Evolution of cellular metabolism and the rise of a globally productive biosphere

Metabolic processes in cells and chemical processes in the environment are fundamentally intertwined and have evolved in concert for most of Earth's existence. Here I argue that intrinsic properties of cellular metabolism imposed central constraints on the historical trajectories of biopsheric productivity and atmospheric oxygenation. Photosynthesis depends on iron, but iron is highly insoluble under the aerobic conditions produced by oxygenic photosynthesis. These counteracting constraints led to two major stages of Earth oxygenation. After a cyanobacteria-driven biospheric expansion near the Archean-Proterozoic boundary, productivity remained largely restricted to continental boundaries and shallow aquatic environments where weathering inputs made iron more accessible. The anoxic deep open ocean was rich in free iron during the Proterozoic, but this iron was largely inaccessible, partly because an otherwise nutrient-poor ocean was limiting to photosynthesis, but also because a photosynthetic expansion would have quenched its own iron supply. Near the Proterozoic-Phanerozoic boundary, bioenergetics innovations allowed eukaryotic photosynthesis to overcome these interconnected negative feedbacks and begin expanding into the deep open oceans and onto the continents, where nutrients are inherently harder to come by. Key insights into what drove the ecological rise of eukaryotic photosynthesis emerge from analyses of marine Synechococcus and Prochlorococcus, abundant marine picocyanobacteria whose ancestors colonized the oceans in the Neoproterozoic. The reconstructed evolution of this group reveals a sequence of innovations that ultimately produced a form of photosynthesis in Prochlorococcus that is more like that of green plant cells than other cyanobacteria. Innovations increased the energy flux of cells, thereby enhancing their ability to acquire sparse nutrients, and as by-product also increased the production of organic carbon waste. Some of these organic waste products had the ability to chelate iron and make it bioavailable, thereby indirectly pushing the oceans through a transition from an anoxic state rich in free iron to an oxygenated state with organic carbon-bound iron. Resulting conditions (and parallel processes on the continents) in turn led to a series of positive feedbacks that increased the availability of other nutrients, thereby promoting the rise of a globally productive biosphere. In addition to the occurrence of major biospheric expansions, the several hundred million-year periods around the Archean-Proterozoic and Proterozoic-Phanerozoic boundaries share a number of other parallels. Both epochs have also been linked to major carbon cycle perturbations and global glaciations, as well as changes in the nature of plate tectonics and increases in continental exposure and weathering. This suggests the dynamics of life and Earth are intimately intertwined across many levels and that general principles governed transitions in these coupled dynamics at both times in Earth history.