Biogenicity of Earth's earliest fossils: A resolution of the controversy

Biogenicity of Earth's earliest fossils: A resolution of the controversy

Gondwana Research 22 (2012) 761–771 Contents lists available at SciVerse ScienceDirect Gondwana Research journal homepage: www.elsevier.com/locate/g...

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Gondwana Research 22 (2012) 761–771

Contents lists available at SciVerse ScienceDirect

Gondwana Research journal homepage: www.elsevier.com/locate/gr

GR focus review

Biogenicity of Earth's earliest fossils: A resolution of the controversy J. William Schopf a, b, c,⁎, Anatoliy B. Kudryavtsev b, c a b c

Department of Earth and Space Sciences and Molecular Biology Institute, University of California, Los Angeles, CA 90095, United States Center for the Study of Evolution and the Origin of Life, University of California, Los Angeles, CA 90095, United States NAI PennState Astrobiology Research Center, University Park, PA 16802, United States

a r t i c l e

i n f o

Article history: Received 28 June 2012 Received in revised form 12 July 2012 Accepted 14 July 2012 Available online 24 July 2012 Handling Editor: M. Santosh Keywords: Apex chert Archean microfossils Confocal laser scanning microscopy Pilbara Craton Raman spectroscopy

a b s t r a c t The abundant and diverse assemblage of filamentous microbial fossils and associated organic matter permineralized in the ~ 3465 Ma Apex chert of northwestern Australia — widely regarded as among the oldest records of life — have been investigated intensively. First reported in 1987 and formally described in 1992 and 1993, the biogenicity of the Apex fossils was questioned in 2002 and in three subsequent reports. However, as is shown here by use of analytical techniques unavailable twenty years ago, the Apex filaments are now established to be bona fide fossil microbes composed of three-dimensionally cylindrical organic(kerogenous-) walled cells. Backed by a large body of supporting evidence of similar age — other microfossils, stromatolites, and carbon isotopic data — it seems clear that microbial life was present and flourishing on the early Earth ~ 3500 Ma ago. © 2012 International Association for Gondwana Research. Published by Elsevier B.V. All rights reserved.

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Introduction . . . . . . . . . . . . . . . . . . . . . . . . . 1.1. Synopsis of the controversy . . . . . . . . . . . . . . . 1.2. Similar episodes in the history of Precambrian paleobiology Apex chert microbial assemblage . . . . . . . . . . . . . . . . 2.1. Biologic diversity . . . . . . . . . . . . . . . . . . . . 2.2. Biologic relations . . . . . . . . . . . . . . . . . . . . 2.3. Mode of occurrence . . . . . . . . . . . . . . . . . . . Establishment of biogenicity . . . . . . . . . . . . . . . . . . Are the Apex Fossils Bona Fide Fossils? . . . . . . . . . . . . . 4.1. Carbonaceous composition . . . . . . . . . . . . . . . 4.2. Three-dimensional cellularity . . . . . . . . . . . . . . 4.3. Organic geochemical maturity . . . . . . . . . . . . . . 4.4. Carbon isotopic composition . . . . . . . . . . . . . . . 4.5. Organic geochemical composition . . . . . . . . . . . . Suggested nonbiologic origins . . . . . . . . . . . . . . . . . 5.1. Abiotic graphitic pseudofossils . . . . . . . . . . . . . . 5.2. Barium carbonate “biomorphs” . . . . . . . . . . . . . 5.3. Clay mineral pseudofossils . . . . . . . . . . . . . . . 5.4. Hematite veinlet pseudofossils . . . . . . . . . . . . . . 5.5. Multiple generations of kerogen . . . . . . . . . . . . . Discussion . . . . . . . . . . . . . . . . . . . . . . . . . .

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⁎ Corresponding author at: CSEOL, Geology Building, University of California, Los Angeles, Los Angeles, CA 90095‐1567, United States. Tel.: +1 310 825 1170; fax: +1 310 825 0097. E-mail address: [email protected] (J.W. Schopf). 1342-937X/$ – see front matter © 2012 International Association for Gondwana Research. Published by Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.gr.2012.07.003

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7. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction The microscopic fossils of the ~ 3465 Ma Apex chert of the northwestern Australian Pilbara Craton — first reported in 1987 (Schopf and Packer, 1987) and described in detail a few years later (Schopf, 1992, 1993) — are widely regarded as among the oldest evidence of life. Though they are not actually the “oldest fossils,” supplanted by reports of similar fossil microbes (Ueno et al., 2001a, 2001b, 2004) and megascopic stromatolites ~ 3496 Ma in age (Walter et al., 1980; Groves et al., 1981; Van Kranendonk, 2006), they are nevertheless especially well known, due primarily to their great age and morphological diversity. In some circles they are known also because of a controversy that for more than a decade has swirled about their biological interpretation — a problem that we regard as solved. We here summarize the history of this controversy, outline the evidence required to establish the biogenicity of putative ancient microbes, and show that these criteria are met by the Apex fossils but not by nonbiologic pseudofossils. 1.1. Synopsis of the controversy The following is a brief summary of the relevant history: (1) In February 2001, a manuscript was submitted to Nature by Brasier et al. that questioned the biological origin of the microbial fossils of the Apex chert, an interpretation proposed a decade earlier (Schopf and Packer, 1987; Schopf 1992, 1993). Several months later, in July 2001, we and our colleagues submitted a manuscript to Nature reporting our Raman spectroscopy-based finding that confirmed the original optical microscopy-based inference that the Apex fossils are composed of kerogenous organic matter — a finding, at the time, that was something of a “breakthrough,” this being the first rigorous application of Raman to rock-embedded organicwalled fossil microbes and a follow-up to our earlier “proof of concept” paper that documented the effectiveness of such studies (Kudryavtsev et al., 2001). Although our paper was formally accepted for publication in November 2001, the Nature editor elected to delay its appearance until March 2002 so that it could be published (Schopf et al., 2002) back-to-back with the paper by Brasier et al. (2002). (2) The Brasier et al. article confirmed that the carbon isotopic composition of the Apex organic matter is consistent with a biological origin (Strauss and Moore, 1992; Schopf, 1993) and that the fossils, like other permineralized Precambrian microbes, are composed of carbonaceous matter (Schopf and Packer, 1987; Schopf, 1992, 1993; Schopf et al., 2002). (3) Despite these biology-consistent data, Brasier et al. (2002, 2005) interpreted the Apex fossils to be nonbiological, suggesting that they are “graphite” mineral pseudofossils formed by the “self-organization” of nonbiological organic matter produced by Fischer–Tropsch-type abiotic syntheses. (4) Presumably spurred by this controversy, the Apex fossils have subsequently been suggested to be mineralic barium carbonate “biomorphs” (García-Ruíz et al., 2002, 2003), inorganic silica or clay mineral needle-like crystals (Pinti et al., 2009), or hematite-infilled veinlets (Marshall et al., 2011). This last report was followed by a study interpreting the Apex organics to have

