keprta, K.L., Clemett, S.J., Bazylinski, D.A., Kirschvink, J.L., McKay, D.S., Wentworth, S.J., Vali, H., Gibson Jr., E.K., McKay, M.F. and Romanek, C.S. 2001. Truncated hexa-octahedral magnetite crystals in ALH84001: presumptive biosignatures. Proceedings of the National Academy of Sciences of the United States of America 98:2164-2169. Torres de Araujo, F.F., Pires, M.A., Frankel, R.B. and Bicudo, C.E.M. 1986. Magnetite and magnetotaxis in algae. Biophysical Journal 50:385-378. Towe, K.M. and Moench, T.T. 1981. Electron-optical characterization of bacterial magnetite. Earth and Planetary Science Letters 52:213-220. Treiman, A.H. and Romanek, C.S. 1998. Bulk and stable isotopic composition of carbonate minerals in Martian meteorite ALH84001: no proof of high formation temperature. Meteoritics and Planetary Science 33:737-742. Valley, J.W., Eiler, J.M, Graham, C.M., Gibson Jr., E.K., Romanek, C.S. and Stolper, E.M. 1997. Low-temperature carbonate concretions in the Martian meteorite ALH84001: evidence from stable isotopes and mineralogy. Science 275:1633-1638. Walcott, C., Gould, J.L. and Kirschvink, J.L. 1979. Pigeons have magnets. Science 205:1027-1029. Walcott, C. and Green, R. P. 1974. Orientation of homing pigeons altered by a change in the direction of an applied magnetic field. Science 184:108-182. Walker, M.M., and Bitterman, M.E. 1989. Honeybees can be trained to respond to very small changes in geomagnetic field intensity. Journal of Experimental Biology 145:489-494. Walker, M.M., Diebel, C.E., Haugh, C.V., Pankhurst, P.M. and Montgomery, J.C. 1997. Structure and function of the vertebrate magnetic sense. Nature 390:371-376. Walker, M.M., Kirschvink, J.L., Dizon, A.E. and Ahmed, G. 1992. Evidence that fin whales respond to the



geomagnetic field during migration. Journal of Experimental Biology 171:67-78. Wilde, S.A., Valley, J.W., Peck, W.H. and Graham, C.M. 2001. Evidence from detrital zircons for the existence of continental crust and oceans on the Earth 4.4 Gyr ago. Nature 409:175-178. Zhulin, I.B., Bespelov, V.A., Johnson, M.S. and Taylor, B.L. 1996. Oxygen taxis and proton motive force in Azospirillum brasiliense. Journal of Bacteriology 178:5199-5204.

magnetism and biology: the magnetotactic bacteria...

Documents