Cavities are considered plausible and favorable habitats for life on early Earth. In such microenvironments, organisms may have found an adequate protection against the intense ultraviolet radiation that characterized the Archean ozone-free atmosphere. However, while there is clear evidence that benthic life existed in the Paleoarchean, the oldest traces of cavity-dwelling microbes (coelobionts) have been found in Neoarchean rocks. Here we present the results of a detailed investigation of early silicified cavities occurring in the oldest well-preserved siliciclastic tidal deposits, the 3.22 Ga Moodies Group of the Barberton Greenstone Belt (South Africa). Downward-growing microstromatolitic columns composed of kerogenous laminae are commonly present in planar, bedding-parallel, now silica-filled cavities that formed in sediments of the peritidal zone. In-situ δ13CPDB (PDB—Peedee belemnite) measurements of the kerogen range from –32.3‰ to –21.3‰ and are consistent with a biogenic origin. Scanning electron microscopy analysis of the silicified cavities shows well-preserved chains of cell-sized molds that are interpreted as fossil filamentous microorganisms. The geological context, the morphology of the microstromatolites, the δ13C composition of the kerogen, and the presence of microfossils all suggest that a microbial community inhabited the cavities. These results extend the geological record of coelobionts by ∼500 m.y., supporting the view that cavities were among the first ecological niches to have been occupied by early microorganisms.
Stromatolites interpreted as fossil microbial mats, permineralized microfossils in chert, and kerogen with characteristic carbon isotopic signatures all suggest that microbial life was widespread in the photic zone of Paleoarchean coastal environments (Nisbet and Sleep, 2001; Altermann and Kazmierczak, 2003; Brasier et al., 2006; Schopf, 2011; Bontognali et al., 2012). However, due to the absence of an ozone shield, the high surface ultraviolet (UV) flux in that period was presumably harsh, even lethal for unprotected microorganisms within minutes to days (Cockell and Raven, 2007). Under such unfavorable conditions, early microbial communities thriving in the photic zone supposedly employed one or several protective mechanisms, e.g., high DNA repair capability, biosynthesis of pigments, radiation screening by mineral incrustation or by matting, and the accumulation of surficial dead biomass (Garcia-Pichel and Bebout, 1996; Cockell, 1998; Phoenix et al., 2001). Furthermore, organisms can actively migrate to and colonize UV-protected subsurface habitats within the sediment (endobenthic; Noffke, 2010), within solid rocks (endolithic; Walker et al., 2005), or in cavities (coelobiontic; Kobluk and James, 1979; Nisbet, 1985; Phoenix et al., 2006). Unambiguous evidence for those strategies, however, is difficult to find in the fossil record; currently, the oldest remnants of cavity-dwelling microbial communities have been identified in 2.75 Ga fluviolacustrine sediments of the Fortescue Group (Australia; Rasmussen et al., 2009). Our study reports on remarkably well preserved remains of a 3.22 Ga microbial community that colonized subsurface cavities beneath microbial mats in tidal sands of the Barberton Greenstone Belt, South Africa.
GEOLOGICAL AND PALEOENVIRONMENTAL SETTING
The Moodies Group (ca. 3.22 Ga), the uppermost unit of the Barberton Greenstone Belt (ca. 3.57–3.22 Ga), comprises mainly fine- to coarse-grained, quartz-rich sandstones and subordinate conglomerates, siltstones, and thin volcanic tuffs deposited in tidal and deltaic settings (Anhaeusser, 1976; Eriksson, 1979; Heubeck and Lowe, 1994, 1999; Heubeck et al., 2013). Moodies strata are particularly well preserved on the ∼3-km-thick overturned limb of the Saddleback syncline in the central Barberton Greenstone Belt north of the Inyoka fault (Fig. DR1 in the GSA Data Repository1), where they have undergone only lower greenschist facies metamorphism (Toulkeridis et al., 1998). The lower part of this subvertically dipping succession (unit MdQ1 of Anhaeusser, 1976), ∼1 km thick, contains the world’s oldest known record of macroscopic microbial mats in a siliciclastic tidal setting, laterally traceable for ∼15 km (Noffke et al., 2006; Heubeck, 2009; Homann et al., 2015). The mats, preserved as kerogen-rich laminae, developed distinct morphological adaptations to coastal floodplain, supratidal, and intertidal conditions and were likely formed by phototrophic microbial communities; this conclusion is based on their consistent shallow-water occurrence and partly tufted morphology (Homann et al., 2015). They are commonly underlain by chert lenses, which are interpreted as former cavities beneath unconsolidated but microbially bound cohesive sediment (Figs. 1A and 1B). In the studied unit of the Moodies Group these bedding-parallel chert-filled cavities are restricted to tidal facies fine- to coarse-grained sandstones, and contain kerogenous microstructures (described in the following).
