Implications of a 3.472-3.333 Gyr-old subaerial microbial mat from the Barberton greenstone belt, South Africa for the UV environmental conditions on the early Earth

Abstract

Modelling suggests that the UV radiation environment of the early Earth, with DNA weighted irradiances of about three orders of magnitude greater than those at present, was hostile to life forms at the surface, unless they lived in specific protected habitats. However, we present empirical evidence that challenges this commonly held view. We describe a well-developed microbial mat that formed on the surface of volcanic littoral sediments in an evaporitic environment in a 3.5-3.3Ga-old formation from the Barberton greenstone belt. Using a multiscale, multidisciplinary approach designed to strongly test the biogenicity of potential microbial structures, we show that the mat was constructed under flowing water by 0.25 microm filaments that produced copious quantities of extracellular polymeric substances, representing probably anoxygenic photosynthesizers. Associated with the mat is a small colony of rods-vibroids that probably represent sulphur-reducing bacteria. An embedded suite of evaporite minerals and desiccation cracks in the surface of the mat demonstrates that it was periodically exposed to the air in an evaporitic environment. We conclude that DNA-damaging UV radiation fluxes at the surface of the Earth at this period must either have been low (absorbed by CO2, H2O, a thin organic haze from photo-dissociated CH4, or SO2 from volcanic outgassing; scattered by volcanic, and periodically, meteorite dust, as well as by the upper layers of the microbial mat) and/or that the micro-organisms exhibited efficient gene repair/survival strategies.

Figure 1

(a) UV flux at the surface of early Earth (3.5 Ga) for the equator at vernal equinox. (b) UV flux on present-day Earth for the equator at vernal equinox. In both the cases, total UV flux is shown along with the total of UVC and UVB (the biologically most important wavelengths). In all the cases, optical depth of dust is taken as 0.1. Here, UVB radiation is defined as 280–315 nm according to the conventions adopted by the International Commission on Illumination. (From Cockell et al. 2000).

Figure 2

Location map of the Josefsdal Chert in the Barberton greenstone belt (simplified after Lowe & Byerly 1999).

Figure 3

(a) Photograph of the Josefsdal Chert sample 96SA05 showing the alternation of black and greenish-white layers. (b) Optical microscope image of one of the black layers at the top of a fining upwards sequence, illustrating its slightly laminated structure and its sharp upper contact with the overlying (coarser-grained) greenish-white layer (arrow). The lower boundary is gradational.

Figure 4

Raman spectral signature obtained from the exposed FIB-cut section across the mat-like structure documenting the kerogenous composition of the interior of the mat. The presence of a well-defined D and G peak demonstrates that the kerogen is mature and is not a recent phenomenon.

Figure 5

SEM micrograph composite of half of the microbial mat that was exposed across the freshly broken surface, showing it in plan view. The large black arrows mark the main direction of current flow. The smaller dotted black arrow marks a 35–40° change in flow direction in the uppermost mat layer. The small white arrow indicates the direction of overturning of a portion of mat that has curled over under the influence of the current flow.

Figure 6

SEM micrographs documenting different characteristics of the microbial mat. (a) Parallel and overturned filaments (white arrow) indicating flow direction (large black arrow). Note the blocky minerals (M) embedded in the mat. (b) Desiccation cracks (arrow) in the film are common. (c) Intercalated evaporite–encrusted mat (em) beneath smooth to ropy surfaced mat (srm) that ‘flows’ around an evaporite precipitate (arrow). (d) Evaporite minerals include oval to platy pseudo-gypsum (see also the desert-rose twinning in the inset) and acicular pseudo-aragonite. A strand of filamentous film partially covers some acicular crystals (arrow). (e) Small association of rare rod/vibroid-shaped structures embedded in smooth EPS. Some individuals are attached to each other at their apices (black arrow). (f) Rare, isolated portion of a turgid filament (arrow). The filaments are usually deeply embedded in the polymer film (compare with figure 8b).

