Understanding what drives self-organization in complex systems and how it arises is a major challenge. We addressed this challenge using dominant oceanic photosynthetic and heterotrophic microbes as a model system. Reconstructing the metabolic evolution of this system suggests that its self-organization and self-amplification were coupled and driven by an increasing cellular energy flux. Specifically, the evolution of cells steadily increased their metabolic rate and excretion of organic carbon. We describe how this increases cellular nutrient uptake and thereby ecosystem biomass. The release of organic carbon, in turn, promotes positive feedbacks among species that reinforce this evolutionary drive at the ecosystem level. We propose the evolutionary self-organization of oceanic microbial ecosystems contributed to the oxygenation of Earth.

Abstract

Metabolism mediates the flow of matter and energy through the biosphere. We examined how metabolic evolution shapes ecosystems by reconstructing it in the globally abundant oceanic phytoplankter Prochlorococcus. To understand what drove observed evolutionary patterns, we interpreted them in the context of its population dynamics, growth rate, and light adaptation, and the size and macromolecular and elemental composition of cells. This multilevel view suggests that, over the course of evolution, there was a steady increase in Prochlorococcus’ metabolic rate and excretion of organic carbon. We derived a mathematical framework that suggests these adaptations lower the minimal subsistence nutrient concentration of cells, which results in a drawdown of nutrients in oceanic surface waters. This, in turn, increases total ecosystem biomass and promotes the coevolution of all cells in the ecosystem. Additional reconstructions suggest that Prochlorococcus and the dominant cooccurring heterotrophic bacterium SAR11 form a coevolved mutualism that maximizes their collective metabolic rate by recycling organic carbon through complementary excretion and uptake pathways. Moreover, the metabolic codependencies of Prochlorococcus and SAR11 are highly similar to those of chloroplasts and mitochondria within plant cells. These observations lead us to propose a general theory relating metabolic evolution to the self-amplification and self-organization of the biosphere. We discuss the implications of this framework for the evolution of Earth’s biogeochemical cycles and the rise of atmospheric oxygen.