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3.5 Detection and geochemical characterization of Earth’s earliest life (Agresti, House, Jögi, Kudryavstev, McKeegan, Runnegar, Schopf, Wdowiak)
Although the fossil record of Archean (>2,500-Myr-old) life is notably sparse (Schopf and Walter 1983; Schopf 1992a), it is both better known and biologically more diverse than is generally appreciated. Indeed, from even among the oldest deposits of the Archean, rocks ~3,200 to ~3,500 Myr in age, eight fossil-bearing units have been described (by some 40 workers from 7 countries), containing in toto both stromatolites and spheroidal and filamentous microfossils backed both by laser-Raman and carbon isotopic analyses of their kerogenous components. Despite this body of evidence, however, the biological origin of the most thoroughly documented of these assemblages - fossils from the second oldest of the eight units, the ~3,465-Myr-old Apex chert of Western Australia (Schopf and Packer 1987; Schopf 1992a, 1993) - has been questioned (Brasier et al. 2002), doubt that has recently been extended to include all reports of particularly ancient evidence of life, anything "older than, say, 3.0 billion years" (M.F. Brasier, quoted in the NASA-sponsored Astrobiology Magazine, January 2003). Such doubt raises a severe problem for Astrobiology. If current techniques are inadequate to establish the existence of early life on Earth, how can we expect them to uncover evidence of ancient life on other worlds? Research proposed in the following sections addresses this issue. 3.5.1 How can biogenicity be established? In a general sense, the answer to the question of biogenicity was shown decades ago when early workers in the field (Barghoorn and Tyler 1965; Cloud 1965; Barghoorn and Schopf 1965) first demonstrated that "Precambrian microfossils" are, indeed, true fossils. Namely, the biological origin of fossil-like microscopic objects can be established by demonstrating that they possess a suite of traits that are unique to life, traits that taken together are shared by fossils and living organisms but not by inanimate matter. Thus, the solution to the problem is to insist that claims of ancient fossils be backed by data that show what the fossil-like objects actually are - rather than what they seemingly might be or apparently are not - positive lines of evidence that when considered as a whole comprise a signature unique to living systems. Of the various traits thus used, three have been shown to be particularly useful: (1) the mm-scale morphology of the objects in question; (2) the carbon isotopic composition of organic matter associated with and/or comprising the fossil-like structures; and (3) the chemical (molecular) makeup of the fossil-like objects. In the case of organic-walled fossils, this is particulate carbonaceous kerogen. Each of these factors can yield strong evidence consistent with a biogenic interpretation. Yet none of them, if considered alone, has proven definitive and use of morphology alone has led to numerous errors of interpretation (Schopf and Walter 1983; Mendelson and Schopf 1992). Reliance on carbon isotopic evidence, by itself, has proven inconclusive (van Zuilen et al., 2002); in and of themselves, analyses showing that such objects are composed of geochemically mature organic matter establish only their carbonaceous makeup, not their biological origin (Schopf et al. 2002a). Nevertheless, other than biology, no mechanism is known that can yield communities of fossil-like objects that have cellular morphologies, exhibit a biologically distinctive carbon isotopic signature, and are themselves composed of particulate carbonaceous matter. Thus, if the three factors are taken together, as a suite of biologically indicative traits, the lines of evidence become mutually reinforcing and a biogenic interpretation, compelling. In principle, therefore, the question of biogenicity can be easily answered. But in practice, the answer has proven elusive, primarily because of a lack of analytical techniques having sufficient power to provide the high resolution three-dimensional morphological information needed to definitively address the question, and an absence of means by which to directly link, in individual microscopic specimens, morphological information to elemental-isotopic and structural-molecular compositions. Means are now at hand to solve this problem, due primarily to advances pioneered during the past three years by UCLA astrobiologists (House et al. 2000; Kudryavtsev et al. 2001; Kempe et al. 2002; Schopf et al. 2002b). Exploitation of these advances, coupled with development of the new analytical techniques outlined below, will provide a firm basis by which to establish or to refute the biogenicity of putative ancient fossils. 3.5.2 Microbial morphology as evidence for early life The fossil record of life's early microbial history is based primarly on "morphology," a term that subsumes a great many variables: organismal shape (e.g., coccoid or filamentous); cell shape, size, and surface ornamentation; structure and thickness of an encompassing sheath, if present; and many others (Schopf 1992b), and in taxonomic studies, routinely includes quantitative (morphometric) analyses of intra-taxon variability and population structure. But interpretation of morphology is notoriously subjective; a microscopic object regarded as a good fossil by one investigator may be considered to be a nonfossil artifact by another. Clearly, there is a need for hard and fast criteria by which to separate the bona fide from the bogus. For three-dimensionally permineralized (petrified) organic-walled fossils, the most life-like of all types of structurally preserved microscopic