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two differing, perhaps nonbiological origins (Marshall et al., 2012). None of these studies is reported to have been based on examination of the originally described Apex fossils, archived at the Natural History Museum in London (Schopf, 1993). Resolution of this controversy has thus hinged on whether the Apex fossils are cellular and composed of kerogenous organic matter (Schopf and Packer, 1987; Schopf 1992, 1993, Schopf et al., 2002, 2007), like similarly chert-permineralized ancient microorganisms, or are solid and mineralic, composed of abiotically derived graphite (Brasier et al., 2002, 2005), barium carbonate (García-Ruíz et al., 2002, 2003), silica or clay minerals (Pinti et al., 2009), or hematite (Marshall et al., 2011), and, if carbonaceous, whether the Apex organic matter has two different origins (Marshall et al., 2012). 1.2. Similar episodes in the history of Precambrian paleobiology Though many years ago uncertainty festered, for more than a century, over the “missing” fossil record of Precambrian life — beginning in 1859 with the deep puzzlement about the problem expressed by Darwin in On the Origin of Species — the intense interest in the Apex fossils, persisting now for the past decade, is unusual in the recent history of Precambrian paleobiology. In the modern development of the field, perhaps the most comparable example is that following the first detailed report of the now famous ~ 1900 Ma stromatolite-building fossil microbes of the Gunflint chert by Barghoorn and Tyler (1965) — even though this work was supported two months later by Cloud (1965). In that instance, the skepticism of the scientific community was soon put to rest, perhaps most effectively by a paper of the same year that reported a second example of Precambrian fossil microbes (Barghoorn and Schopf, 1965) demonstrating that the first report, of the Gunflint fossils, was not some sort of fluke. Even though, in 1965, the Gunflint microbes and the stromatolites in which they occur comprised the oldest compelling evidence of life then known, controversy about their biogenicity persisted for only a few years. In those times, however, nearly a half-century ago, the study of Precambrian microbes was dominated by the two widely acknowledged pioneering experts, Barghoorn and Cloud, workers whose findings supported the seminal discoveries of B.V. Timofeev, an “unsung hero” in the initial studies of microscopic Precambrian fossils (for a summary of this history, see Schopf 1999, pp. 35–50). Now, there are far more workers in the field — an increase spurred by the emergence of Precambrian paleobiology as a active field of science and of ever-increasing interest in the astrobiological search for past life on other planets, studies that are based on understanding of Earth's Precambrian fossil record. These developments, coupled with the introduction of an impressive array of new analytical techniques and the multidisciplinary approaches this has fostered, have encouraged divergent opinions. 2. Apex chert microbial assemblage 2.1. Biologic diversity The microbial assemblage of the Apex chert includes 11 taxa of filamentous microorganisms, ranging in width from ~0.5 to ~16.5 μm and differentiated by their medial- and terminal-cell size and shape, described on the basis of measurements of ~1800 cells in 175 specimens

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Fig. 1. Optical photomicrographs and interpretive drawings illustrating the diversity of filamentous microfossils present in petrographic thin sections of the Apex chert. a) Archaeotrichion septatum (0.5–1.5 μm broad, spheroidal cells). b, c) Primaevifilum delicatulum (1–3 μm broad, discoidal cells). d–f) P. minutum (1–3 μm broad, quadrate cells). g–i) P. amoenum (2–5 μm broad, quadrate to discoidal cells). j, k) Archaeoscillatoriopsis disciformis (3–6 μm broad, discoidal cells, rounded end cells). l–n) P. conicoterminatum (3–6 μm broad, discoidal cells, conical end cells). o, p) P. laticellulosum (6–9 μm broad, short-cylinder to quadrate cells).

(Schopf, 1993, table 1). Shown in Fig. 1 are optical photomicrographs and interpretive drawings of seven representative taxa. Although notable in such ancient rocks for their broad range of morphological diversity, they are similar in size, form, mode of preservation, and paleoenvironmental setting to chert-permineralized filamentous fossils reported from numerous other deposits of similar age (Awramik et al., 1983; Walsh and Lowe, 1985; Walsh, 1992; Rasmussen, 2000; Ueno et al., 2001a, 2001b, 2004; Tice et al., 2004; Kiyokawa et al., 2006; Sugitani et al., 2010; Wacey et al., 2011).

