In Situ Fe and S isotope analyses in pyrite from the 3.2 Ga Mendon Formation (Barberton Greenstone Belt,South Africa): Evidence for early microbial iron reduction

On the basis of phylogenetic studies and laboratory cultures, it has been proposed that the ability of microbes to metabolize iron has emerged prior to the Archaea/Bacteria split. However, no unambiguous geochemical data supporting this claim have been put forward in rocks older than 2.7–2.5 giga years (Gyr). In the present work, we report in situ Fe and S isotope composition of pyrite from 3.28‐ to 3.26‐Gyr‐old cherts from the upper Mendon Formation, South Africa. We identified three populations of microscopic pyrites showing a wide range of Fe isotope compositions, which cluster around two δ⁵⁶Fe values of ?1.8‰ and +1‰. These three pyrite groups can also be distinguished based on the pyrite crystallinity and the S isotope mass‐independent signatures. One pyrite group displays poorly crystallized pyrite minerals with positive Δ³³S values > +3‰, while the other groups display more variable and closer to 0‰ Δ³³S values with recrystallized pyrite rims. It is worth to note that all the pyrite groups display positive Δ³³S values in the pyrite core and similar trace element compositions. We therefore suggest that two of the pyrite groups have experienced late fluid circulations that have led to partial recrystallization and dilution of S isotope mass‐independent signature but not modification of the Fe isotope record. Considering the mineralogy and geochemistry of the pyrites and associated organic material, we conclude that this iron isotope systematic derives from microbial respiration of iron oxides during early diagenesis. Our data extend the geological record of dissimilatory iron reduction (DIR) back more than 560 million years (Myr) and confirm that micro‐organisms closely related to the last common ancestor had the ability to reduce Fe(III).     

Early Archean origin of Photosystem II

Photosystem II is a photochemical reaction center that catalyzes the light‐driven oxidation of water to molecular oxygen. Water oxidation is the distinctive photochemical reaction that permitted the evolution of oxygenic photosynthesis and the eventual rise of eukaryotes. At what point during the history of life an ancestral photosystem evolved the capacity to oxidize water still remains unknown. Here, we study the evolution of the core reaction center proteins of Photosystem II using sequence and structural comparisons in combination with Bayesian relaxed molecular clocks. Our results indicate that a homodimeric photosystem with sufficient oxidizing power to split water had already appeared in the early Archean about a billion years before the most recent common ancestor of all described Cyanobacteria capable of oxygenic photosynthesis, and well before the diversification of some of the known groups of anoxygenic photosynthetic bacteria. Based on a structural and functional rationale, we hypothesize that this early Archean photosystem was capable of water oxidation to oxygen and had already evolved protection mechanisms against the formation of reactive oxygen species. This would place primordial forms of oxygenic photosynthesis at a very early stage in the evolutionary history of life.     

Early Archean planktonic mode of life: Implications from fluid dynamics of lenticular microfossils

Lenticular, and commonly flanged, microfossils in 3.0–3.4 Ga sedimentary deposits in Western Australia and South Africa are unusually large (20–80 μm across), robust, and widespread in space and time. To gain insight into the ecology of these organisms, we performed simulations of fluid dynamics of virtual cells mimicking lenticular forms of variable sizes, oblateness, flange presence, and flange thickness. Results demonstrate that (a) the flange reduces sedimentation velocity, (b) this flange function works more effectively in larger cells, and (c) modest oblateness lowers sedimentation rate. These observations support interpretations that the lenticular microbes were planktonic—a lifestyle that could have been advantageous in an early Earth harsh environment including violent volcanic activities, repeated asteroid impacts, and relatively high UV‐radiation. Although the robustness of these organisms could have provided additional protection on the early Earth, this architecture may have impeded a planktonic lifestyle by increasing cell density. However, our data suggest that this disadvantage could have been compensated by enlargement of cell volume, which could have enhanced the ability of the flange to slow sedimentation rate, especially if coupled with vacuolation. The results of this simulation study may help to explain the unique morphology and unusually large size of these Archean microfossils.     

