Filaments 0.02 ± 0.008 0.04 ± 0.016 0.0012 ± 0.00048 0.0024 ± 0.00097

Spheroids 0.12 ± 0.047 0.22 ± 0.086 0.0073 ± 0.00284 0.0133 ± 0.00519

Laminae 0.12 ± 0.047 1.00 ± 0.039 0.0073 ± 0.00284 0.0604 ± 0.00236

4. Discussion

For spheroidal and filamentous microfossils, the NanoSIMS C- and S- distributions are virtually identical to each other and to the CN- distributions, and a one-to-one correspondence exists with optical microscopic images (Figs. 2-6).

This suggests that all three elements (C, N, and S) are primarily remnants of biogenic organic matter. The size, shape, texture, and nature of the boundaries of the nanoscale remnants of C, N, and S of the filaments and spheroids constitute biosignatures for sedimentary remnants of these Proterozoic microorganisms.

Nitrogen is a good indicator of organic material because it is common in organic matter but rare in rock-forming minerals. Because nitrogen in rocks commonly derives from biological fixation processes, it can be considered an indicator of biological activity when associated with organic remains. While some chemical reactions might produce abiotic organics with nitrogen under certain hydrothermal or extraterrestrial conditions (Brearley, 2003; Ueno et al., 2004; Remusat et al., 2005), nitrogen associated with amorphous carbon in sedimentary rocks is most likely to be an indicator of biogenicity.

The S- probably represents a mixture of cellular sulfur with sulfur incorporated during early diagenesis by the common process of sulfurization (Kohnen et al., 1989; Eglinton et al., 1993; Werne et al., 2000; Brocks and Summons, 2003). While not completely understood, the process of sulfurization is thought to incorporate sulfur derived from pre-existing microbial remains or biologically reduced sulfur and reactive, inorganic sulfur species [e.g., from sulfate-reducing bacteria (Werne, 2002)]. Given the low metamorphic grade of the Bitter Springs Formation (Schopf et al., 2005b), the added sulfur is unlikely to have been derived from thermochemically produced H2S or volcanic sources. Therefore, the sulfur, though partially secondary, is nevertheless likely to be an indicator of microbial activity.

The general correspondence of relatively high Si- and O- yields with the microfossils was a surprise (Figs. 2E and F, 6E and F, and 7E and F). This is partly a reflection of the contrast that was used to illustrate those images. In Fig. 5F, for example, a background response for Si- and O- from chert can be seen within the cells imaged. The enhanced yields of Si- and O- associated mainly with the organic matter may be ascribed to (1) a matrix effect, in which secondary Si-and O- yields are greater in organic-rich regions compared with areas of "pure" chert lacking organic material and/or (2) the silicification process, whereby silica has nucleated on organic surfaces during permineralization (Oehler and Schopf, 1971; Oehler, 1976; Benning et al., 2002; Phoenix et al., 2000, 2002; Toporski et al., 2002; Yee et al., 2003), and as a result, the Si- and O- concentrations are actually greater in the region of organic matter compared with the concentrations imaged from the chert. Both processes may be at work, and follow-up studies will be aimed at investigating this further.

N/C ratios determined for the different structures range over two orders of magnitude, and such large variations are likely to be significant (Table 1), though we caution that the N/C results are preliminary. There are two types of instrumental fractionation (referred to as "matrix effects") that might affect measured CN-/C-and, therefore, the calibrated N/C ratios. These can occur because (1) the kerogen that makes up the microfossils and organic laminae is measured in its matrix of silica, while the standard was measured in purified acid extracts, and (2) the standard is an Eocene type I kerogen from the Green River Shale (i.e., rich in aliphatic chains), whereas kerogen in the nearly 1 billion year old Bitter Springs chert is likely to be much more aromatic. However, such matrix effects typically only result in differences of a few percent, and so it is highly unlikely that such effects could account for the two-orders-of-magnitude variation among the measured CN-/C- ratios of the different Bitter Springs structures. Thus, the large disparity in CN-/C- ratios of the Bitter Springs spheroids, filaments, and laminae is likely to be real.