2.2. Biologic relations Although widely assumed to be cyanobacteria, the Apex fossils were formally described as “Bacteria Incertae Sedis” — that is, prokaryotes of uncertain affinities belonging to the Bacterial Domain (Schopf, 1993, 1999). In the paper in which they were taxonomically defined (Schopf, 1993), care was taken to negate a cyanobacterial interpretation since it would have implied that the Apex fossils were capable of oxygen-producing photosynthesis for which there was then, and is

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Apex chert (Schopf, 1993) has more recently been reinterpreted to be a brecciated and altered hydrothermal vein deposit (Van Kranendonk, 2006). Though such a setting has been suggested to be unlikely for preservation of delicate fossil microbes (Brasier et al., 2002, 2005; Pinti et al., 2009), microorganisms morphologically comparable to the Apex filaments are common in modern hydrothermal environments (Pentecost, 2003); filamentous microbes similar to Primaevifilum amoenum, the most abundant of the described Apex taxa (Schopf, 1993), have long been known to occur at deep-sea thermal vents (Jannasch and Wirsen, 1981); and chert-permineralized fossil filaments, including specimens so similar to those of the Apex chert that they have been assigned to two of the Apex taxa (Ueno et al., 2004), are present in three other Paleoarchean hydrothermal units of the northwestern Australian Pilbara Craton (Rasmussen, 2000; Ueno et al., 2001a, 2001b, 2004; Kiyokawa et al., 2006). As shown in Fig. 2a–c, the Apex fossils typically occur in subrounded millimeter-sized carbonaceous chert granules. Within such clasts the Apex fossils are commonly closely spaced, multiple specimens occurring within a given granular clast (Fig. 2d–j). Like some of the microfossils permineralized in other Paleoarchean thermal vent deposits, it is possible that the Apex filaments represent remnants of thermophilic microbes preserved in situ, in the Apex chert perhaps permineralized in hydrothermally “milled” and rounded organic-rich clasts. Given their mode of occurrence, however, and its similarity to the fossiliferous chert clasts of younger Precambrian units (Fig. 2k), it seems to us at least equally likely that the granule-embedded fossils are allocthonous to the deposit, older than or penecontemporaneous with the Apex chert, fossilized mesophiles emplaced in the unit in reworked detrital granules. 3. Establishment of biogenicity

Fig. 2. a, b, c) Optical photomicrographs of subrounded carbonaceous chert granules, containing cellularly permineralized filamentous fossils embedded in clouds of flocculent organic matter, in petrographic thin sections of the Apex chert. d) Primaevifilum minutum. e, f) P. delicatulum. g–i) P. amoenum. j) P. conicoterminatum. k) An optical photomicrograph of subrounded fossil-bearing carbonaceous granules in a petrographic thin section of chert from the ~780-Ma-old Auburn Formation of South Australia (Schopf et al., 2005), showing fossiliferous chert granules similar to those of the Apex chert (a–c) in a younger Precambrian deposit. Arrows denote locations of filamentous microfossils.

now, no compelling evidence (Schopf, 1999; Schopf et al., 2007). Although they might be cyanobacteria, as are the majority of similar fossils known from younger Precambrian fossiliferous units (e.g., see the references cited in Mendelson and Schopf, 1992), the available evidence is equally consistent with their assignment to non-oxygen-producing bacteria. Moreover, they could be members of an early-evolved microbial lineage that is now extinct or has yet to be recognized in the modern biota. The available evidence is inconclusive. 2.3. Mode of occurrence Geologically mapped initially as a shallow marine facies (Hickman and Lipple, 1978; Hickman, 1983), the fossiliferous locality of the

Establishing the biogenicity of ancient microscopic fossils — the problem of distinguishing bona fide fossil microbes from “fossillike” mineral grains and other microscopic pseudofossils — posed serious difficulties in the 1960s and 1970s when studies of Precambrian microorganisms were just beginning (e.g., Cloud, 1973). In the early stages of such studies, the field was plagued by the problem of distinguishing between modern contaminants (air- or water-born pollen, spores, microscopic fungi, micro-algae and the like) and authentic microfossils. This difficulty was resolved by centering investigations on organic-walled three-dimensionally permineralized objects studied in petrographic thin sections (such as the Apex fossils shown here), a strategy that demonstrates that such objects are embedded within and indigenous to the investigated rock. Since those early days, establishment of the biogenicity of microscopic Precambrian fossils has been addressed repeatedly and effectively: comprehensive tabulations have been compiled, separating authentic fossils from non-fossil “lookalikes” (e.g., Schopf and Walter, 1983; Mendelson and Schopf, 1992), and the characteristics expected of bona fide fossils have been tabulated and discussed in detail in a paper that presents side-by-side comparisons of authentic Precambrian microbes and reported pseudofossils with which they might be confused (Schopf et al., 2010a). A principal conclusion of such analyses is that of the cascade of mutually reinforcing evidence needed to establish biogenicity, two traits stand out: (1) relatively well-preserved authentic permineralized fossil microorganisms should exhibit cells and cell lumina, discernible walled compartments that typically are devoid of remnants of their originally water-rich cytoplasmic contents; and (2) the three-dimensional walls of such cells should be demonstrably of carbonaceous (kerogenous) composition.

