The burial of organic carbon, which prevents its remineralization via oxygen-consuming processes, is considered one of the causes of Earth’s oxygenation. Yet, higher levels of oxygen are thought to inhibit burial. Here we propose a resolution of this conundrum, wherein Earth’s initial oxygenation is favored by oxidative metabolisms generating partially oxidized organic matter (POOM), increasing burial via interaction with minerals in sediments. First, we introduce the POOM hypothesis via a mathematical argument. Second, we reconstruct the evolutionary history of one key enzyme family, flavin-dependent Baeyer–Villiger monooxygenases, that generates POOM, and show the temporal consistency of its diversification with the Proterozoic and Phanerozoic atmospheric oxygenation. Finally, we propose that the expansion of oxidative metabolisms instigated a positive feedback, which was amplified by the chemical changes to minerals on Earth’s surface. Collectively, these results suggest that Earth’s oxygenation is an autocatalytic transition induced by a combination of biological innovations and geological changes.

Organic matter degradation and preservation are crucial components of Earth’s carbon cycle. Empirical and phenomenological models usually contain parameters determined by site-specific data and focus on different aspects of the decay and accretion characteristics. To investigate more fundamental mechanisms, this study suggests a hierarchical model that links microscopic physical quantities to macroscopic degradation and preservation patterns. This mechanistic model predicts several commonly observed phenomena, including the lognormal distribution of degradation rate constants, the recalcitrance-dependent sensitivity to temperature, the dependence of a heterogeneous organic-matter system’s persistence on its complexity, logarithmic-time decay, and power-law degradation behavior. The theoretical predictions of this model are consistent with the observational data from marine and lake environments. This hierarchical model may provide a step towards a fundamental theory of organic matter degradation and preservation in aquatic and other ecosystems.

Methanogenic archaea have been shown to reduce iron from ferric [Fe(III)] to ferrous [Fe(II)] state, but minerals that form during iron reduction by different methanogens remain to be characterized. Here, we show that zero-valent iron (ZVI) minerals, ferrite [α-Fe(0)] and austenite [γ-Fe(0)], appear in the X-ray diffraction spectra minutes after the addition of ferrihydrite to the cultures of the methanogenic archaeon Methanosarcina barkeri (M. barkeri). M. barkeri cells and redox-active, non-enzymatic soluble organic compounds in organic-rich spent culture supernatants can promote the formation of ZVI; the latter compounds also likely stabilize ZVI. Methanogenic microbes that inhabit organic-and Fe(III)-rich anaerobic environments may similarly reduce oxidized iron to Fe(II) and ZVI, with implications for the preservation of paleomagnetic signals during sediment diagenesis and potential applications in the protection of iron metals against corrosion and in the green synthesis of ZVI.

Oxygenation events remarkably altered the distribution, diversity, and abundance of minerals on Earth’s surface. However, the causality in the opposite direction—the influence of mineral evolution on atmospheric oxygen levels—has rarely been explored. Here I propose that mineral evolution might have led Earth’s oxygen cycle to lose stability, facilitating oxygenation events in deep time. First, I introduce a conceptual model for the system of organic matter and minerals and investigate their interactions via a probabilistic approach. Second, in light of the theoretical results, I suggest that the evolution of iron and clay minerals likely had an underappreciated relevance to the Great Oxidation Event and Neoproterozoic Oxidation Event, respectively. Finally, I use the parameter values estimated from observations in modern environments as benchmarks to test these speculations. This study provides a minimalistic theoretical framework illustrating the possible influence of mineral evolution on Earth’s oxygen cycle over geologic time.

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