Genomics of a phototrophic nitrite oxidizer: insights into the evolution of photosynthesis and nitrification.
Oxygenic photosynthesis evolved from anoxygenic ancestors before the rise of oxygen ~2.32 billion years ago; however, 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 simpler redox chemistry, such as nitrite or Mn. To determine whether nitrite could have had a role in the transition to high-potential phototrophy, we sequenced and analyzed the genome of Thiocapsa KS1, a Gammaproteobacteria capable of anoxygenic phototrophic nitrite oxidation. The genome revealed a high metabolic flexibility, which likely allows Thiocapsa KS1 to colonize a great variety of habitats and to persist under fluctuating environmental conditions. We demonstrate that Thiocapsa KS1 does not utilize a high-potential reaction center for phototrophic nitrite oxidation, which suggests that this type of phototrophic nitrite oxidation did not drive the evolution of high-potential phototrophy. In addition, phylogenetic and biochemical analyses of the nitrite oxidoreductase (NXR) from Thiocapsa KS1 illuminate a complex evolutionary history of nitrite oxidation. Our results indicate that the NXR in Thiocapsa originates from a different nitrate reductase clade than the NXRs in chemolithotrophic nitrite oxidizers, suggesting that multiple evolutionary trajectories led to modern nitrite-oxidizing bacteria.
Department of Geological and Planetary Sciences, California Institute of Technology, Pasadena, CA, USA.
James
J
Hemp
Department of Microbiology, Radboud University Nijmegen, Nijmegen, The Netherlands.|Division of Microbial Ecology, Department of Microbiology and Ecosystem Research, University of Vienna, Vienna, Austria.
Sebastian
S
Lücker
Division of Microbial Ecology, Department of Biology, University of Konstanz, Konstanz, Germany.
Joachim
J
Schott
Division of Gastroenterology, Department of Medicine, University of California, San Diego, La Jolla, CA, USA.
Laura A
LA
Pace
Department of Geological and Planetary Sciences, California Institute of Technology, Pasadena, CA, USA.
Jena E
JE
Johnson
Division of Microbial Ecology, Department of Biology, University of Konstanz, Konstanz, Germany.
Bernhard
B
Schink
Division of Microbial Ecology, Department of Microbiology and Ecosystem Research, University of Vienna, Vienna, Austria.
Holger
H
Daims
Department of Geological and Planetary Sciences, California Institute of Technology, Pasadena, CA, USA.
Woodward W
WW
Fischer
D001419:Bacteria / Q000201:enzymology / Q000235:genetics / Q000302:isolation & purification / Q000378:metabolism*; D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism; D019143:Evolution, Molecular; D016680:Genome, Bacterial; D023281:Genomics; D058465:Nitrification; D009572:Nitrite Reductases / Q000235:genetics / Q000378:metabolism; D009573:Nitrites / Q000378:metabolism*; D010084:Oxidation-Reduction; D010088:Oxidoreductases / Q000235:genetics / Q000378:metabolism; D010788:Photosynthesis; D052817:Phototrophic Processes; D010802:Phylogeny
D001426:Bacterial Proteins; D009573:Nitrites; D010088:Oxidoreductases; D009572:Nitrite Reductases; C048879:nitrite dehydrogenase