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Fig. 3. Optical photomicrographs (a, c, e, g, i, j), and CLSM (b, f) and two-dimensional Raman images (d, h, k) of three specimens of Primaevifilum amoenum in petrographic thin sections of the Apex chert. The red rectangle in (a) denotes the area in (c) and (d); that in (e), the area in (g) and (h); and that in (i), the area in (j) and (k). The dark brown color of the fossils (a, c, e, g, i, j) suggests that they are composed of carbonaceous matter, an interpretation supported by their CLSM images (b, f), derived from laser-induced fluorescence of the interlinked polycyclic aromatic hydrocarbons that comprise their kerogenous cell walls, and that is established both by the 2-D Raman images (d, h, k), acquired at the ~1605−1 cm kerogen band, and their Raman spectrum (l).

These two prime traits should be expected to be exhibited by permineralized bona fide organic-walled microscopic fossils, backed by additional biogenicity indicators such as the occurrence of specimens

ranging from relatively well preserved to partially or completely degraded (for a compilation of such traits, see Schopf et al., 2010a, Table 1).

Fig. 4. Optical photomicrographs (a, b), three-dimensional (c) and two-dimensional (d–h) Raman images, and CLSM images (i, j) of a specimen of Primaevifilum amoenum in a petrographic thin section of the Apex chert. The red rectangle in (a) denotes the area in (c) through (h); the Raman images were acquired at the ~1605−1 cm kerogen band. The arrows in (b) point to quartz grains of the fossil-embedding chert matrix, virtually all of which are larger or smaller and more irregularly shaped than the quadrate cells (a) of the cylindrical fossil filament (c), indicating that it is not composed of organic-coated quartz grains. In (d) through (h), the box-like cells of the fossil filament are shown in 2-D Raman images (acquired at the ~1605−1 cm kerogen band) at the indicated sequentially increasing depths below the upper surface of the fossil, images that establish the kerogenous composition of its cell walls (white) and the presence of cell lumina, denoted by arrows in (d) and shown also in (e) through (h). The green three-dimensional “chicken wire fabric” shown in (i) and (j) in CLSM images of the fossil-containing area, acquired at the indicated depths below the upper surface of the thin section (in which the arrows are provided for orientation), is a product of the laser-induced fluorescence of microscopy immersion oil that penetrated at quartz grain boundaries into the section, an intricate 3-D fabric differs markedly from that of the discrete cylindrical fossil, showing that the filament is not a pseudofossil formed by seepage of organic fluids (e.g., petroleum) into the chert.

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4. Are the Apex Fossils Bona Fide Fossils? 4.1. Carbonaceous composition Shown here are optical photomicrographs (Fig. 3a, e, c, g, i, j), images obtained by confocal laser scanning microscopy, “CLSM” (Fig. 3b, f), and two-dimensional (Fig. 3d, h, k) and three-dimensional (Fig. 4c) Raman images of the Apex fossil Primaevifilum amoenum. CLSM and 2-D and 3-D Raman imagery are techniques relatively new to Precambrian paleobiology (Kudryavtsev et al., 2001; Schopf et al., 2002, 2005, 2006). The application, effectiveness, and limitations of these techniques for studies of rock-embedded fossils, and the instrumental configurations used to acquire the data presented here, have recently been discussed in detail (Schopf et al., 2010b). The CLSM images of P. amoenum (Fig. 3b, f), derived from the laser-induced fluorescence of the interlinked polycyclic aromatic hydrocarbons (PAHs) that comprise the cell walls of this and similarly permineralized organic-walled Precambrian microfossils (Schopf et al., 2005, 2006; Schopf and Kudryavtsev, 2010), are consistent with the kerogenous composition of the fossil, as established by its 2-D (Fig. 3d, h, k) and 3-D (Fig. 4c) Raman images and Raman spectrum (Fig. 3l). 4.2. Three-dimensional cellularity Raman spectroscopy documents the three-dimensional cellularity of the kerogenous cell walls of a representative specimen of the Apex fossil Primaevifilum amoenum illustrated in Fig. 4c–h. Optical microscopy (Fig. 4a, b) shows that the kerogen-defined cells of this specimen are not a result of non-biological organic coating of the irregularly shaped quartz grains in which the Apex fossils are embedded. And CLSM images show that the fossil is not be a result of the penetration of organic fluids (e.g., petroleum) into the chert, a process that results in a three-dimensional “chicken-wire” fabric unlike that of such cellularly permineralized microorganisms (Fig. 4i, j). 4.3. Organic geochemical maturity Does the composition of the organic matter that comprises the Apex fossils fit with that of microfossils similarly preserved in other Precambrian deposits? In Fig. 5 are compared the Raman spectra of organic-walled fossils chert-permineralized in seven Precambrian units, including the Apex chert (Fig. 5, broad arrow), ordered by their geochemical maturation from less mature (top) to more mature (bottom). As these data show, the primary Raman bands of the kerogenous cell walls of such fossils change in relative intensity and width as geochemical alteration results in an increase in the domain-size and orderly stacking of their PAH-dominated graphene layers (Schopf et al., 2005). The spectra illustrated show that the Apex fossils are more geochemically mature than those of the ~ 800 Ma Bitter Springs and ~ 1900 Ma Gunflint Formations — but are appreciably better preserved, less geochemically altered, than the partially graphitized fossils of the ~720 Ma Auburn Dolomite and ~775 River Wakefield Formation. Chert-permineralized carbonaceous fossils from more than a score of Precambrian geological units have been characterized by this same technique (Schopf et al., 2005), results showing that the kerogenous composition of the Apex fossils fits with that of all similarly analyzed permineralized ancient microscopic organisms. Importantly, such Fig. 5. Raman spectra of kerogen comprising fossils of the Apex chert (broad arrow) and similarly permineralized microfossils in six other Precambrian cherts — ordered, from top to bottom, by the changes in the Raman “D” and “G” bands of kerogen (denoted by narrow arrows at the top of the figure) that accompany geochemical maturation (Schopf et al., 2005) — compared with the Raman spectrum of graphite (bottom). This comparison demonstrates that the kerogen comprising the Apex fossils is similar to that of other chert-permineralized Precambrian microorganisms and is not graphite.

