Biogenic Magnetite Particles

Perhaps the most contentious discussions erupted around the magnetite crystals in ALH84001 (Fig. 1). They were claimed by McKay et al. (1996) to represent a biomarker for life on Mars. The original argument was based on the singledomain crystals, purity, and lack of structural defects of the magnetite grains. This idea was extended by Thomas-Keprta et al. (2000) who argued that 25% of the magnetite crystals in ALH84001 conformed to six properties, which constitute a robust Magnetite Assay for Biogenicity (MAB): (1) narrow size range, (2) restricted width to length ratios, (3) chemical purity, (4) few crystallographic defects, (5) crystal morphology, and (6) elongation along only one of the possible rotation axes of a regular octahedron. Magnetotactic bacteria, a widespread type of aquatic prokaryotes on Earth, synthesize intracellular magnetite crystals, called magnetosomes, which typically meet all properties in the MAB. The magnetite crystals in the magnetotactic bacteria appear aligned in chains, a highly unstable configuration that is achieved by means of cytoskeletal microfilaments and proteins (Scheffel et al., 2006; Komeili et al., 2006). Comparative studies of morphological and structural defects between magnetite crystals from magnetot-actic bacteria and from ALH84001 also seemed to support the biogenic origin of the later (Taylor et al., 2001), and single-domain magnetite crystals aligned in chains in ALH84001 were eventually found by Friedmann et al. (2001), who argued that they would be nearly impossible to produce inorganically and were consistent with a biological origin.

These claims were vigorously disputed. Barber and Scott (2002) noted that solid-state diffusion as a result of carbonate decomposition during impact heating could result in magnetite nano-crystals similar to those found associated to the carbonate globules. Thomas-Keprta et al. (2002) responded by pointing out that the heat necessary to decompose iron carbonates and form magnetite was not present and would require a homogenization of all magnetic dipoles. Instead, they observed considerable heterogeneity in the ALH84001 carbonates inconsistent with significant heating. Replicating the microscopy and crystallographic analyses conducted by Thomas Keprta et al. (2000, 2001, 2002), Golden et al. (2004) presented a detailed electron microscopy work on magnetite crystals extracted from ALH84001, and compared them to magnetite crystals from the magnetotactic bacteria strain MV-1. The authors concluded that the shape of the [111]-elongated magnetite crystals in ALH84001 is not identical to that from the bacterium MV-1, an argument that undermines the biogenic hypothesis. Bell (2007) conducted shock-recovery experiments with naturally occurring siderite, and obtained magnetite crystals with a similar composition, size and morphology as those found in ALH84001. The shock temperatures required for siderite composition were >470°C, somewhat in excess of the 300°C upper limit mentioned above for the formation of the carbonate globules. The author argued that local thermal excursions within the meteorite could account for the high temperatures required by this process, without substantially altering the bulk temperature of the rock.

While several authors have concluded that the magnetite crystals in ALH84001 cannot be taken as evidence for biological activity, it is important to note that some results supporting the biogenic hypothesis remain undisputed. Particularly intriguing is the claim by Friedmann et al. (2001) that chains of magnetite particles are present in ALH84001 in close association to the carbonate globules. The authors used backscattered-SEM to study undisturbed, carbonate-rich fragments of the meteorite, and imaged chains of Single-Domain magnetite crystals (Fig. 2). Auger Electron Spectroscopy and Energy Dispersive X-ray Spectroscopy showed that the particles in the chains contained a heavy element. Due to the limited resolution of these techniques, the exact chemical composition of the particles could not be determined, but based on indirect evidence the authors interpreted this heavy element to be Iron and concluded that the particles forming the chains where in fact magnetite. There are two main results published by Friedmann et al. (2001) that have not yet been disproved: (i) small crystals (ca. 50-100 nm) composed of (possibly) Fe and O occur in chain-like structures in the outer rim of the carbonate globules in the ALH84001, and (ii) these chains are not the result of terrestrial contamination. The only known process that has been shown to originate similar structures is magnetosome formation in the magneto-tactic bacteria. Moreover, in the same paper the authors identified five properties of the chains that may constitute a possible biosignature, namely: uniform crystal size and shape; gaps between crystals; orientation of elongation along the chain axis and flexibility of the chain. Friedmann et al. (2001) also reported electron-dense regions surrounding the chains. The electron dense regions were consistent with the magnetosomal matrices reported by Taylor and Barry (2004) and the electron-dense regions surrounding terrestrial magnetofossils reported by McNeill (1990). Barber and Scott (2002) argued that magnetite crystals growing on ledges and kink sites on microfractures could align in chains, however the authors failed to support their claim with any form of evidence.