SAMPLES AND METHODS
Outcrop samples (n = 32) were slabbed and polished to identify the best-developed chert lenses for the preparation of 150-µm-thick polished thin sections (n = 12). Scanning electron microscopy (SEM) analysis of the samples was conducted at the Freie Universität Berlin (Germany) using a Zeiss SUPRA 40 VP SEM operating with 20 kV acceleration voltage. In-situ carbon isotope analyses of silicified kerogen were performed with a CAMECA IMS 1280 at the SwissSIMS (secondary ion mass spectrometry) facility located at the University of Lausanne, Switzerland (see additional notes and Table DR1 in the Data Repository).
Cavities and Associated Kerogenous Microstructures
The lens-shaped, laterally tapering cavities are up to tens of centimeters in width and <0.5 cm in height. They typically occur below a <3-mm-thick sandstone layer, which is overlain by a fossil microbial mat (Fig. 1B). Cavity ceilings are commonly coated by dark kerogenous laminae (Fig. DR3) with downward-facing protrusions and pendant columns that are up to 1.5 mm and 0.6 mm wide (Fig. 2A). Well-preserved single or coalescing columns contain multiple, closely spaced, 1–5-µm-thick, subparallel stromatolitic laminae of kerogenous composition that are oriented convex-down and taper toward the margins of the columns (Figs. 2B and 2C). Some columns terminate in a prominent lamina, up to 30 µm thick (Fig. 2C). Remnants of zoned ferroan dolomite rhombs, 10–100 µm in diameter, occur scattered throughout the cavity-filling chert and are particularly abundant in the tips of some columns (Figs. 2D–2F). The dark kerogenous laminae are commonly encrusted by light colored silicified cements that are 100–400 µm thick and widely discontinuous. In some places, these cement crusts are botryoidal and contain bladed to acicular ghost crystals resembling aragonite (Figs. 2G and 2H). In other places, laminae are disrupted and bent upward (Fig. 2H) or occur as detached, slightly deformed fragments near the cavity floor (Fig. 2I).
SEM images of the cavity-filling chert show a meshwork of interwoven filamentous molds that is completely embedded in the chert (Fig. 3A). These thread-like, nonbifurcating filamentous microstructures are 0.3–0.5 µm in diameter (n = 180; Fig. DR4) and up to several tens of microns. They are commonly bent with abundant changes in orientation; in places, they show a subdivision in regularly spaced, ∼2-µm-long, rod-shaped segments (Figs. 3B–3D). Individual segments are ∼5× longer than wide and have rounded ends. Transverse cross sections through filamentous structures show that they are cylindrical, hollow, and encased by an ∼100-nm-thick silica layer (Figs. 3D–3F).
Carbon Isotope Data
In-situ measured δ13CPDB (Peedee belemnite) values from the kerogenous laminae within the cavities vary between −32.3‰ and −21.3‰, with a mean value of −26.5‰ (n = 12; Figs. 4A and 4B), and are consistent with a biotic origin of the kerogen (Schidlowski, 2001). Bulk δ13CPDB measurements of extracted kerogenous material from the mats above the cavities show a similar range of values (i.e., between −33.2‰ and −21.9‰) with a slightly more negative mean value of −29.5‰ (n = 6). Poorly preserved dolomite crystals within the chert yield mean values of −0.3‰ δ13CPDB and −14.9‰ δ18OPDB (n = 6), common values for dolomitic carbonates of Archean age (Shields and Veizer, 2002; Grossman, 2012).
The shape and size of the observed cavities resemble gas-filled, fenestral hollows in modern tidal environments that occur widely near the sediment-water interface a few millimeters to centimeters beneath cohesive, impermeable microbial mats and mat-bound sediments (Gerdes et al., 2000; Schieber et al., 2007; Noffke, 2010). Such cavities form either through accumulation of gases produced by metabolic activity (e.g., O2, CO2, CH4) or simply by tidal-driven hydraulic pumping of the ambient air trapped in pore space.
