The emergence of metabolisms through Earth history and implications for biospheric evolution

We investigate the evolution of microbial metabolisms from the last universal common ancestor to the extant biota through comparative phylogenomics, reconciling the evolution of the genes that underpin metabolic pathways with a time-calibrated tree of life. We find that the majority of metabolic pathways were established within the first 2 billion years of Earth history, with pathways accreting at different rates. Methanogenesis and acetogenesis are recovered to be among the earliest energy metabolisms, whereas photosynthetic pathways achieved completeness by 2 Ga, much later than most previous studies have envisaged. Horizontal exchange of metabolic genes is widespread, but it has occurred largely among closely related lineages and for some pathways there is a strong signal of vertical inheritance. We also find that the rate of horizontal gene transfer has been higher in Bacteria than in Archaea through evolutionary history. Finally, we evaluate how our reconstructed history of metabolism can help to constrain hypotheses of biospheric evolution, considering the entropic and Darwinized Gaia hypotheses as well as a simple neutral model for the assembly of biogeochemical cycles.

This article is part of the discussion meeting issue ‘Chance and purpose in the evolution of biospheres’.