Ecological Expansion of Complex Life Forms at the End of the Paleoproterozoic Great Oxidation Event

Changes in Earth’s surface redox conditions have strongly influenced nutrient availability and biological evolution. A key milestone in the interplay between Earth’s surface oxygenation and biogeochemical cycles occurred during the ca. 2.43-2.06 Ga Great Oxidation Episode (GOE) when atmospheric oxygen rose above 10-6 of the present atmospheric level. The late stage of the GOE corresponds to the ca. 2.22-2.06 Ga Lomagundi Event (LE), the most pronounced and longest-lasting positive carbon isotope excursion in Earth's history. The LE is attributed to increased organic carbon burial, generated via high rates of oxygenic photosynthesis during a period of enhanced phosphorus flux to the oceans in association with intense oxidative weathering on the continents. Despite the pivotal role of the LE in expanding aerobic biogeochemical cycles, the biological processes and metabolic complexities underlying organic productivity, as well as the interaction between inorganic and organic carbon sedimentary fluxes during the peak of the LE, remain highly debated. Here, carbon (δ13Ccarb and δ13Corg ‰, VPDB) and zinc (δ66/64Zn ‰, JMC-L) isotope compositions were analyzed in marine carbonates and black shales from the Francevillian Group, deposited during the LE and in its aftermath, and bearing macrostructures interpreted to be macroscopic organisms. Within the Francevillian Group, where δ13Ccarb values consistently exceed +4‰—a signature of the LE—the marine carbonates and black shales exhibit δ66/64Zn values higher than the lithogenic Zn isotope composition (~0.3‰). In contrast, δ13Corg values at the same stratigraphic level show a pronounced negative excursion of up to 9‰, with values decreasing from an average of −25.8‰ in the lower part to −34.8‰ in the upper part of the sedimentary interval recording the LE. The δ66/64Zn values >0.3‰ may reflect an isotope composition imparted by preferential uptake of light Zn isotopes by photosynthetic or complex organisms with high Zn demand. In support of this, the complex Francevillian biota has been found to be significantly enriched in light Zn isotopes, with δ66/64Zn values as low as −0.152‰, while their host sediments have much higher δ66/64Zn values up to +0.477‰. We propose that the negative excursion in δ13Corg values, recorded in the portion of the Francevillian Group where carbonates still yield highly positive δ13Ccarb values, represents a decoupling of marine organic and inorganic carbon sedimentary fluxes, likely controlled by changes in organic productivity driven by marine organisms with sufficiently complex Zn metabolisms, such as eukaryotes, that widely expanded in marine habitats.