Evolution of iron and oxygen biogeochemical cycles during the Precambrian.

Iron (Fe) is an essential element for life, and its geochemical cycle is intimately linked to the coupled history of life and Earth's environment. The accumulated geologic records indicate that ferruginous waters existed in the Precambrian oceans not only before the first major rise of atmospheric O2 levels (Great Oxidation Event; GOE) during the Paleoproterozoic, but also during the rest of the Proterozoic. However, the interactive evolution of the biogeochemical cycles of O2 and Fe during the Archean-Proterozoic remains ambiguous. Here, we develop a biogeochemical model to investigate the coupled biogeochemical evolution of Fe-O2 -P-C cycles across the GOE. Our model demonstrates that the marine Fe cycle was less sensitive to changes in the production rate of O2 before the GOE (atmospheric pO2 < 10-6 PAL; present atmospheric level). When the P supply rate to the ocean exceeds a certain threshold, the GOE occurs and atmospheric pO2 rises to ~10-3 -10-1 PAL. After the GOE, the marine Fe(II) concentration is highly sensitive to atmospheric pO2 , suggesting that the marine redox landscape during the Proterozoic may have fluctuated between ferruginous conditions and anoxic non-ferruginous conditions with sulfidic water masses around continental margins. At a certain threshold value of atmospheric pO2 of ~0.3% PAL, the primary oxidation pathway of Fe(II) shifts from the activity of Fe(II)-utilizing anoxygenic photoautotrophs in sunlit surface waters to abiotic process in the deep ocean. This is accompanied by a shift in the primary deposition site of Fe(III) hydroxides from the surface ocean to the deep sea, providing a plausible mechanistic explanation for the observed cessation of iron formations during the Proterozoic.

Biogeochemical transformations after the emergence of oxygenic photosynthesis and conditions for the first rise of atmospheric oxygen.

The advent of oxygenic photosynthesis represents the most prominent biological innovation in the evolutionary history of the Earth. The exact timing of the evolution of oxygenic photoautotrophic bacteria remains elusive, yet these bacteria profoundly altered the redox state of the ocean-atmosphere-biosphere system, ultimately causing the first major rise in atmospheric oxygen (O2 )-the so-called Great Oxidation Event (GOE)-during the Paleoproterozoic (~2.5-2.2 Ga). However, it remains unclear how the coupled atmosphere-marine biosphere system behaved after the emergence of oxygenic photoautotrophs (OP), affected global biogeochemical cycles, and led to the GOE. Here, we employ a coupled atmospheric photochemistry and marine microbial ecosystem model to comprehensively explore the intimate links between the atmosphere and marine biosphere driven by the expansion of OP, and the biogeochemical conditions of the GOE. When the primary productivity of OP sufficiently increases in the ocean, OP suppresses the activity of the anaerobic microbial ecosystem by reducing the availability of electron donors (H2 and CO) in the biosphere and causes climate cooling by reducing the level of atmospheric methane (CH4 ). This can be attributed to the supply of OH radicals from biogenic O2 , which is a primary sink of biogenic CH4 and electron donors in the atmosphere. Our typical result also demonstrates that the GOE is triggered when the net primary production of OP exceeds >~5% of the present oceanic value. A globally frozen snowball Earth event could be triggered if the atmospheric CO2 level was sufficiently small (<~40 present atmospheric level; PAL) because the concentration of CH4 in the atmosphere would decrease faster than the climate mitigation by the carbonate-silicate geochemical cycle. These results support a prolonged anoxic atmosphere after the emergence of OP during the Archean and the occurrence of the GOE and snowball Earth event during the Paleoproterozoic.

Evolution of Superoxide Dismutases and Catalases in Cyanobacteria: Occurrence of the Antioxidant Enzyme Genes before the Rise of Atmospheric Oxygen.

Knowledge on the evolution of antioxidant systems in cyanobacteria is crucial for elucidating the cause and consequence of the rise of atmospheric oxygen in the Earth's history. In this study, to elucidate the origin and evolution of cyanobacterial antioxidant enzymes, we analyzed the occurrence of genes encoding four types of superoxide dismutases and three types of catalases in 85 complete cyanobacterial genomes, followed by phylogenetic analyses. We found that Fe superoxide dismutase (FeSOD), Mn superoxide dismutase (MnSOD), and Mn catalase (MnCat) are widely distributed among modern cyanobacteria, whereas CuZn superoxide dismutase (CuZnSOD), bifunctional catalase (KatG), and monofunctional catalase (KatE) are less common. Ni superoxide dismutase (NiSOD) is distributed among marine Prochlorococcus and Synechococcus species. Phylogenetic analyses suggested that bacterial MnSOD evolved from cambialistic Fe/MnSOD before the diversification of major bacterial lineages. The analyses suggested that FeSOD evolved from MnSOD before the origin of cyanobacteria. MnCat also evolved in the early stages of bacterial evolution, predating the emergence of cyanobacteria. KatG, KatE, and NiSOD appeared 2.3-2.5 billion years ago. Thus, almost all cyanobacterial antioxidant enzymes emerged before or during the rise of atmospheric oxygen. The loss and appearance of these enzymes in marine cyanobacteria may be also related to the change in the metal concentration induced by the increased oxygen concentration in the ocean.

A sluggish mid-Proterozoic biosphere and its effect on Earth's redox balance.

The possibility of low but nontrivial atmospheric oxygen (O2 ) levels during the mid-Proterozoic (between 1.8 and 0.8 billion years ago, Ga) has important ramifications for understanding Earth's O2 cycle, the evolution of complex life and evolving climate stability. However, the regulatory mechanisms and redox fluxes required to stabilize these O2 levels in the face of continued biological oxygen production remain uncertain. Here, we develop a biogeochemical model of the C-N-P-O2 -S cycles and use it to constrain global redox balance in the mid-Proterozoic ocean-atmosphere system. By employing a Monte Carlo approach bounded by observations from the geologic record, we infer that the rate of net biospheric O2 production was 3 . 5 - 1.1 + 1.4 Tmol year-1 (1σ), or ~25% of today's value, owing largely to phosphorus scarcity in the ocean interior. Pyrite burial in marine sediments would have represented a comparable or more significant O2 source than organic carbon burial, implying a potentially important role for Earth's sulphur cycle in balancing the oxygen cycle and regulating atmospheric O2 levels. Our statistical approach provides a uniquely comprehensive view of Earth system biogeochemistry and global O2 cycling during mid-Proterozoic time and implicates severe P biolimitation as the backdrop for Precambrian geochemical and biological evolution.

Osmium evidence for synchronicity between a rise in atmospheric oxygen and Palaeoproterozoic deglaciation.

Early Palaeoproterozoic (2.5-2.0 billion years ago) was a critical phase in Earth's history, characterized by multiple severe glaciations and a rise in atmospheric O(2) (the Great Oxidation Event). Although glaciations occurred at the time of O(2) increase, the relationship between climatic and atmospheric transitions remains poorly understood. Here we report high concentrations of the redox-sensitive element Os with high initial (187)Os/(188)Os values in a sandstone-siltstone interval that spans the transition from glacial diamictite to overlying carbonate in the Huronian Supergroup, Canada. Together with the results of Re, Mo and S analyses of the sediments, we suggest that immediately after the second Palaeoproterozoic glaciation, atmospheric O(2) levels became sufficiently high to deliver radiogenic continental Os to shallow-marine environments, indicating the synchronicity of an episode of increasing O(2) and deglaciation. This result supports the hypothesis that climatic recovery from the glaciations acted to accelerate the Great Oxidation Event.