biologic remnants, a prime criterion is the mineral-infilled spheroidal or tubular structure defined by their enclosing carbonaceous cell walls, a character by which they differ decisively from solid mineralic pseudofossils (Ruiz et al. 2002). Backed by analyses establishing the chemical composition of the enclosing walls, such cellularity, combined with other morphologic features, can be used to unambiguously distinguish true fossils from mineralic look-alikes. At the current state of the science, high-resolution optical microscopy can demonstrate the requisite three-dimensional cellularity. In a fossil microbial trichome, for example, the presence of surrounding cell walls and regularly spaced transverse septa that enclose mineral-infilled cell lumina. But, because of the shallow depth of field of the high magnification (e.g., 100x) required to obtain such information, and the limitations imposed by scientific journals on space allotted for illustrative figures, the existence of such cellularlity cannot be effectively conveyed in published form without use of interpretive drawings (e.g., Schopf 1993). This is an unacceptably subjective means of data presentation. To remedy this deficiency, Schopf and coworkers plan to generate high resolution three-dimensional optical images of individual petrified microscopic fossils, an easily achievable technological advance that, combined with the chemical analyses outlined below, will provide data crucial to answering the question of biogenicity. 3.5.3 In-situ isotopic analysis The carbon isotopic composition of microfossil-associated Precambrian organic matter is known from thousands of measurements in hundreds of Precambrian deposits (Strauss and Moore 1992), studies that have traced isotopic signature of microbial photosynthesis to at least 3,500 Myr ago (Hayes et al. 1983; Strauss et al. 1992). Such analyses of bulk samples, however, yield average isotopic values of carbon derived from a mix of sources, including microfossils of diverse types and states of preservation as well as sapropelic carbonaceous particles of multiple origins. By making use of the spatial resolution afforded by ion microprobe mass spectrometry (e.g., the Cameca 1270 at UCLA), isotopic analyses have now been extended to the kerogenous materials comprising specific microscopic fossils (House et al. 2000; Ueno et al. 2001), an analytical advance that links morphology and carbon isotopic composition in individual fossil microorganisms. The potential of this technique has been barely tapped, and the analytical advance first developed at UCLA (House et al. 2000) has yet to be applied to all but one of the eight earliest fossil assemblages known. Schopf and colleagues therefore plan to combine this newly established method with three-dimensional optical and Raman imaging techniques to evaluate the putative biogenicity of ancient microscopic fossils in rock samples already on hand. These samples represent some of the oldest reputed fossiliferous units known and include those of the ~3,375 Myr old Kromberg and ~3,465 Myr old Apex deposits. 3.5.4 Molecular composition and geochemical alteration of organic matter Another important key to establishing the biological origin of ancient microscopic fossil-like objects is to link their morphology to their chemical composition. Studies of the molecular-structural makeup of the organic matter comprising such fossils have only recently begun, most effectively by laser-Raman imagery and atomic force microscopy (Kudryavtsev et al. 2001; Kempe et al. 2002; Schopf et al. 2002b). These analytical techniques have only just recently been applied to the kerogenous components of Precambrian organic-walled microfossils and associated sapropelic debris, yet they hold great promise. In particular, Raman imagery provides the means to correlate optically-discernable morphology with molecular structure in individual carbonaceous microfossils (Figure 3.5.4, Kudryavtsev et al. 2001; Schopf et al. 2002b). Atomic force microscopy studies of carbonaceous microfossils permit visualization of the sub-µm-scale micromorphology of their preserved kerogenous constituents (Kempe et al. 2002). Results thus far have demonstrated a one-to-one two-dimensional correlation between cellular morphology and chemical composition. But to answer the question of biogenicity unambiguously and to rule out the possibility that fossil-like objects represent some sort of solid mineralic (e.g., graphitic) sports of nature, these composition and structure-dependent visualization techniques must be extended to three dimensions. This will be achieved by the installation of a new, state-of-the-art laser Raman imaging facility at UCLA. Schopf and colleagues recently used laser-Raman imagery (Kudryavtsev et al. 2001; Schopf et al. 2002b) to conduct a comprehensive study of the chemistry of carbonaceous microscopic fossils permineralized in 25 fine-grained chert units ranging in age from Devonian to Archean. Results demonstrate that the structure of the spectra acquired varies systematically with the metamorphic grade of the fossil-bearing rock units sampled, the fidelity of preservation of the fossils studied, the color of the organic matter analyzed, and with both the H/C and N/C ratios measured in kerogens isolated from bulk samples of the fossil-bearing cherts (Schopf et al. in press). To compare quantitatively the systematic variations observed among the various spectra, this work introduces the concept of the Raman Index of Preservation (RIP), an approximate measure of the degree of geochemical alteration of the 25 kerogens analyzed. Deconvolution of the various spectra, facilitated by comparisons with spectra obtained from experimentally heated fossil specimens, has provided insight into the molecular and chemical makeup of ancient kerogens and the changes that accompany organic metamorphism. To refine and extend this work, arrangements have been made to obtain additional samples of kerogens that are well characterized as to maximum temperature (by vitrinite reflectance, palynomorph color, H/C ratios, etc.), from U.S. petroleum companies (via Dr. W. Dow) and from the Institut Français du Pétrole (via Dr. Mireille Vandenbroucke). Schopf and collaborators intend to analyze these ~400 specimens by Raman spectroscopy in order to provide a firm basis for calibrating the thermal (catagenic) history evidenced by their RIP values and to determine the activation energies that have resulted in loss of various chemical moieties as a function of their geologic (or laboratory-simulated) thermal histories. 