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Fig. 6. Carbon isotopic composition of biogenic kerogen and co-existing inorganic carbonate carbon, the Precambrian data in (a) measured in 100 geological units (Strauss and Moore, 1992; Schopf, 2004) and those in (b) based on ~200 measurements of nine Paleoarchean microfossil-bearing cherts (Schopf, 2006). These data show that carbon isotopic evidence of CO2-based autotrophy extends from the present to ~3500 Ma ago (a) and that the carbon isotopic composition of the organic matter of the Apex chert (b, arrow) is like that of eight other similarly ancient fossil-bearing chert units.

data establish that the Apex fossils are not composed of graphite, as proposed by Brasier et al. (2002, 2005), as is evident from comparison of the Raman spectrum of an Apex fossil (Fig. 5, broad arrow) with that of graphite (Fig. 5, bottom spectrum). 4.4. Carbon isotopic composition Throughout the geological record from 3500 Ma to the present, preserved carbonaceous matter typically exhibits a δ 13CPDB value of − 25 ± 10‰ (Fig. 6a), a signature of biological (autotrophic) carbon-fixation (cf. House et al., 2003). The carbon isotopic composition of the Apex organics, having an average δ 13CPDB value of − 27.7‰ (n = 10; Schopf, 2006) — similar to the δ 13CPDB value of − 28.8‰ (n = 192; Schopf, 2004) of kerogens preserved in eight other 3200– 3500 Ma deposits from which microfossils have been reported (Fig. 6b) — is consistent with a biological origin. The carbon isotopic composition of the Apex organic matter thus supports interpretation of the fossil assemblage as including CO2-fixing autotrophs, but it is insufficient to establish that such microbes were photoautotrophs, whether oxygenic or anoxygenic (Schopf, 1993; House et al., 2003). 4.5. Organic geochemical composition As established by Raman spectroscopy (Fig. 5; Schopf et al., 2002, 2007), the Apex fossils are composed of carbonaceous matter. This finding, showing the non-graphitic nature of such material and

associated organic detritus has been confirmed by numerous other techniques (De Gregorio and Sharp, 2003, 2006; De Gregorio et al., 2005, 2009), with these and related studies having rendered implausible an abiotic origin for the organic matter preserved in this and other ancient deposits (cf. Ueno et al., 2004) and indicating that the Apex organics are “consistent with the interpretation that the microbial-like features in the Apex chert are bona fide microfossils” (De Gregorio et al., 2005, p. 1866). More recently, De Gregorio et al. (2009) used data acquired by transmission electron microscopy (TEM), electron loss near-edge structure spectroscopy (ELNES), synchrotron-based scanning-transmission X-ray microscopy (STXM), STXM-based X-ray absorption near-edge spectroscopy (XANES), and secondary ion mass spectroscopy (SIMS) to characterize the structure, carbon bonding, functional group chemistry, and light element composition of the carbonaceous components of the Apex chert. Highlights of their results can be summarized as follows: (1) The ELNES-detectable peak (at 292 eV) characteristic of graphite and highly disordered graphitic carbon is not present in Apex carbonaceous matter. This finding confirms that the Apex carbonaceous matter is kerogen, as originally inferred (Schopf, 1992, 1993), not graphite as postulated by Brasier et al. (2002, 2005). (2) “In addition, Apex carbonaceous matter [is composed of] chemically complex organic materials rather than simple hydrocarbon materials … [and] contains … nitrogen, sulfur, and

Fig. 7. Scanning electron micrographs (a, e) and optical photomicrographs (b–d, f) comparing (a) laboratory synthesized barium carbonate crystallite “biomorphs” (García-Ruíz et al., 2003, Fig. 2A, reprinted by permission); (b–d) filamentous microfossils of the Apex chert, imaged in petrographic thin sections; (e) clay and silica mineral pseudofossils reported from the Apex chert (Pinti et al., 2009, Figs. 1h, 2h and i, reprinted by permission); and (f) an Apex chert hematite-infilled pseudofossil veinlet (Marshall et al., 2011, Fig. S2, reprinted by permission). Such barium carbonate (witherite) “biomorphs” (a) lack cell-defining kerogenous cell walls (Fig. 4d–h) and have not been reported from the geological record. The clay and silica pseudofossils (e) — objects that are mineralic, not carbonaceous like the Apex fossils, and are straight and needle-like, not sinuous and cellular as are the Apex fossils — are much too small to be confused with the Apex fossils (b–d). Unlike the Apex fossils, hematite veinlets (f) are rock-transecting planar structures, not rock-embedded cylindrical filaments; are mineralic, rather than carbonaceous; and are solid, rather than cellular. These pseudofossils (a, e, f) differ distinctly from the bona fide fossils of the Apex chert (b–d).

