Roger Buick

A Whiff of Oxygen Before the Great Oxidation Event

High-resolution chemostratigraphy reveals an episode of enrichment of the redox-sensitive transition metals molybdenum and rhenium in the late Archean Mount McRae Shale in Western Australia. Correlations with organic carbon indicate that these metals were derived from contemporaneous seawater. Rhenium/osmium geochronology demonstrates that the enrichment is a primary sedimentary feature dating to 2501 ± 8 million years ago (Ma). Molybdenum and rhenium were probably supplied to Archean oceans by oxidative weathering of crustal sulfide minerals. These findings point to the presence of small amounts of O2 in the environment more than 50 million years before the start of the Great Oxidation Event.

Isotopic evidence for microbial sulphate reduction in the early Archaean era.

Sulphate-reducing microbes affect the modern sulphur cycle, and may be quite ancient, though when they evolved is uncertain. These organisms produce sulphide while oxidizing organic matter or hydrogen with sulphate. At sulphate concentrations greater than 1 mM, the sulphides are isotopically fractionated (depleted in 34S) by 10–40‰ compared to the sulphate, with fractionations decreasing to near 0‰ at lower concentrations. The isotope record of sedimentary sulphides shows large fractionations relative to seawater sulphate by 2.7 Gyr ago, indicating microbial sulphate reduction. In older rocks, however, much smaller fractionations are of equivocal origin, possibly biogenic but also possibly volcanogenic. Here we report microscopic sulphides in ∼3.47-Gyr-old barites from North Pole, Australia, with maximum fractionations of 21.1‰, about a mean of 11.6‰, clearly indicating microbial sulphate reduction. Our results extend the geological record of microbial sulphate reduction back more than 750 million years, and represent direct evidence of an early specific metabolic pathway—allowing time calibration of a deep node on the tree of life.

Late archean biospheric oxygenation and atmospheric evolution

High-resolution geochemical analyses of organic-rich shale and carbonate through the 2500 million-year-old Mount McRae Shale in the Hamersley Basin of northwestern Australia record changes in both the oxidation state of the surface ocean and the atmospheric composition. The Mount McRae record of sulfur isotopes captures the widespread and possibly permanent activation of the oxidative sulfur cycle for perhaps the first time in Earths history. The correlation of the time-series sulfur isotope signals in northwestern Australia with equivalent strata from South Africa suggests that changes in the exogenic sulfur cycle recorded in marine sediments were global in scope and were linked to atmospheric evolution. The data suggest that oxygenation of the surface ocean preceded pervasive and persistent atmospheric oxygenation by 50 million years or more.

A reconstruction of Archean biological diversity based on molecular fossils from the 2.78 to 2.45 billion-year-old Mount Bruce Supergroup, Hamersley Basin, Western Australia

Abstract Bitumens extracted from 2.7 to 2.5 billion-year-old (Ga) shales of the Fortescue and Hamersley Groups in the Pilbara Craton, Western Australia, contain traces of molecular fossils. Based on a combination of molecular characteristics typical of many Precambrian bitumens, their consistently and unusually high thermal maturities, and their widespread distribution throughout the Hamersley Basin, the bitumens can be characterized as ‘probably of Archean age’. Accepting this interpretation, the biomarkers open a new window on Archean biodiversity. The presence of hopanes in the Archean rocks confirms the antiquity of the domain Bacteria, and high relative concentrations of 2α-methylhopanes indicate that cyanobacteria were important primary producers. Oxygenic photosynthesis therefore evolved > 2.7 Ga ago, and well before independent evidence suggests significant levels of oxygen accumulated in the atmosphere. Moreover, the abundance of cyanobacterial biomarkers in shales interbedded with oxide-facies banded iron formations (BIF) indicates that although some Archean BIF might have been formed by abiotic photochemical processes or anoxygenic phototrophic bacteria, those in the Hamersley Group formed as a direct consequence of biological oxygen production. Biomarkers of the 3β-methylhopane series suggest that microaerophilic heterotrophic bacteria, probably methanotrophs or methylotrophs, were active in late Archean environments. The presence of steranes in a wide range of structures with relative abundances like those from late Paleoproterozoic to Phanerozoic sediments is convincing evidence for the existence of eukaryotes in the late Archean, 900 Ma before visible fossil evidence indicates that the lineage arose. Sterol biosynthesis in extant eukaryotes requires molecular oxygen. The presence of steranes together with biomarkers of oxygenic photosynthetic cyanobacteria suggests that the concentration of dissolved oxygen in some regions of the upper water column was equivalent to at least ∼1% of the present atmospheric level (PAL) and may have been sufficient to support aerobic respiration.