In addition, the 2a error calculated for the CN-/C- of the kerogen standard includes the statistical ion counting and the reproducibility determined by measuring four different locations on the standard; that is CN-/C- = 0.414 ± 0.083 (2a). The 2a errors reported for CN-/C- measured in multiple locations in each type of Bitter Springs structure would include similar effects (Table 1). In summary, while the statistical error on the standard can be used for precise comparisons with statistical errors determined for measured CN-/C- of Bitter Springs structures, the N/C atomic ratios determined for the structures should be regarded as semi-quantitative estimates.

The CN-/C- ratios of the filaments were found to be significantly lower (0.02-0.04) than the ratios of the spheroids (0.12-0.22). This difference is unlikely to be attributable to subtle diagenetic differences (since all structures are from the same thin section), and there is no evidence of hydrothermal activity or meteoritic contribution, which could account for abiotic formation of organic compounds. Thus, the large disparity in the CN-/C- ratios would seem likely to reflect original differences in the biological precursor materials. This interpretation is consistent with the preservation of an exopolysaccharide precursor for the sheath-like material, which would have surrounded the living filaments, and a peptidoglycan precursor (with much higher expected nitrogen content) for the material that would have been contained in the outer cell walls of the spheroids.

Similarly, a disparity in the original chemistry of the two types of microfossils may explain the apparently thicker and more continuous pattern of silicifica-tion in the filaments compared to that in the spheroids (cf. Figs. 6E and F and 5A, B, and F). If the filamentous forms are remnants of mucilaginous sheaths, then their originally exopolysaccharide chemistry may have promoted more extensive silicification (by a combination of permeation and encrustation) than occurred on the peptidoglycan of the walls of the spheroids. This possibility is suggested by artificial permineralization studies in which laboratory-fossilized microbial filaments with sheaths were both encrusted and permeated by silica (Oehler, 1976). It is supported further by recent studies showing that active per-mineralization favors exopolysaccharides of cyanobacterial sheaths (Phoenix et al., 2000, 2002; Yee et al., 2003).

Surprisingly, the organic laminae contain filamentous and apparently compressed spheroidal structures that are defined by strong enrichments in C-, CN-, and S- (Fig. 7). These microfossil-like structures in the organic laminae are also characterized by sizes and thicknesses reminiscent of the well-preserved microfossils in the mineral matrix of the rocks (cf. Figs. 2, 4, and 7). Thus, the laminae are interpreted as most likely representing remnants of densely packed microbial mats. This conclusion is consistent with the generally accepted view that such laminae are derived from biological precursors that are simply less well preserved than the optically recognizable filaments and spheroids. Since obvious microfossils were not apparent within the laminae, using optical microscopy or scanning electron microscopy (Figs. 1 and 8), this result also demonstrated the potential of NanoSIMS to reveal new structure in kerogenous organic materials that were presumed to be generally amorphous.

CN-/C- and N/C ratios for the laminae displayed higher absolute values and a much greater range than equivalent values from the individual spheroids and filaments (Table 1). The higher absolute values may reflect greater degradation in the laminae, which would result in increased CN-/C- values through oxidation of organic carbon and/or addition of nitrogen by microbial nitrification; such degradation also could account for the relatively poor state of preservation in the laminae, as noted above. The large range in CN-/C- values could also result from laminae that contain a mixture of microbial constituents; such a mixture might be composed of compressed filaments and spheroids that originally were similar in size and shape to the well-preserved microfossils and other microbial constituents of the ecosystem (e.g., Des Marais, 2003) or possible remnants of biofilms.