Of all the original evidences for ancient life on Mars put forward by McKay et al. (1996), the carbonate globules, the presence of indigenous organic compounds and the occurrence of nanobacteria like structures and of minerals that resemble bacterial precipitates on Earth, remain plausible, albeit disputed. The conditions in which the carbonate globules formed are likely to remain highly speculative, given the lack of basic data required to build up realistic geochemical scenarios. PAHs, however Martian they might be, do not represent a good indicator of biological activity, and can hardly be considered evidence for life in

Figure 2. Top: Backscattered Scanning Electron Microscope (SEM-BSE) image of the magnetite-rich area around a carbonate globule. Brighter tonalities are indicative of elements with high atomic weight, and darker tonalities are indicative of lighter elements. Bottom: three SEM-BSE images of chains of particles (arrows) containing a high atomic weight element. Similar structures were interpreted as fossil chains of magnetosomes, analogue to those synthesized by terrestrial magnetotactic bacteria (By Friedmann et al. 2001). Scale Bars is 1 ^m. (Photo Credit: Jacek Wierzchos and Carmen Ascaso.)

Figure 2. Top: Backscattered Scanning Electron Microscope (SEM-BSE) image of the magnetite-rich area around a carbonate globule. Brighter tonalities are indicative of elements with high atomic weight, and darker tonalities are indicative of lighter elements. Bottom: three SEM-BSE images of chains of particles (arrows) containing a high atomic weight element. Similar structures were interpreted as fossil chains of magnetosomes, analogue to those synthesized by terrestrial magnetotactic bacteria (By Friedmann et al. 2001). Scale Bars is 1 ^m. (Photo Credit: Jacek Wierzchos and Carmen Ascaso.)

themselves, given their widespread existence in the universe. But the putative presence of nanobacteria and of fossil chains of magnetosomes do represent important contributions of ALH84001 to the search for life beyond our planet, and are still considered by some as indicators of past biological activity on Mars.

3. Martian Nanobacteria

The main argument against the nature of the bacteria-like structures in ALH84001 was their size, well below the theoretical limit proposed by the NAS panel of experts. However, estimating the theoretical size limit of life is not without problems.

As the experts in the panel pointed out: "Commonly used methods of measuring cell size have inherent uncertainties or possibilities of error. Perhaps more important, most cells found in nature cannot be cultivated. Thus, ignorance about biological diversity at small sizes remains large".

The lower limit in size for a free-living cell is set by the necessity of being large enough to house the required biological molecules to perform its basic functions (Koch, 1996). Because terrestrial life is our only model, our estimates on the lower size limit of life are therefore based on the minimum requirements of terrestrial microorganisms. However, the cell machinery of terrestrial organisms is a result of evolution and natural selection of traits that are not necessarily fully optimized in terms of size (Koch, 1996). Not just size but also cell shape is important; an efficient surface/volume ratio is likely the reason that many bacteria are rod-shaped, filamentous, vibrios, or fusiforms. These shapes increase the surface/ volume ratio because a sphere has the least surface for the volume enclosed. An organism inhabiting a nutrient depleted environment, would be the least limited by diffusion of resources into the cell if it is as small as possible in cross-section, even if that entails being longer (Koch, 1996).

In the past years a large amount of literature related to nanobacteria has accumulated. Most of that research is carried out within the medical community, where it is hypothesized that an extremely small self-replicating particle, that is ubiquitous in living terrestrial organisms, may be responsible for several types of urologic pathologies (i.e. Akerman et al., 1997, Wood and Shoskes, 2006, Shiekh et al., 2006). While these claims are disputed, research carried out in natural samples is providing a second line of evidence to the existence of nano-organisms, and further suggests that they may be more widespread and complex than previously thought (Folk, 1992, 1993; Uwins et al., 1998; Sommer et al., 2002; Miyoshi et al., 2005; Baker et al., 2006). Typically these deceptive forms of life seem to be characterized by their small size (80-500 nm), very slow growth rates, their capability to induced mineral precipitates, and their adaptability to extreme environmental conditions, including temperatures of up to 90°C, starvation, extremes of pH and oxidizing agents, and high doses of gamma radiation (Bjorklund et al., 1998; Wood and Shoskes, 2006).

