Genomics of a phototrophic nitrite oxidizer: insights into the evolution of photosynthesis and nitrification

Abstract

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.

Genomic profiling of four cultivated Candidatus Nitrotoga spp. predicts broad metabolic potential and environmental distribution

“…The deeply branching Ca. Nitrotoga NxrA protein sequences may represent a fourth evolutionary development of nitrite oxidation, separate from the cytoplasmic-facing, periplasmic-facing, and phototrophic Thiocapsa nitrite oxidizers [50,66]. Interestingly, some contigs surrounding the Ca.…”

“…Nitrotoga genomes (see below). Organisms possessing cbb 3 -type oxidases, including the NOB Nitrospina gracilis and the phototrophic nitrite-oxidizer Thiocapsa KS1, are likely capable of growth in microoxic environments [49,66,82]. For instance, Nitrospina-like bacteria have been found to play a crucial role in carbon fixation in marine oxygen minimum zones, due in part to their cbb3type terminal oxidases [11,83,84].…”

“…PTS genes were also found in Nitrobacter winogradskyi and Thiocapsa sp. KS1 [65,66]. Genes encoding the EI and HPr subunits of the PTS were both found in Ca.…”

An uncharacterized clade in the DMSO reductase family of molybdenum oxidoreductases is a new type of chlorate reductase

“…It is unclear whether the ability of Rhodoplanes species to perform both metabolisms is related. Another DMSO reductase family enzyme, nitrite oxidoreductase, enables the phototrophic oxidation of nitrite to nitrate by providing electrons to photosystem II (Griffin et al, 2007;Hemp et al, 2016). It is unlikely that chlorate and chlorite serve as electron donors for phototrophy, however, because the reduction potential of the half-couple reactions are higher than that of photosystem II (Hemp et al, 2016).…”

“…Another DMSO reductase family enzyme, nitrite oxidoreductase, enables the phototrophic oxidation of nitrite to nitrate by providing electrons to photosystem II (Griffin et al, 2007;Hemp et al, 2016). It is unlikely that chlorate and chlorite serve as electron donors for phototrophy, however, because the reduction potential of the half-couple reactions are higher than that of photosystem II (Hemp et al, 2016). Additionally, while some DMSO reductase family enzymes have been observed to perform both forward and reverse oxidoreductase activity, the enzyme Cld only performs the forward reaction of separating chlorite into chloride and oxygen, which would favour the reduction of perchlorate, chlorate and chlorite.…”