The oldest records of photosynthesis

There is diverse, yet controversial fossil evidence for the existence of photosynthesis 3500 million years ago. Among the most persuasive evidence is the stromatolites described from low grade metasedimentary rocks in Western Australia and South Africa. Based on the understanding of the paleobiology of stromatolites and using pertinent fossil and Recent analogs, these Early Archean stromatolites suggest that phototrophs evolved by 3500 million years ago. The evidence allows further interpretation that cyanobacteria were involved. Besides stromatolites, microbial and chemical fossils are also known from the same rock units. Some microfossils morphologically resemble cyanobacteria and thus complement the adduced cyanobacterial involvement in stromatolite construction. If cyanobacteria had evolved by 3500 million years ago, this would indicate that nearly all prokaryotic phyla had already evolved and that prokaryotes diversified rapidly on the early Earth.     

A morphogram for silica‐witherite biomorphs and its application to microfossil identification in the early earth rock record

Archean hydrothermal environments formed a likely site for the origin and early evolution of life. These are also the settings, however, were complex abiologic structures can form. Low‐temperature serpentinization of ultramafic crust can generate alkaline, silica‐saturated fluids in which carbonate–silica crystalline aggregates with life‐like morphologies can self‐assemble. These “biomorphs” could have adsorbed hydrocarbons from Fischer–Tropsch type synthesis processes, leading to metamorphosed structures that resemble carbonaceous microfossils. Although this abiogenic process has been extensively cited in the literature and has generated important controversy, so far only one specific biomorph type with a filamentous shape has been discussed for the interpretation of Archean microfossils. It is therefore critical to precisely determine the full distribution in morphology and size of these biomorphs, and to study the range of plausible geochemical conditions under which these microstructures can form. Here, a set of witherite‐silica biomorph synthesis experiments in silica‐saturated solutions is presented, for a range of pH values (from 9 to 11.5) and barium ion concentrations (from 0.6 to 40 mmol/L BaCl₂). Under these varying conditions, a wide range of life‐like structures is found, from fractal dendrites to complex shapes with continuous curvature. The size, spatial concentration, and morphology of the biomorphs are strongly controlled by environmental parameters, among which pH is the most important. This potentially limits the diversity of environments in which the growth of biomorphs could have occurred on Early Earth. Given the variety of the observed biomorph morphologies, our results show that the morphology of an individual microstructure is a poor criterion for biogenicity. However, biomorphs may be distinguished from actual populations of cellular microfossils by their wide, unimodal size distribution. Biomorphs grown by diffusion in silica gel can be differentiated by their continuous gradient in size, spatial density, and morphology along the direction of diffusion.     

On the Plausibility of a UV Transparent Biochemistry

Some molecules, particularly aromatics, have high molar extinction coefficients at wavelengths in the damaging ultraviolet radiation region of the spectrum between 200 and 400 nm. Thus, under a UV radiation flux in which thesewavelengths are represented, it could be argued that aselection pressure would exist for a UV transparentbiochemistry in which they were not represented. Thishypothesis is explored using data made available fromproteomics, focusing particularly on tryptophan, againstwhich a selection pressure could exist on present-day Earth as a result of its absorbance shoulder at wavelengths greater than290 nm. The abundance of tryptophan in whole proteomes is lowerthan expected from the degeneracy of the genetic code.A lower usage of tryptophan is found in the cytochrome c oxidase polypeptide I of UV-exposed organisms compared to nocturnal and subterranean organisms, but not in ATP synthase chain A. Examination of the amino acid composition of photolyase, an enzyme that requires exposure to light to function, shows that the tryptophan abundances exceed those of the total proteome of most organismsand the abundances expected from the degeneracy of the genetic code. This is also true for cytochrome c oxidase, another enzymethat makes extensive use of the electron transfer propertiesof tryptophan. We suggest that the selection pressure for the useof tryptophan caused, among other factors, by the uses of delocalised pi-electrons that this aromatic provides in active sites and binding motifs outweighs the selection pressure for UVtransparency. This trade-off explains the lack of conclusive evidence for a UV transparent selection pressure. We suggest thatthis trade-off applies to the stacked pi-electrons of DNA. It offers a solution to the long-standing paradox of why the macromolecule responsible for the faithful replication of information has high absorbance in the damaging UV radiation region of the spectrum.     