When did oxygenic photosynthesis evolve

The atmosphere has apparently been oxygenated since the ‘Great Oxidation Event’ ca 2.4 Ga ago, but when the photosynthetic oxygen production began is debatable. However, geological and geochemical evidence from older sedimentary rocks indicates that oxygenic photosynthesis evolved well before this oxygenation event. Fluid-inclusion oils in ca 2.45 Ga sandstones contain hydrocarbon biomarkers evidently sourced from similarly ancient kerogen, preserved without subsequent contamination, and derived from organisms producing and requiring molecular oxygen. Mo and Re abundances and sulphur isotope systematics of slightly older (2.5 Ga) kerogenous shales record a transient pulse of atmospheric oxygen. As early as ca 2.7 Ga, stromatolites and biomarkers from evaporative lake sediments deficient in exogenous reducing power strongly imply that oxygen-producing cyanobacteria had already evolved. Even at ca 3.2 Ga, thick and widespread kerogenous shales are consistent with aerobic photoautrophic marine plankton, and U–Pb data from ca 3.8 Ga metasediments suggest that this metabolism could have arisen by the start of the geological record. Hence, the hypothesis that oxygenic photosynthesis evolved well before the atmosphere became permanently oxygenated seems well supported.

The antiquity of microbial sulfate reduction

The phylogenetic positions of sulfate-reducing organisms, as revealed from comparisons of small-subunit ribosomal RNA (SSU rRNA), are spread over both the Archaeal and Bacterial domains, though when they evolved is uncertain. The low-branching positions of some of these groups on the Tree of Life have inspired the hypothesis that the metabolic innovation of microbial sulfate reduction is of great antiquity. Only recently, however, have sulfur isotope data from Precambrian rocks begun to emerge that clearly demonstrate sulfate-reducing microbes had evolved by the early Archean. The large spread of δ34S values of microscopic pyrites aligned along growth faces of former gypsum crystals in the ∼3.47-Ga North Pole barite deposit of northwestern Australia provide the oldest evidence of microbial sulfate reduction and the earliest indication of a specific microbial metabolism. The distinct expression of microbial sulfate reduction in this localized and cool sulfate-rich environment provides the oldest date for calibrating the temporal progress of early evolution on the Tree of Life.

Isotopic evidence for an aerobic nitrogen cycle in the latest Archean

The nitrogen cycle provides essential nutrients to the biosphere, but its antiquity in modern form is unclear. In a drill core though homogeneous organic-rich shale in the 2.5-billion-year-old Mount McRae Shale, Australia, nitrogen isotope values vary from +1.0 to +7.5 per mil (‰) and back to +2.5‰ over ∼30 meters. These changes evidently record a transient departure from a largely anaerobic to an aerobic nitrogen cycle complete with nitrification and denitrification. Complementary molybdenum abundance and sulfur isotopic values suggest that nitrification occurred in response to a small increase in surface-ocean oxygenation. These data imply that nitrifying and denitrifying microbes had already evolved by the late Archean and were present before oxygen first began to accumulate in the atmosphere.

Air density 2.7 billion years ago limited to less than twice modern levels by fossil raindrop imprints

According to the ‘Faint Young Sun’ paradox, during the late Archaean eon a Sun approximately 20% dimmer warmed the early Earth such that it had liquid water and a clement climate. Explanations for this phenomenon have invoked a denser atmosphere that provided warmth by nitrogen pressure broadening or enhanced greenhouse gas concentrations. Such solutions are allowed by geochemical studies and numerical investigations that place approximate concentration limits on Archaean atmospheric gases, including methane, carbon dioxide and oxygen. But no field data constraining ground-level air density and barometric pressure have been reported, leaving the plausibility of these various hypotheses in doubt. Here we show that raindrop imprints in tuffs of the Ventersdorp Supergroup, South Africa, constrain surface air density 2.7 billion years ago to less than twice modern levels. We interpret the raindrop fossils using experiments in which water droplets of known size fall at terminal velocity into fresh and weathered volcanic ash, thus defining a relationship between imprint size and raindrop impact momentum. Fragmentation following raindrop flattening limits raindrop size to a maximum value independent of air density, whereas raindrop terminal velocity varies as the inverse of the square root of air density. If the Archaean raindrops reached the modern maximum measured size, air density must have been less than 2.3 kg m−3, compared to today’s 1.2 kg m−3, but because such drops rarely occur, air density was more probably below 1.3 kg m−3. The upper estimate for air density renders the pressure broadening explanation possible, but it is improbable under the likely lower estimates. Our results also disallow the extreme CO2 levels required for hot Archaean climates.