3.5.5 Quantitative methods for evaluating the biogenicity of fossil stromatolites
Spectacular, conical stromatolites arranged in egg carton-like arrays were reported recently from 3.45 Gyr-old Warrawoona Group strata in Western Australia (Hofmann et al. 1999). These stromatolites are arguably the best evidence for the nature of early life on Earth because they may record some aspects of the behavior and ecology of early Archean microorganisms. However, it is first necessary to be convinced that these structures are, at least in part, biogenic constructions. Understanding their morphogenesis also serves as a prelude to lander and rover explorations of the ancient terrains of Mars because distinctive, large, and widely-distributed sedimentary structures of this type are an obvious target for astrobiological missions. The case for an abiotic origin for at least some Precambrian stromatolites was advanced by Grotzinger and Rothman (1996), who used a power spectral analysis to quantify the three-dimensional shape of some Paleoproterozoic stromatolites as observed in outcrops and in sawn sections. They believed that the stromatolite growth process could be modeled in 2+1 dimensions by the classic KPZ interface equation of condensed matter physics (Kardar et al. 1986). Although numerical show that this is not correct (Jögi and Runnegar 2002), Grotzinger and Rothman made a very important advance by showing how the terms in the KPZ equation (upward growth, surface-normal growth, diffusion, gaussian noise) can represent processes that are meaningful in sedimentological and biological contexts (sediment fallout, spherulitic crystallization, downslope movement, and environmental fluctuations, respectively). Simulations are carried out in 1+1 and 2+1 dimensions using code written by Jögi over the past three years. For small problems (say, 256 x 256 grid points), the calculations are performed locally on Sun workstations; larger arrays have been run using parallelized code on the San Diego Supercomputer Center’s IBM "Blue Horizon".
Results to date have shown conclusively that the KPZ equation, and others like it (EW; Edwards and Wilkinson 1982) are incapable of producing simulated structures that resemble the Archean coniform stromatolites from Western Australia. On the other hand, an equation that is important in the physics of metal atom sputtering (Smilaeur et al. 1999) simulates conical structures effectively (Figure 3.5.5). The reason is that the process being modeled (electron beam epitaxy) has an uphill component caused by an edge effect at the atomic scale. Thus, models constructed using this equation (SRK) incorporate an upslope diffusion term that is not present in KPZ-based models. As upslope diffusion is a process that is easily attributable to life but not to other non-vital environmental agents at anything larger than atomic scale, this parameter may provide a definitive test for biogenicity. There are other features of the Warrawoona stromatolites that need to be explored mathematically. The SRK equation produces cones that either slowly coalesce ("coarsen") or exhibit rounded tops and froth-like behavior in long simulations. Similar behaviors are seen in experimental and industrial settings when metals are deposited using these methods. Jögi and Runnegar have discovered that there is a narrow zone of stability between these two realms that corresponds to a phase transition between regimes controlled by the endmember EW (frothy) and SRK (coarsening) equations. Simulations that occupy this transition zone generate suitably conical structures (Figure 3.5.5) that do not coalesce. After numerous experiments of this kind, it is now possible to accurately specify the slope angles (in two orthogonal directions as in the stromatolites; Figure 3.5.5) and grow cones to a specified size. It should be emphasized that the only "environmental" input to these simulations is uncorrelated random noise. This and the values given to the various diffusion terms are the controlling parameters. They provide the beginnings of a precise understanding of the physical and biological factors that may have generated these ancient structures. The next step is to try to incorporate features not captured by the current model (down-dip asymmetry, higher-frequency wrinkles, etc.) and then to make careful, quantitative comparisons between the modeled stromatolites and the field exposures. This will require the development of more sophisticated metrics than the method used by Grotzinger and Rothman (1996), the production of 3D physical models using rapid prototyping technology, and additional analysis of the natural objects using digital images of outcrop and sawn sections, and, possibly, computerized X-ray tomography. Ultimately, the goal is to extend this approach to other distinctive stromatolite types.
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