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

Abstract

The metabolic processes of cells and chemical processes in the environment are fundamentally intertwined and have evolved in concert over billions of years. 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. Cyanobacterial photosynthesis drove a major biospheric expansion near the Archean-Proterozoic boundary but subsequently 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 remained effectively inaccessible since a photosynthetic expansion would have quenched its own supply. Near the Proterozoic-Phanerozoic boundary, bioenergetic innovations allowed eukaryotic photosynthesis to expand into the deep open oceans and onto the continents, where nutrients are inherently harder to come by. Key insights into 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 Prochlorococcus reveals a sequence of innovations that ultimately produced a form of photosynthesis 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 in turn 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. The periods of Earth history around cyanobacteria- and eukaryote-driven biospheric expansions share several other parallels. Both epochs have also been linked to major carbon cycle perturbations and global glaciations, as well as 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 general principles governed Neoarchean and Neoproterozoic transitions in these coupled dynamics.