Abstract. Metabolism is the chemical system that supplies the energy and building blocks of all cells. The collective activity of all cells mediates the global biogeochemical cycles, which in turn regulate the Earth's climate. Reconstructing metabolic evolution provides a powerful lens for identifying general principles of biospheric self-organization and how life has shaped our planet. I will illustrate these ideas using highly abundant microbial ecosystems in the worlds surface oceans as a model system. I will argue these ecosystem evolved through a sequence of "niche constructing adaptive radiations" that drew down limiting nutrients in the surface oceans while increasing dissolved organic carbon, in turn promoting the co-evolution of all cells. I will further argue this led to a collective metabolism in oceanic microbial ecosystems that is highly similar to that of organelles within plant cells. Finally I will argue that the evolutionary self-organization of oceanic microbial ecosystems contributed to the oxygenation of Earth, and more generally that the latter reflects an increasing metabolic rate of the biosphere.