Reappraisal of hydrocarbon biomarkers in Archean rocks

Significance The advent of oxygenic photosynthesis set the stage for the evolution of complex life on an oxygenated planet, but it is unknown when this transformative biochemistry emerged. The existing hydrocarbon biomarker record requires that oxygenic photosynthesis and eukaryotes emerged more than 300 million years before the Great Oxidation Event [∼2.4 billion years ago (Ga)]. We report that hopane and sterane concentrations measured in new ultraclean Archean drill cores from Australia are comparable to blank concentrations, yet their concentrations in the exteriors of conventionally collected cores of stratigraphic equivalence exceed blank concentrations by more than an order of magnitude due to surficial contamination. Consequently, previous hydrocarbon biomarker reports no longer provide valid evidence for the advent of oxygenic photosynthesis and eukaryotes by ∼2.7 Ga. Hopanes and steranes found in Archean rocks have been presented as key evidence supporting the early rise of oxygenic photosynthesis and eukaryotes, but the syngeneity of these hydrocarbon biomarkers is controversial. To resolve this debate, we performed a multilaboratory study of new cores from the Pilbara Craton, Australia, that were drilled and sampled using unprecedented hydrocarbon-clean protocols. Hopanes and steranes in rock extracts and hydropyrolysates from these new cores were typically at or below our femtogram detection limit, but when they were detectable, they had total hopane (<37.9 pg per gram of rock) and total sterane (<32.9 pg per gram of rock) concentrations comparable to those measured in blanks and negative control samples. In contrast, hopanes and steranes measured in the exteriors of conventionally drilled and curated rocks of stratigraphic equivalence reach concentrations of 389.5 pg per gram of rock and 1,039 pg per gram of rock, respectively. Polycyclic aromatic hydrocarbons and diamondoids, which exceed blank concentrations, exhibit individual concentrations up to 80 ng per gram of rock in rock extracts and up to 1,000 ng per gram of rock in hydropyrolysates from the ultraclean cores. These results demonstrate that previously studied Archean samples host mixtures of biomarker contaminants and indigenous overmature hydrocarbons. Therefore, existing lipid biomarker evidence cannot be invoked to support the emergence of oxygenic photosynthesis and eukaryotes by ∼2.7 billion years ago. Although suitable Proterozoic rocks exist, no currently known Archean strata lie within the appropriate thermal maturity window for syngenetic hydrocarbon biomarker preservation, so future exploration for Archean biomarkers should screen for rocks with milder thermal histories.

Release of bound aromatic hydrocarbons from late Archean and Mesoproterozoic kerogens via hydropyrolysis

Hydrogen-lean kerogens (atomic H/C<0.4) isolated from the 2.5-billion-year-old (Ga) Mt. McRae Shale, Hamersley Group, at Tom Price, Western Australia, were studied via hydropyrolysis, a continuous-flow technique that degrades organic matter in a stream of high-pressure hydrogen assisted by a dispersed Mo catalyst. The hydropyrolysates yielded predominantly phenanthrene and pyrene, and higher polyaromatic hydrocarbons and alkylated homologues were generated in low relative concentrations. Saturated hydrocarbons were not detected. The molecular and carbon isotopic compositions of the hydropyrolysates are very similar to aromatic hydrocarbons obtained by solvent extraction of the host rocks. Because molecular structures covalently attached to kerogen are unaffected by contamination, this indicates that both the bound and extractable aromatic fractions are syngenetic with the host rocks. Therefore, the results of the hydropyrolysis experiments provide compelling evidence for preserved bitumen of Archean age. The very high proportion of nonalkylated polyaromatic hydrocarbons in the hydropyrolysates is consistent with hydrothermal dehydrogenation of the kerogen, and a marked concentration difference of pyrene in rock extracts and hydropyrolysates might be explained by hydrothermal redistribution of the bitumen. The kerogen and bitumen composition is therefore consistent with models suggesting a hydrothermal origin for the giant iron ore deposits at Mt. Tom Price. Comparison of the Archean samples with hydropyrolysates from immature Mesoproterozoic kerogens from the Roper Group, McArthur Basin, Northern Territory, and with pyrolysis experiments on Proterozoic kerogens in the literature suggests that Precambrian kerogens are frequently highly aromatic and lipid-poor regardless of their degree of thermal preservation.