Origin of oxygenic photosynthesis from Anoxygenic type I and type II reaction centers

Abstract

All anoxygenic photosynthetic bacteria currently known have photosynthetic reaction centers of only one type, either type I or II. In contrast, all oxygenic photosynthetic systems-of plants, algae, and cyanobacteria-have both type I and type II reaction centers. Molecular oxygen is the oxidation product of water in a type II reaction center that is connected, in series, with a type I reaction center. Around 2.4 billion years ago, the evolutionary origin of this series connection initiated biological water oxidation and began to transform our planet irrevocably. Here I consider the question of how separate type I and type II reaction centers diverged from a common ancestor. How they later became linked together, to become interdependent, is also considered, and an answer proposed. The "redox switch hypothesis" for the first cyanobacterium envisages an evolutionary precursor in which type I and type II reaction center genes are present in the genome of a single anoxygenic bacterial lineage, but never expressed at the same time, their gene products forming different reaction centers for light energy conversion under different growth conditions. I suggest that mutation disrupting redox control allowed these two reaction centers to coexist-an arrangement selected against prior to the acquisition of a catalyst of water oxidation while having a selective advantage thereafter. Predictions of this hypothesis include a modern, anoxygenic descendent of the proto-cyanobacterium whose disabled redox switch triggered the Great Oxidation Event, transforming both biology and Earth's surface geochemistry.