Insights into the evolution of oxygenic photosynthesis from a phylogenetically novel, low-light cyanobacterium

Abstract

AbstractAtmospheric oxygen level rose dramatically around 2.4 billion years ago due to oxygenic photosynthesis by the Cyanobacteria. The oxidation of surface environments permanently changed the future of life on Earth, yet the evolutionary processes leading to oxygen production are poorly constrained. Partial records of these evolutionary steps are preserved in the genomes of organisms phylogenetically placed between non-photosynthetic Melainabacteria, crown-group Cyanobacteria, and Gloeobacter, representing the earliest-branching Cyanobacteria capable of oxygenic photosynthesis. Here, we describe nearly complete, metagenome assembled genomes of an uncultured organism phylogenetically placed between the Melainabacteria and crown-group Cyanobacteria, for which we propose the name Candidatus Aurora vandensis {au.rora Latin noun dawn and vand.ensis, originating from Vanda}.The metagenome assembled genome of A. vandensis contains homologs of most genes necessary for oxygenic photosynthesis including key reaction center proteins. Many extrinsic proteins associated with the photosystems in other species are, however, missing or poorly conserved. The assembled genome also lacks homologs of genes associated with the pigments phycocyanoerethrin, phycoeretherin and several structural parts of the phycobilisome. Based on the content of the genome, we propose an evolutionary model for increasing efficiency of oxygenic photosynthesis through the evolution of extrinsic proteins to stabilize photosystem II and I reaction centers and improve photon capture. This model suggests that the evolution of oxygenic photosynthesis may have significantly preceded oxidation of Earth’s atmosphere due to low net oxygen production by early Cyanobacteria.