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phosphorous … in which the presence of phosphorus, in particular, implies a biogenic origin” (De Gregorio et al., 2009, p. 632). This result, combined with Raman and ELNES data documenting the presence of carbon, oxygen and hydrogen, shows that the Apex organic matter is composed of all of the biologically definitive elements, C, H, O, N, S and P — a firm indicator of biogenicity. (3) “C-XANES spectra acquired from … Apex carbonaceous matter [show spectral features], including the presence of carboxyl

[―COOH] and phenol [Caromatic―OH] peaks” (De Gregorio et al., 2009, p. 632), chemical functional groups characteristic of biogenic kerogen that do not occur in graphite. From this detailed study, De Gregorio et al. (2009, p. 631) conclude that “the Apex microbe-like features represent authentic biogenic organic matter,” an interpretation consistent with the reported presence of geochemical biomarkers in the geological unit immediately underlying the Apex chert that “support a scenario according to which life was present on Earth 3.5 By ago” (Derenne et al., 2008, p. 480). 5. Suggested nonbiologic origins 5.1. Abiotic graphitic pseudofossils The data presented here show that the Apex fossils are cellular (Figs. 1–4), not solid, and are composed of biogenic kerogen, not graphite derived from abiotic organic syntheses. They are not opaque minerals, not contaminants, and not products of permeating organic fluids (Figs. 3, 4). Further, as discussed below, the Raman-documented molecular structure and geochemical maturity of their carbonaceous components (Figs. 3l, 5) and that of associated flocculent kerogen (Fig. 2a–c) are essentially identical, showing that all analyzed organics of the Apex chert have experienced the same geological history. Although, in comparison with much younger Precambrian fossils, their cells (Figs. 1–4) and kerogenous constituents (Fig. 5) are not particularly well preserved (e.g., see the references cited in Mendelson and Schopf, 1992), their biogenicity is consistent with all relevant evidence: their cellular and organismal morphology is like that of modern microbes and other permineralized fossil microscopic organisms; their mode of occurrence and cellular degradation is similar to that of other organic-walled Precambrian microfossils; the biology-consistent carbon isotopic composition of Apex organics fits with thousands of analyses, including those of organic matter in deposits of comparable age; the chemistry of the Apex organics shows it to be biogenic, not abiotic; and the Apex fossils, like those known from geological units of a similar age, are consistent with the history of early life. Moreover, and perhaps most notably, nonbiologically produced particulate organic matter — such as that that postulated to compose the Apex fossils (Brasier et al., 2002, 2005) — has not been reported to occur in the geological record. 5.2. Barium carbonate “biomorphs” Millimeter- to micron-sized filamentous, spiral, and radiating “biomorphic” crystallites of co-precipitated barium carbonate (BaCO3, witherite) and silica (SiO2), the most minute of which resemble certain of the Apex fossils (e.g., Fig. 7a), have been synthesized in laboratory experiments by García-Ruíz et al. (2002, 2003). Rather than being composed of organic-walled box-like cells, however, such structures are solid nanocrystals, their surficial cell-like segmentation (Fig. 7a) reflecting the presence of grain boundaries that separate adjacent Fig. 8. a) Raman spectra of kerogen analyzed in a petrographic thin section of the Apex chert as reported by Marshall et al. (2012). b) The spectra in (a) normalized to the height of their kerogen “G” bands. c) Spectra of permineralized kerogenous fossils and particulate kerogen analyzed in thin sections of cherts of the Apex, Skillogalee, and River Wakefield geological units (the analyses of each derived from specimens in a single thin section) and of highly oriented pyrolytic graphite, “HOPG.” The spectra in (a) appear to differ primarily because they were not normalized to the “G” band of kerogen (b). Differences in the intensity of the “D” band in “G” band-normalized spectra (c) are typical of geochemically relatively mature kerogens, such as those of the Apex, Skillogalee, and River Wakefield deposits (c), composed of relatively large-domain PAHs that dominate their stacked graphene layers. As documented by Katagiri et al. (1988) for HOPG (c, bottom spectrum), such spectral differences are a function of the relative contributions of the Raman signatures of the basal planes and edge planes of the material analyzed.