Non‐enzymatic glycolysis and pentose phosphate pathway‐like reactions in a plausible Archean ocean

The reaction sequences of central metabolism, glycolysis and the pentose phosphate pathway provide essential precursors for nucleic acids, amino acids and lipids. However, their evolutionary origins are not yet understood. Here, we provide evidence that their structure could have been fundamentally shaped by the general chemical environments in earth's earliest oceans. We reconstructed potential scenarios for oceans of the prebiotic Archean based on the composition of early sediments. We report that the resultant reaction milieu catalyses the interconversion of metabolites that in modern organisms constitute glycolysis and the pentose phosphate pathway. The 29 observed reactions include the formation and/or interconversion of glucose, pyruvate, the nucleic acid precursor ribose‐5‐phosphate and the amino acid precursor erythrose‐4‐phosphate, antedating reactions sequences similar to that used by the metabolic pathways. Moreover, the Archean ocean mimetic increased the stability of the phosphorylated intermediates and accelerated the rate of intermediate reactions and pyruvate production. The catalytic capacity of the reconstructed ocean milieu was attributable to its metal content. The reactions were particularly sensitive to ferrous iron Fe(II), which is understood to have had high concentrations in the Archean oceans. These observations reveal that reaction sequences that constitute central carbon metabolism could have been constrained by the iron‐rich oceanic environment of the early Archean. The origin of metabolism could thus date back to the prebiotic world.     

Towards a 'natural' time scale for the Precambrian – A proposal

A proposal is put forward to redefine the geological time scale for the Precambrian. Flaws of the present, chronometrically defined, time scale are discussed and illustrated. It is concluded that we need to go back to the rock record to define a “natural” time scale, in which major divisions (eons, eras, etc.) are defined in terms of first-order events and transitions in the observable stratigraphic record. For the earliest part of Earth history, we need a time scale, including a formalized Hadean eon, that is fully consistent with rapidly evolving insights from planetary science.     

A Coupled Ecosystem-Climate Model for Predicting the Methane Concentration in the Archean Atmosphere

A simple coupled ecosystem-climate model is described that canpredict levels of atmospheric CH₄, CO₂, and H₂during the Late Archean, given observed constraints on Earth'ssurface temperature. We find that methanogenic bacteria shouldhave converted most of the available atmospheric H₂ intoCH₄, and that CH₄ may have been equal in importance to CO₂ as a greenhouse gas. Photolysis of this CH₄ may have produced a hydrocarbon smog layer that would have shielded the surface from solar UV radiation. Methanotrophic bacteria would have consumed some of the atmospheric CH₄,but they would have been incapable of reducing CH₄ to modern levels. The rise of O₂ around 2.3 Ga would have drastically reduced the atmospheric CH₄ concentrationand may thereby have triggered the Huronian glaciation.     

Phosphate Solubility and the Cyanate-Mediated Synthesis of Pyrophosphate

The justification for a less alkaline primordial ocean (than present) is briefly reviewed, along with constraints on aqueous phosphate under such conditions. Based on the assumption that CaHPO₄ dihydrate determined the availability of phosphorus species, we have carried out laboratory simulations to determine equilibrium concentrations as a function of pH (in PIPES buffer) with added NaCl and CaCl₂. Consistent with expectations, solubility declines with higher pH and [CaCl₂], but increases only slightly with [NaCl]. Significantly, PIPES shows no specific effect on the dissolution beyond its influence on pH and ionic strength. Data are also presented on the synthesis of pyrophosphate from the NaOCN/CaHPO₄·2H₂O system, which could have provided a source of this phosphate anhydride on the early Earth.