Accepting the existence of nano-organisms does not imply that the putative fossils in ALH84001 are indeed remnants of past Martian life, however this would remain as a possible explanation. The conditions on the Martian surface have been intolerable to life likely for several billion years, particularly due to the high doses of radiation that bath the surface. ALH84001 was ejected from the Martian subsurface, and while radiation is not a major concern for organisms living underneath the uppermost layers of soil, starvation, extremely low temperatures, hyper-aridity and oxidizing agents also contribute to make life on Mars a difficult challenge, even in the subsurface. While the surface of Mars appears relatively stable and in equilibrium at large scales, things may be different at the microscale. Atmospheric photochemistry, transient dew and fog events, meteorite fallout, or daily radiation cycles are but a few processes that can induce a small disequilibrium in the conditions of the surface soil. Life feeds on disequilibrium and a form of life that is able to adapt its metabolism to these frequent and short-lasting events may be better suited to survive in these extreme environment. Because of their large surface/volume ratio, extremely small organisms may be more efficient at gathering resources from the environment in short periods of time. The transition from resistant (i.e. spore like) to active stages may also be more effective if the required morphological changes are small.

The notion of nanobacteria is an intriguing and interesting one, not only with regard to the search for life on Mars, but also with regard to life in our own planet. When samples are returned from Mars, there will be a battery of biological assays lined up to search for evidence of life. Nanobacteria will arguably be searched for too, and it is therefore necessary to unambiguously verify the existence of nanobacteria, and to establish a consensus in the scientific community. In that respect extreme environments such as the hyper-arid Atacama Desert or the Antarctic Dry Valleys, which are also important Martian analogs, may be ideal candidates to search for nano-bacteria, and if present, to understand their distribution, diversity and abundance.

4. Fossil Chains of Magnetosomes as Biomarkers on Mars

The use of fossil chains of magnetosomes as extraterrestrial biomarkers is also an important contribution of the research conducted around ALH84001. These biominerals could in principle resist billions of years of oxidative conditions on the Martian surface and near subsurface, and their intrinsic characteristics could be used to assess their biogenicity.

On Earth two general types of magnetotactic bacteria can be distinguished based on the type of minerals they synthesize: the iron-oxide type that mineralize crystals of magnetite (Fe3O4) and the iron-sulfide type that mineralize crystals of greigite (Fe3S4) (i.e. Bazylinski and Frankel, 2000). Magnetite producing magne-totactic bacteria have optimized their magnetotactic response by maximizing the magnetic moment per atom of ion of their intracellular magnetic crystals. This has resulted in defect free, nearly stoichiometric precipitates, with morphologies that increase the magnetic SD stability field (Witt et al., 2005). However, there seem to be more diversity in magnetosome morphology among greigite-producing magnetotactic bacteria, for example several particle morphologies have been observed within a single cell (Posfai et al., 1998b). Among this type of magnetotactic bacteria, transition metals other than Fe are incorporated in the magnetosomes, which often show defects in their crystal lattice (Posfai et al., 1998a, b). Furthermore, greigite magnetosomes occasionally contain a mixture of transient, non-magnetic, iron sulfide phases that likely represent mineral precursors to greigite; these non-magnetic crystals are still aligned in chains and fall within the magnetic SD size range (Posfai et al., 1998a, b).

Taking the biochemistry and ecology of all known magnetotactic bacteria on Earth as a reference, then the evolution of magnetotaxis on Mars at least required the presence of liquid water habitats and a planetary magnetic field. It has been established by orbiter measurements that Mars possessed a magnetic field early in its history (Acuña et al., 1999). Additionally, recent missions with landers and orbiters have provided evidence of aqueous sedimentation or aqueous alteration on the Martian surface, a finding consistent with models of liquid water near the surface (i.e. Squyres et al., 2004; Bibring et al., 2005), coexistent with the active Martian magnetic field.

0 0

Post a comment