The emergence of a globally productive biosphere

A productive biosphere and oxygenated atmosphere are defining features of Earth and are fundamentally linked. Here I argue that cellular metabolism imposes 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 biospheric expansion and Earth oxygenation. Near the Archean-Proterozoic boundary, cyanobacterial photosynthesis expanded in shallow aquatic environments and along the edges of continents, where weathering inputs made iron more easily accessible. The anoxic deep open ocean was rich in free iron, but this iron remained effectively inaccessible since a photosynthetic expansion would have quenched its own supply. Near the Proterozoic-Phanerozoic boundary, major bioenergetic innovations allowed eukaryotic photosynthesis to begin expanding out into the deep open ocean and onto the continents. These arguments emerge from a recent reconstruction of metabolic evolution in marine Synechococcus and Prochlorococcus, abundant marine picocyanobacteria whose ancestors colonized the oceans in the Neoproterozoic. This reconstruction revealed 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 a by-product increased production of iron-chelating organic carbon. This pushed the oceans through a transition from an anoxic state rich in free iron to an oxygenated state with organic carbon-bound iron. In addition to major increases in biospheric productivity, both the Neoarchean and Neoproterozoic have also been linked to global glaciations, major carbon cycle perturbations and changes in the nature of mantle convection and plate tectonics. This suggests the dynamics of life and Earth are intimately intertwined across many levels and that similar general principles governed Neoarchean and Neoproterozoic transitions in these coupled dynamics.