Cavities and kerogenous laminae are syngenetic. Both formed within a short time after sand deposition because they (1) are parallel to subvertical bedding, thus predating regional folding ca. 3.22 Ga; (2) are never related to fractures, veins, or any other demonstrably late structures; and (3) show a clear facies dependency. In addition, kerogenous laminae show Raman spectra that are consistent with the regional peak metamorphic temperatures of the host rocks (Fig. DR3C). The in-situ formation of the lamina with common columnar microstromatolitic structures at the cavity ceiling is further supported by their downward-accretionary growth habit. This gravity-oriented geometry is well known from cavity-dwelling microorganisms attached to the roof of cryptic voids, e.g., in Paleozoic reefal limestones (Kobluk and James, 1979; Jakubowicz et al., 2014), and has also been observed in modern sea caves that are encrusted by pendant microbialites (Léveillé et al., 2000). It is evident that the microstromatolitic structures found in the cavities of the Moodies Group formed in situ and were built by a coelobiontic community distinct from those of the overlying epibenthic microbial mats.
The carbonate cement fans alternating with the kerogenous laminae built by coelobionts likely formed through abiogenetic encrustation (Riding, 2008) during periods of partial or complete desiccation, a common feature in tidal environments. Subsequently, early silicification replaced large parts of the carbonates and prevented the destruction of the cavities while promoting the preservation of the biological components (Bartley, 1996).
The biogenic origin of the observed filaments is supported by the following attributes: (1) tubular morphology with constant diameter; (2) regular segmentation; (3) hollow interior; (4) colonial occurrence; and (5) curved appearance indicating a former flexibility (Schopf, 2004). The morphology of the filaments with respect to their size, shape, and cell-like segmentation is comparable to that of modern filamentous microorganisms (Boone and Castenholz, 2001), such as some chemotrophic (e.g., methanogens) and phototrophic bacteria (e.g., non-sulfur and some cyanobacteria), which are known to be well preserved in modern siliceous stromatolites and other settings (Jones et al., 2005).
Similar filamentous structures have been identified as former microorganisms in chert-filled cavities from 1.2 Ga paleokarst deposits (Horodyski and Knauth, 1994) and in various shallow-marine cherts of Archean age (Schopf, 2006; Westall et al., 2006; Sugitani et al., 2013).
The radiation-screening effect of epibenthic microbial mats creates UV-protected subsurface habitats a few millimeters beneath the mat (Garcia-Pichel and Bebout, 1996; Jackson, 2015). Such microhabitats would have provided protection from UV radiation even in the worst-case scenario calculations of the Archean surficial UV flux (Cockell, 1998). A modern analog environment with increased solar radiation is found in Chilean high-altitude hotspring sinters, where photosynthetic communities thrive in UV-protected voids 1–10 mm below the siliceous sinter surface (Phoenix et al., 2006). If the photosynthetically active radiation penetrating into the cavities described in this study was not sufficient for photosynthesis, it can be assumed that the microbial communities were dominated by chemotrophic organisms. Rasmussen et al. (2009) reported geochemical evidence for the presence of chemotrophic coelobionts preserved as columnar microstructures in synsedimentary cavities of the Neoarchean Fortescue Group (Australia); they interpreted the negative δ34S values (−8.5‰) of pyrites within the columns as evidence for sulfur-respiring microorganism, and the extremely depleted δ13C values (between −55.4‰ and −43.3‰) of the organic laminae as evidence for methanotrophic metabolism. Although the Moodies Group structures are morphologically similar to those described by Rasmussen et al. (2009), Moodies coelobionts lack cavity-associated sulfide minerals, and the δ13C values of the kerogen (between −32.3‰ and −21.3‰) are not indicative of an ecosystem dominated by methanotrophs. Beyond excluding a methanotrophic metabolism of the coelobionts, the isotopic data and the observed microfossils are consistent with a purely chemotrophic or a photosynthetic community (House et al., 2000; Williford et al., 2013), the latter being the dominant metabolism of the surficial mats located a few millimeters above the cavities (Homann et al., 2015). In conclusion, the data reported here not only record the oldest evidence for cavity-dwelling life on Earth, but can also serve as an analog for UV-protected extraterrestrial habitats, e.g., on Mars.
This work was funded by Deutsche Forschungsgemeinschaft (DFG) grant He2418/13–1 and the collaboration of the European Cooperation in Science and Technology (COST) Action TD1308. We thank Uwe Wiechert (Freie Universität Berlin) and Ulrich Struck (Museum für Naturkunde Berlin) for bulk isotope analyses and James Spotila, Nora Noffke, and two anonymous reviewers for constructive criticism.