Oxygenation of Earth's atmosphere and its impact on the evolution of nitrogen-based metabolisms

Biology

Scientific paper

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1060 Planetary Geochemistry (5405, 5410, 5704, 5709, 6005, 6008), 1094 Instruments And Techniques, 4840 Microbiology, 4870 Stable Isotopes, 5494 Instruments And Techniques

Scientific paper

The evolution of metabolic pathways is closely linked to the evolution of the redox state of the terrestrial atmosphere. Nitrogen has been an essential biological element since the emergence of life when reduced nitrogen compounds (e.g. ammonia) were utilized in the prebiotic synthesis of proteins and nucleic acids. The nitrogen isotopic composition of sediments has been used to trace the origin of sedimentary organic matter in the rock record. Nitrogen is therefore suitable as a biosignature to trace the emergence of life on Earth or other planetary bodies as well as to follow the subsequent evolution of the biosphere in response to global redox changes. Evidence is strong that biological nitrogen fixation evolved very early in the history of life. The Last Common Ancestor (LCA) on Earth was most likely capable of nitrogen fixation as seen from the phylogenetic distribution of nitrogen-fixing organisms in both the domains of Bacteria and Archaea. Phylogenetic trees plotted with nitrogen-fixing gene (Nif) sequences from lineages of Bacteria and Archaea suggest that the Nif genes originated in a common ancestor of the two domains. Other phylogenetic analyses have also demonstrated that the paralogous duplication of the nifDK and nifEN operons, central to nitrogen fixation, predated the divergence of Archaea from Bacteria and therefore occurred prior to the emergence of the LCA. Although the same may be true for denitrification, this metabolic pathway probably did not become dominant until atmospheric pO2 increased between ~2.4 to 1.9 Ga during the Great Oxygenation Event (GOE). Recent work has shown a general depletion in 15N content of Archean (pre-2.5 Ga) relative to Phanerozoic (<540 Ma) kerogens. Studies have shown that the distribution of the δ15N values in kerogens shift from negative values in the Early Archean (from -6 to +6‰ with an average near 0‰ ) to approximately contemporary positive values (from +2 to +10‰ with an average at +6‰ ) by the Early Proterozoic. In the anoxic Archean atmosphere, the nitrogen cycle must have been different and the instability of oxidized nitrogen species such as NO3- under low pO2 must have limited its availability. Therefore nitrogen fixation probably was the dominant nitrogen-based metabolic pathway during the Archean until the rise of oxygen in the atmosphere in the Early Proterozoic, which resulted in more favorable conditions for denitrification to become the dominant nitrogen-based metabolism. Stable isotopic ratios can be used to detect denitrification (which positively fractionates δ15N) and nitrogen fixation (which negatively fractionates δ15N) in K+-containing minerals such as biotite and muscovite. In an effort to characterize the transition from the essentially anoxic Archean atmosphere to the modern oxidizing atmosphere, we are investigating sedimentary rocks spanning 2.4 to 1.9 Ga from Rovaniemi, Finland. Structural NH4+ in minerals is characterized by μFTIR spectroscopy. Our new μFTIR measurements of Early Proterozoic metasediments spanning the 2.4 - 1.9 Ga time interval (and focused on the well-represented 2.2 - 1.9 Ga time interval from Rovaniemi) provide a high-resolution record of ammonium content during the GOE as a prelude to future detailed δ15N measurements by laser mass spectrometry. This work traces the evolution of nitrogen fixation in the biosphere, its response to changes in global redox and provides a tool for the investigation of biosignatures in samples returned from other ancient planetary surfaces.

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