Photosynthesis Has Been Established Only Once—Evolution of Photosynthetic Reaction Center Proteins and Bacteriochlorophyll Biosynthesis

The first forms of photosynthetic life date back to more than 3.2-3.5 billion years ago. They performed photosynthesis in an anoxic world of the early earth and formed large mass accumulations on any kind of surface and in shallow waters. During evolution they diverged into several major phyla with differences in structure and function of the photosynthetic machinery including two different types of photosynthetic reaction centers. The combination of both of these types eventually led to the establishment of oxygenic photosynthesis present in cyanobacteria and chloroplast-containing plants. Common to all photosynthetic life is the presence of phylogenetically related reaction center proteins and of various chlorophyll molecules as mediators of light energy transformation into biochemical forms of energy. Therefore, we used phylogenetic analyses of reaction center proteins and representative enzymes of (bacterio)chlorophyll biosynthesis in addition to synteny of genome organization to unravel early divergencies of all known phyla of photosynthetic prokaryotes: Cyanobacteria, Chloroflexi, Chlorobi, Heliobacteria, Chloracidobacteria, and phototrophic purple Proteobacteria including <i>Gemmatimonas</i>. It was concluded that photosynthesis evolved only once, and all known forms diverged by various mechanisms from one primordial principal ancestor with properties resembling an ancestral cyanobacterium driving anoxygenic photosynthesis with a Type I photosystem and reduced inorganic electron donors.