Eukaryotization of the early biosphere: A biogeochemical aspect

Abstract

The synthesis of data on the paleobiology and geochemistry of the Archean and Proterozoic and the ecology, biochemistry, and comparative genomics of living organisms provides a means for reconstructing the development of biological complexity on the subcell, organism, and ecosystem levels. The conditions and time of the origin of oxygenic photosynthesis, eukaryotic cells, and multicellular animals were determined. These evolutionary events had a profound influence on the global biogeochemical cycles, sedimentogenesis, and climate of the Earth. Irreversible geochemical changes in the biosphere and the biochemical evolution of living systems are described as complementary processes. A decrease in hydrogen concentration in the early biosphere, an increase in oxygen concentration in the ocean, and changes in the bioavailability of metals (Fe, Ni, Co, V, W, Cu, Mo, etc.) known as enzyme activators were considered as key factors of eukaryotization. The reasons for variations in the availability of the metals in the biosphere were distinguished. The continuity of life was maintained owing to the preservation of the functionality of archaic metabolism types through the compartmentalization of biochemical reactions and the complication of cellular metabolic networks. The metabolic cascades of living cells probably recapitulate this prolonged evolutionary process. The exhaustion of abiogenic hydrogen sources stimulated the symbiosis of hydrogen-producing and hydrogen-consuming prokaryotes and the involvement of simple hydrogen-bearing volatile compounds (CH4, NH3, H2S, and, finally, H2O) as a substrate for life, which eventually predefined the chemical composition of the terrestrial atmosphere strongly dominated by nitrogen and oxygen as by-products of exchange reactions. The oxygenation of the ocean diminished the mobility and bioavailability of some metals that had served as the earliest enzyme activators. The evolutionary response to this process was the formation of mechanisms of extraction, accumulation, and the retention of ancient activator metals (e.g., Fe, W, and Ni) in the cell and in the ecosystem, as well as the active involvement of new metals (e.g., Mo, Cu, and Zn). Oceanic biota became the main concentrator and reservoir for these metals. The appearance of eukaryotic cells, the increasing role of heterotrophy, an increase in biodiversity, the complication of trophic relationships, the acceleration of the cycle of biophile elements, and other features of the biosphere eukaryotization were to large extent a response to the narrowing of the geochemical basis of life. A pivotal point in the prolonged process of biosphere eukaryotization was a series of glaciations at the end of the Proterozoic (750–540 Ma) and the active oxygenation of the ocean, which enabled the global expansion of eukaryotic organisms.