Figure 7

(a) The main mat has peeled away from this area to reveal the initial intimate intergrowth of the filaments (black arrow) and granular precipitates (including a halide, white arrow) with the underlying sediment particles. (b) Portion of the filamentous mat ‘flowing’ around a trapped detrital particle. (c and d) Filaments in a lightly etched (15 min), polished thin section surface. The filaments traverse the boundary between two quartz crystals (arrow in c) and are clearly embedded in the quartz (small arrow in d), showing that they predate the formation of the quartz matrix. The filaments were bent around a particle (represented by an empty mould; large arrow), demonstrating flexibility (d).

Figure 8

(a) Areas of the smooth to ropy-surfaced mat that have suffered from mechanical tearing (arrows). (b) Filament deeply embedded in EPS (arrow). Note the high-Mg calcite pseudomorphs embedded in the mat surface on the right. (c) Individual filament (arrow). (d) EDX spot measurement of the filament. Note the C peak in the spectrum (arrow). (e) Part of mat surface showing plastic deformation of the filaments and polymer across cracks indicating desiccation before silicification.

Figure 9

Hypothetical Early Mid-Archaean coastal landscape in the Josefsdal area. (a) Volcano erupting ashy material onto the coastal plain and into the lagoon; rivers transporting eroded sediments into the lagoon surrounded by a strip of beach sediments; alternating layers of lava flows separated by thin layers of sediments underling the lagoon and coastal plain; hydrothermal dykes or veins cut through the lava and sediment layers to reach the surface. (b) Close up view of the beach area showing the prevalence of hydrothermal springs, also on the beach, and evaporite deposits on the beach. (c and d) Close up views (SEM) of the surface of the sediments on the beach showing different aspects of the microbial biofilm formed in the vicinity of the spring. In (c) a portion of the filamentous mat is overturned (small arrow) and overlain by another strand of filamentous mat (large arrow). In (d) the current direction is given by the main arrow and overturned portions of the film are marked by small arrows. The location of figure 6a is shown. A large halide hopper (h) is wedged under the mat.

Figure 10

FIB section across a ropy portion of the mat. (a) Secondary image showing the location of the FIB section (arrow). (b) Ion beam image of the section surface documenting the alveolar-like structure of the degraded organic matter (amorphous kerogen, K) in the interior of the mat (cf. kopara in modern calcareous lagoons, Défarge et al. 1994). The fineness of the silica coating in the top of the mat is observable in this image (arrows). (c) EDX analysis illustrating the strong carbon peak detected in the amorphous kerogen below the surface of the mat.

Figure 11

FIB-cut sections across different parts of the microbial mat. (a and b) show a cut across a portion of the mat that is not coated with evaporite minerals. (a) A secondary electron image of the smooth to ropy surface of this portion of the mat, showing the location of the FIB cut. (b) A backscattered image of the FIB section. Although bundles of filaments and individual filaments (fat black arrows) have been well-preserved on the surface of the mat by a thin layer of silica, individual filaments do not appear to have been preserved within the body of the mat. Instead, the kerogen (K, dark in appearance in this backscattered image, i.e. low z) is amorphous. Note the thin intervening layers of authigenic crystallites within the body of the mat (white arrow). The ‘toe’-like structures below the mat (dotted white arrow) are an artefact of the ion beam sputtering, as are the holes in the high reflectance surface of the Au-coated mat in (small black arrow). (c and d) FIB section across an evaporite mineral encrusted portion of the mat. (c) Secondary electron image showing the location of the FIB section (white line). (d) In this backscattered image, the evaporite encrusted mat exhibits extreme complexity in its vertical structure. Dark amorphous masses of kerogen (white arrows) are indiscriminated interspersed with evaporite crystallites within the body of the mats. Note the quartz crystal (q) ‘floating within the mineralized kerogen matrix’.