Modern bacteria have N/C ratios that range from 0.15 to 0.28 (Fagerbakke et al., 1996; Fukuda et al., 1998), values that are much higher than those from either the individual microfossils or the laminae (overall range of 0.0012-0.0604; Table 1). However, the N/C ratios from the laminae (0.0073-0.0604) overlap with

Figure 8. Scanning electron microscopy (SEM) (left) and NanoSIMS (right) comparison of organic lamina in a polished thin section of chert from the Bitter Springs Formation. The white ovals show the same area in each image and these ovals correspond to the ovals in Fig. 7; arrows show corresponding structures. The dashed arrows illustrate a structure suggestive of a cross section of a filament; in NanoSIMS, the structure is defined by C, CN, S, Si, and O enrichment (only C enrichment is illustrated here; see Fig. 7 for other element maps); in the backscattered SEM image, a faint hint of the same structure is seen.

Figure 8. Scanning electron microscopy (SEM) (left) and NanoSIMS (right) comparison of organic lamina in a polished thin section of chert from the Bitter Springs Formation. The white ovals show the same area in each image and these ovals correspond to the ovals in Fig. 7; arrows show corresponding structures. The dashed arrows illustrate a structure suggestive of a cross section of a filament; in NanoSIMS, the structure is defined by C, CN, S, Si, and O enrichment (only C enrichment is illustrated here; see Fig. 7 for other element maps); in the backscattered SEM image, a faint hint of the same structure is seen.

the range of values reported in bulk kerogen samples from a variety of Precambrian cherts [0.0015-0.03 (Beaumont and Robert, 1999)]. The larger ranges of N/C ratios of the bulk kerogens and Bitter Springs laminae (compared to that reported for modern bacteria) likely represent a combination of (1) mixtures of precursor organisms, (2) early diagenetic changes that altered the original N/C ratios (for example, Gillaizeau et al., 1997; Bennett and Love, 2000), and (3) microbial degradation. Indeed, a large range in N/C ratios, such as we have observed in the organic laminae, may be a characteristic and, thus, a biosignature of a degraded biological community.

5. NanoSIMS of Organic Materials in Extraterrestrial Samples

The sub-micron scale resolution of NanoSIMS is ideally suited to studying elemental and isotopic composition of organic material that is found in some extraterrestrial materials, and the technique is now being applied to gain information about the formation and occurrence of organic compounds in the solar system. Particularly interesting recent studies include (1) that by Nakamura-Messenger et al. (2006) on the Tagish Lake carbonaceous chondrite meteorite which found organic globules that might represent types of prebiotic carbon compounds that might have been delivered to a young Earth; (2) those of Floss and Stadermann (2005) and Floss et al. (2004) on organics in interplanetary dust particles; (3) recently-published first results on particles collected from Comet Wild 2 in the Stardust Mission (Sandford et al., 2006); and (4) ongoing work on organics in the Nakhla Martian meteorite (Gibson et al., 2006; McKay et al., 2006). Eventually, NanoSIMS-derived chemical composition will be compared for extraterrestrial organic materials and ancient terrestrial organic residues; these comparisons should provide new insight into the sources of organic materials on earth, their relationship to the evolution of life on earth, and the potential for development of life elsewhere in the solar system.

6. Summary and Conclusions

The results of the NanoSIMS study described have demonstrated that in situ elemental composition of Proterozoic microfossils can be mapped and quantified with NanoSIMS at a spatial resolution of about 50 nm. The spatial correspondence of C, N, and S, along with the N/C ratios, provides new biosignatures for specific Proterozoic microorganisms and remnants of microbial communities. Moreover, N/C ratios as well as the distinctive patterns of silicification in the filaments and spheroids are suggestive of original differences in their chemical makeup (i.e., an exopolysaccharide precursor for the sheath-like filamentous forms vs. a peptidoglycan precursor for the walls of the spheroids). Finally, NanoSIMS

images of organic laminae previously thought to be amorphous reveal structures suggestive of densely packed remnants of microorganisms. These results are particularly notable, as the preponderance of organic matter in sedimentary rocks of any age occurs as similarly "amorphous," fragmentary remains, even in deposits with coexisting, bona fide microfossils (see Fig. 1, as an example). Therefore, it is possible that NanoSIMS will provide fresh insight into a large body of previously uninterpretable material.