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crystallites, not the transverse carbonaceous walls that define microbial filaments. Although such crystallites can be enveloped by a silica skin (García-Ruíz et al., 2009; Kunz and Kellermeir, 2009) capable of absorbing introduced organics on their exterior surfaces (García-Ruíz et al., 2003), their lack of cellular organization — were they to be found in nature — would allow them to be distinguished from bona fide fossils (Schopf et al., 2010a). However, like the graphite pseudofossils proposed by Brasier et al. (2002, 2005) to be composed of abiotically generated organic matter, such witherite-silica “biomorphs” are unknown in the geological record. 5.3. Clay mineral pseudofossils Needles composed of hallosite (Al2Si2O5[OH]4), a clay mineral, and of quartz (SiO2), have been compared with the Apex fossils (Pinti et al., 2009). These mineralic needles, however, are more than 40 times narrower than the carbonaceous Apex fossils (Fig. 7e) and, like the “biomorphs” discussed above, the needles are neither cellular nor kerogenous. The authors of this work acknowledge that their “… observations are not applicable to the microfossils of the Apex chert … because [they] did not observe carbonaceous filaments” (Pinti et al., 2009, pp. 640, 642). 5.4. Hematite veinlet pseudofossils Hematite- (Fe2O3–) infilled secondary veinlets in the Apex chert have also been compared with the Apex fossils (Marshall et al., 2011), primarily because the authors of this work assumed that reports of the carbonaceous composition of the fossils were based on the ~ 1350 cm −1 Raman band of kerogen — which they imagined might have been mistaken for the ~ 1330 cm −1 Raman band of hematite — rather than the source of the data, the ~ 1605 cm −1 Raman band of kerogen (as specified in Figs. 3d, h, k; 4c–h). This error of misinterpreting mineral veinlets to be authentic fossils has a well-documented history (Schopf et al., 2010a). As has been previously discussed (Schopf and Kudryavtsev, 2011), the hematite-infilled veinlets described by Marshall et al. (2011) differ markedly from the Apex fossils: the veinlets are mineralic (Fig. 7f), not carbonaceous (Fig. 3b, d, f, h, k); are rock-transecting planar structures, not rock-embedded cylindrical filaments (Fig. 4c–h); are more or less straight (Fig. 7f), not sinuous (Fig. 7b–d); and are relatively large, having an average diameter of 17 μm and a size-range of 4 to 65 μm (n = 50; Marshall et al., 2011, p. 240), about three times broader than the Apex fossils (avg. diameter = 6 μm, range = 0.5–19 μm, n = 1788; Schopf, 1993). 5.5. Multiple generations of kerogen Based on differences in the Raman spectra of samples of Apex kerogen, primarily a difference in the intensity of their Raman “D” bands (Fig. 8a, b), Marshall et al. (2012) suggested that the Apex chert contains two generations of carbonaceous matter. However, as is shown here by Raman spectra of particulate and microfossil-comprising kerogens analyzed in single thin sections of Apex, Skillogalee, and River Wakefield fossiliferous cherts (Fig. 8c; Schopf et al., 2005), such differences are typical of the spectra of geochemically relatively mature chert-permineralized carbonaceous matter (Fig. 5). Such differences are not due to a polarization effect; rather, as is discussed below, they evidence the orientation of Raman-analyzed kerogens composed of stacked, large PAH-domain-dominated graphene layers. As first shown for highly oriented pyrolytic graphite (HOPG) by Katagiri et al. (1988) and, later, in other studies of similar materials (e.g., Compagnini et al., 1997; Kawashima and Katagari, 1999; Tan et al., 2004), the intensity of the “D” band (relative to the “G” band) of such carbonaceous matter is a function of the relative contributions

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of the Raman signatures of the basal planes and edge planes of the material studied. Such signatures are sensitive to the orientation of the analyzed specimen, spectral features of the edge planes being due to molecular discontinuities at the periphery of the largedomain components of their graphene layers (Katagiri et al., 1988). In chert samples containing geochemically relatively mature permineralized kerogen, randomly oriented particles that comprise flocculent carbonaceous clouds (Fig. 2a–c) can be oriented such that molecular discontinuities at the periphery of their stacked largedomain PAHs produce a Raman signature exhibiting edge plane features such as the enhanced kerogen “D” band reported by Marshall et al. (2012). In contrast, in geochemically less altered kerogens the domain size of the PAHs that comprise the graphene layers is very much smaller and, because Raman averages molecular compositions over the ~1-μm-diameter area of the focused laser beam, such edge plane features are not detectable. It is notable, however, that unlike the randomly oriented particles of carbonaceous clouds, the kerogenous cell walls of permineralized fossils are composed of regularly stacked platelets of graphene layers (Kempe et al., 2002, 2005). Thus, in Raman spectra of permineralized organic-walled fossils, such as those of the Apex chert, the relative intensity of the “D” and “G” bands is uniform throughout an individual specimen and is invariant for all fossils of any particular biological community — as has been shown for diverse chertpermineralized carbonaceous fossils (Schopf et al., 2002, 2005, 2007, 2008, 2010a, 2010c) — a Raman signature consistent with their biogenicity. The minor spectral differences reported by Marshall et al. (2012) are detectable only in geochemically relatively mature kerogens, such as those preserved in the Apex, Skillogalee, and River Wakefield cherts (Fig. 8c), but not in less altered kerogens such as those of the Bitter Springs and Gunflint Formations (Fig. 5). Raman analyses show that the geochemical maturity of the Apex carbonaceous fossils (Figs. 3l, 5) is the same as that of the associated flocculent kerogen (Fig. 2a–c), a characteristic of the co-existing permineralized fossils and particulate kerogens similarly analyzed in more than 20 other Precambrian microbial communities (Schopf and Kudryavtsev, 2005, 2010; Schopf et al., 2005, 2008, 2010c). Raman spectra of the Apex kerogens do not evidence two generations of carbonaceous matter. 6. Discussion Studies of rock-embedded carbonaceous microscopic fossils have advanced markedly over the two decades since the Apex microbes were first reported (Schopf and Packer, 1987) and formally described (Schopf, 1992, 1993). Foremost among such advances are two analytical techniques, both having sub-micron spatial resolution: (1) Raman spectroscopy, a technique that can provide twodimensional (Figs. 3d, h, k; 4d–h; Schopf et al., 2002, 2005) and three-dimensional kerogen-derived images (Fig. 4c; Schopf and Kudryavtsev, 2005, 2010; Schopf et al., 2010b) of permineralized organic-walled microscopic fossils and of their embedding minerals, to a depth of ~150 μm — a thickness equivalent to that of five standard 30-μm-thick petrographic thin sections — introduced to such studies only a decade ago (Kudryavtsev et al., 2001). (2) Confocal laser scanning microscopy, an analytical technique that for carbonaceous fossils is based on detection of laser-induced fluorescence emitted from the interlinked polycyclic aromatic hydrocarbons that comprise their kerogenous cell walls (Fig. 3b, f) — a technique, like Raman, applicable to thin section-embedded fossils to depths of ~150 μm — introduced to Precambrian paleobiology some six years ago (Schopf et al., 2006) that has recently been shown effective for studies of permineralized fossil animals, plants, fungi, protists and prokaryotes (Schopf et al., 2010b).

