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The presence of magnetite crystal chains in ALH84001 was demonstrated by high-power …


Biology Articles » Astrobiology » Chains of magnetite crystals in the meteorite ALH84001: Evidence of biological origin » Introduction

Introduction
- Chains of magnetite crystals in the meteorite ALH84001: Evidence of biological origin

In 1996, McKay et al. (1) suggested that the Martian meteorite ALH84001 harbors relics of early biological activity. Thomas-Keprta et al. (2) proposed that magnetite crystals in the meteorite are magnetofossils and postulated six criteria that characterize biologically produced magnetite crystals. The simultaneous presence of all six characteristics---i.e., a definite size range and width/length ratio, chemical purity, crystallographic perfection, arrangement of crystals in linear chains, unusual crystal morphology, and elongation of crystals in the [111] crystallographic direction---should constitute evidence of biological origin. These researchers demonstrated the presence of five of these characteristics but not of the sixth---i.e., magnetite crystals in linear chains---because the method used, dissolution of the carbonate in 20% acetic acid, causes the chains to collapse. Earlier, we reported magnetite chains in ALH84011 (3), and here we present more complete information. We used high-power backscattered scanning electron microscopy (SEM-BSE), a method introduced by two of us (J.W. and C.A.) to study endolithic microorganisms (e.g., see ref. 4). Whereas in conventional SEM (SEM-SE) images of surface structures are formed by reflected secondary electrons, SEM-BSE uses backscattered electrons that originate from below the surface, in our material from a depth of up to about 400-1000 nm, as determined by Monte Carlo trajectory simulation (5). SEM-BSE records not surface morphologies but chemical compositions, as structures composed of heavier elements appear brighter than those of lighter ones. Resolution is limited by the scattered nature of the signal, so images of very small objects appear fuzzy. Also, chains oriented obliquely to the image plane may not be resolved. To alleviate these problems, we used here SEM-BSE in the three-dimensional (stereo) mode. Our method thus made possible the in situ direct visualization of the spatial arrangement of nanometer-sized structures inside the rock substrate.

Magnetotactic Bacteria and Magnetosomes. Terrestrial magnetotactic bacteria form magnetosomes, single-domain crystals of magnetite (Fe3O4) or greigite (Fe3S4) surrounded by a biological membrane. The magnetosomes are arranged in linear chains, held together by organic material, which fills the narrow gaps between them (6, 7). Because of the elastic property of this material, the chains have a remarkable elastic stability (8). In the chains, the crystals are roughly cuboidal, elongated, or bullet-shaped, and the crystal morphology is characteristic of the species or strain. The size of crystals generally falls within the theoretical limits of single-domain grain size (9). Magnetotactic bacteria live mostly at the water-sediment interface in both marine and freshwater habitats, where microaerobic conditions are frequently present. The bacteria function as permanent magnetic dipoles and are passively aligned, like a compass, along the prevailing magnetic field lines (7). All magnetotactic bacteria are motile (10). Magnetotaxis appears to be advantageous for finding and maintaining an optimal position along a vertical O2 concentration gradient in an oxic/anoxic transition zone, characteristic of microaerobic environments (7, 11).

Magnetite Chains as Indicators of Biological Origin. The formation of magnetite crystals within a definite size range and their arrangement in linear chains is in itself a conspicuous example of genetically controlled biomineralization (7, 12). Magnetosome chains are not in the energetically most favorable configuration, as the total energy of the system can be reduced if the particles are allowed to collapse into a clump (13) or into a jackknife structure (14). No inorganic process is known to produce similar structures. Below we suggest five additional morphological characteristics that are present in biologically formed magnetite chains. The first four of these criteria, listed below, are evident from the numerous published transmission electron micrographs of various magnetotactic bacteria (e.g., in refs. 6, 7, 10, 11, 15, and 16), which show consistent morphological characteristics, whereas the fifth is based on observations (8) on postmortem changes in magnetosome chains in bacteria. Such magnetite chains could not be formed abiotically---e.g., in a strong magnetic field, by crystals concentrated at grain boundaries, or by being accidentally positioned into a narrow channel in the rock substrate.

(i) Uniform crystal size and shape within chains. Despite the considerable range of variation in magnetite crystal size and shape (isodiametric or elongated) within a bacterial species (2), the crystals within individual chains are of similar size because each is formed at the end of the chain as it grows into a preformed membrane vesicle, which appears to function as a template. (ii) Gaps between crystals. Crystals in chains are separated by gaps ascribable to the membrane bounding the magnetosomes and to the organic substance between them, as seen in Magnetospirillum magnetotacticum (Fig. 1C). Magnetite crystal chains formed nonbiologically (e.g., in a strong magnetic field) would abut without gaps. (iii) Orientation of elongated crystals. In chains of elongated magnetosomes the crystals are oriented with the long axes along the chain. The energetically more favorable arrangement would be a side-by-side position (i.e., with their long axes perpendicular to the chain axis) where every second particle has opposite magnetization as in a multidomain state, so as to reduce the magnetic stray field of the configuration. (iv) Halo (traces of membrane) around chains. At the magnifications used, the traces of membranes surrounding magnetosomes (6) should be detectable as thin halos around fossil chains. (v) Flexibility of chains. Magnetosome chains do not necessarily disintegrate upon death of the bacterium but may undergo strong but smooth bends (8) and become fossilized in that position (14). Mathematical analysis (8) has revealed that it is the elastic property of the soft organic material between the crystals (and not crystal morphology) that imparts stability and flexibility to such chains, resulting in deformations into smooth arcs (Fig. 2a). A chain with rigid gap filling will respond with a sharp kink in the middle of the chain (Fig. 2b), so that the whole elastic transformation is concentrated in a single gap rather than being equally distributed over all gaps. In Fig. 2, the total energy (W) of a magnetosome chain is plotted against the angle between the first and last magnetosome in the chain for soft and rigid gap fillings and for bend and kink modes of deformation. The energetically preferred deformation mode (lower value of W) is bending for soft gap filling but formation of a sharp kink for rigid gap filling. [Derivation of the W(a) curves and further details are given in Appendix 1, which is published as supplemental data on the PNAS web site, www.pnas.org.] Significantly, all soft and elastic, yet electron-transparent (low-atomic-number), substances are of biological origin, and no inorganic (mineral), naturally occurring substance is known to have such properties.

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