Nevertheless, these first chemical maps of fossil cells are just a beginning. There are two additional types of chemical analyses possible with NanoSIMS that could provide significant new information about the nature of the organisms that produced these fossils: Namely, sub-micron scale analyses of (1) stable isotope ratios of H, C, N, and S and (2) elemental compositions of other potential indicators of biologic activity, such as Mg, Fe, and P. Both could provide insight into the metabolic pathways utilized by the ancient organisms that are fossilized in Precambrian-aged sediments.

Future work will aim at characterization of microfossils and organic fragments in Precambrian sedimentary rocks of varying ages, depositional environments, and lithologies. Key to selection of structures for this characterization will be their undisputed biogenicity, so that results can be used as a guide to interpreting less well-preserved, problematic materials. In situ stable isotope compositions from NanoSIMS will be performed and are expected to provide additional criteria for distinguishing biologically produced organic matter from that produced by abiotic mechanisms [e.g., 515N values of Precambrian kerogens generally are distinct from 515N of primitive organics in interplanetary dust particles and carbonaceous chondrites (Beaumont and Robert, 1999; Floss and Stadermann, 2005; Remusat et al., 2005)]. And finally, elemental analyses of the other potential metabolic indicators, such as Mg, Fe, and P, will be performed.

Thus, the new elemental and isotopic data obtainable with NanoSIMS will add significantly to the repository of criteria that can be used for assessing biogenicity and understanding the origin and significance of poorly preserved organic residues in some of the Earth's oldest rocks. In addition, establishment of nano-scale element and isotope ratios of early forms of life on earth and comparison with equivalent data from organic matter found in carbonaceous chondrites, Martian meteorites, cometary materials, and interplanetary dust particles, will provide new insight regarding the interplay of extraterrestrial organic compounds, the origin and early evolution of life on earth, and the potential for development of living systems on planetary bodies beyond earth.

7. Acknowledgements

We are grateful to Mary Ann Liebert, Inc. for granting permission to reprint sections of Oehler et al., 2006 (Astrobiology 6 (6): 838-850), on which much of this chapter is based. We thank the Astromaterials Research and Exploration Science

(ARES) Directorate at NASA-Johnson Space Center (JSC) and Centre National de la Recherche Scientifique (CNRS) for support. We are grateful to Drs. Carlton C. Allen (NASA - JSC), Malcolm Walter (Australian Centre for Astrobiology), and Jochen Brocks (Australian National University) for insightful comments and suggestions, and to Dr. Craig Schwandt and Ms. Georg Ann Robinson (JSC-ARES) for assistance with scanning electron microscopy. This work was partially supported by a PNP grant from the CNRS and NASA grant NRA-03-OSS-01-EXOB to D.S.M.

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Biodata of Maud Walsh and Frances Westall, authors of the chapter "Disentangling the Microbial Fossil Record in the Barberton Greenstone Belt: A Cautionary Tale"

Dr. Maud Walsh is an Associate Professor in the School of Plant, Environmental, and Soil Sciences at Louisiana State University, where her primary responsibilities are teaching and advising undergraduate students in the environmental management program. She received her Ph.D. in Geology from Louisiana State University in 1989. Here current research interests include the geological record of early life on Earth and environmental remediation and restoration. She has been involved for several years in several professional development programs for middle-school science teachers.

E-mail: [email protected]

Dr. Frances Westall is Director of research at the Centre de Biophysique Moléculaire of the CNRS, Orléans, France. Her main research interests are the earliest traces of life and the geological context of the early Earth, as well as the search for life on Mars. She is involved in the ExoMars mission to Mars (2013) and is participating in the planning of the future Mars Sample Return Mission. She is Director of the French Astrobiology Group (GDR-Exobiologie). She received her Ph.D. in Marine Geology from the University of Cape Town, South Africa, in 1984.

E-mail: [email protected]

Maud Walsh Frances Westall
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