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These two new techniques have improved studies of the Precambrian fossil record (Schopf and Kudryavtsev, 2010) and, as is shown in Fig. 3 for fossils of the Apex chert, are especially useful for establishment of biogenicity: applied in situ to the same specimen, and backed by optical microscopy, they can be used together to document a one-to-one correlation of cellular morphology and organic composition, a hallmark of biologic systems. Yet another novel technique, secondary ion mass spectroscopy (SIMS), holds promise for such studies. Since its introduction to investigations of Precambrian microfossils (House et al., 2000), SIMS has been used to document the lightelement isotopic composition of thin section surface-exposed microscopic fossils in several Precambrian deposits to provide additional evidence of biogenicity (e.g., McKeegan et al., 2007; Oehler et al., 2006, 2009; Wacey et al., 2011). Major advances have also been made in techniques used to analyze the chemical composition of ancient organic matter, as shown effectively by De Gregorio et al. (2009) who used ELNES, TEM, STXM, XANES and SIMS to document the biogenicity of the kerogen of the Apex chert, on the basis of which, as noted above, they conclude that the Apex fossils are composed of biogenic organic matter. Twenty years ago, when the Apex fossils were first described, neither Raman, nor CLSM, nor any of the modern geochemical techniques (e.g., ELNES, TEM, STXM, XANES and SIMS) had been applied to analyses of these or any other Precambrian fossils. Then, the three-dimensional organismal morphology of the Apex filaments, discernible by optical microscopy, could be illustrated only by photomicrographs acquired at varying optical depths that were literally pasted together to demonstrate the typically sinuous organismal form of fossils detected (Schopf 1992, 1993). No analytical technique — provided now by Raman spectroscopy — was available to establish the kerogenous composition of these or any other rock-embedded ancient fossils, an inference that could be drawn (as it had been for the preceding 40 years) based only on the dark brown “organic-like” color of their cell walls (e.g., Barghoorn and Schopf, 1965; Barghoorn and Tyler, 1965; Cloud, 1965). The application of these new techniques has shown that the biogenic interpretation of the Apex fossils proposed 20 years ago — and, by extension, that of a great many other Precambrian microbes described over the past five decades — remains valid. This is reassuring, for if the early workers had been wrong, if their assumption of organic composition and biogenicity based on the color and optically discernible morphology of such fossils had been mistaken, understanding of the early history of life would be grievously in error. Indeed, if the detailed laboratory work carried out on the Apex fossils and their associated organic matter had proven incapable of establishing biogenicity in rocks from Earth's geological record — where interpretations are backed by decades of studies of Precambrian microscopic fossils, microbially produced stromatolites, and a large body of data documenting the elemental, molecular and carbon isotopic composition of preserved organic matter — how would this science fare in attempts to document evidence of ancient life on other planets such as Mars? 7. Conclusion As summarized here, the ~ 3465 Ma fossils and associated organic components of the Apex chert are well studied. A host of analytical techniques — most notably, 2-D and 3-D Raman imagery (Figs. 3d, h, k, 4c–h, 5), CLSM imagery (Figs. 3b, f, 4i, j), and methods used to characterize the chemistry of geochemically altered organic matter (De Gregorio et al., 2009) — have been applied to the Apex chert, establishing the biogenicity of the exceedingly ancient microbial assemblage and organic matter that it contains. The decade-long controversy over the biogenicity of the Apex fossils has been resolved: “microbial life was present and flourishing on the early Earth ~ 3500 Ma ago” (Schopf et al., 2010d).

Abbreviations CLSM confocal laser scanning microscopy ELNES electron loss near-edge structure spectroscopy PAH polycyclic aromatic hydrocarbon SIMS secondary ion mass spectroscopy STXM synchrotron-based scanning-transmission X-ray microscopy TEM transmission electron microscopy XANES STXM-based X-ray absorption near-edge spectroscopy

Acknowledgements This article was invited by the Elsevier Review Papers Coordinator, Tim Horscroft. For helpful comments, we thank Malcolm R. Walter, J. Shen-Miller, Ian Foster, Sean Loyd and an anonymous reviewer of this manuscript.

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J. William Schopf is Distinguished Professor of Paleobiology at the University of California, Los Angeles. He received his undergraduate training in Geology at Oberlin College, Ohio, and his advanced degrees, in Biology, from Harvard. A member of the U.C.L.A. faculty since 1968, he was the first to discover permineralized Precambrian fossil microbes in Australia, China, India, Russia, South Africa, and the U.S.A. Active both in Precambrian Paleobiology and the emergent field of Astrobiology, his recent work has centered on the use of Raman spectroscopy and confocal laser scanning microscopy to document the morphology and composition of ancient fossils. A member of the U.S. National Academy of Sciences and recipient of book prizes and medals, he has authored some 370 scientific publications.

Anatoliy B. Kudryatsev is Senior Scientist at U.C.L.A.'s Center for the Study of Evolution and the Origin of Life (CSEOL). He received his undergraduate training in Physics at the Moscow Institute of Physics and Technology, and his Ph.D. at the General Physics Institute of the Russian Academy of Sciences. After serving for nine years as a Research Professor in the Department of Physics at the University of Alabama, Birmingham, in 2004 he moved to U.C.L.A. where he has used his expertise in optical spectroscopy to investigate ancient microscopic fossils. The author of numerous publications, in 2006 he received a Raman Imaging Prize from HORIBA Jobin Yvon for his three-dimensional reconstruction of quartzenclosed apatite-embedded graphite granules from the ~3,800 Ma Isua Supracruastal Group of Greenland.