Genomic Characterization of a Phototrophic Nitrite Oxidizer: Insights into the Evolution of Oxygenic Photosynthesis and Nitrification. Thiocapsa sp. KS1 draft genome sequence

Oxygenic photosynthesis evolved from anoxygenic ancestors before the rise of oxygen around 2.32 Ga, but little is known about this transition. A high redox potential reaction center is a prerequisite for the evolution of the water-oxidizing complex of photosystem II. Therefore it is likely that high-potential phototrophy originally evolved to oxidize alternative electron donors that utilized a simpler redox chemistry, such as nitrite or Mn. To determine whether nitrite could have played a role in the transition to high-potential phototrophy we sequenced and analyzed the genome of Thiocapsa KS1, a physiologically highly versatile gammaproteobacterium capable of anoxygenic phototrophic nitrite oxidation. We demonstrate that Thiocapsa KS1 does not utilize a high potential reaction center, eliminating nitrite as an intermediate in the evolution of high potential phototrophy. Additional analyses of the ancestral features of photosystem II strongly suggest that direct Mn2+ oxidation was the key intermediate in the evolution of oxygenic photosynthesis. Moreover, phylogenetic and biochemical analyses of the nitrite oxidoreductase (NXR) from Thiocapsa KS1 illuminate the complex evolutionary history of nitrification. Our results show that the NXR in Thiocapsa evolved from nitrite reductases independently of those in chemolithotrophic nitrite oxidizers. This suggests that at least three evolutionary trajectories led to the modern nitrite oxidizing bacteria.