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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.

SUBMITTER: Hemp J

PROVIDER: S-EPMC5113846 | biostudies-literature | 2016 Nov

REPOSITORIES: biostudies-literature

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

Hemp James J Lücker Sebastian S Schott Joachim J Pace Laura A LA Johnson Jena E JE Schink Bernhard B Daims Holger H Fischer Woodward W WW

The ISME journal 20160419 11

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 ha ...[more]

PMID: 27093047

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Project description:Nitrification is an important biological link between oxidized and reduced forms of nitrogen (N). The efficiency of nitrification plays a key role in mitigating excess N in eutrophic systems, including those with cyanobacterial harmful algal blooms (cyanoHABs), since it can be closely coupled with denitrification and removal of excess N. Recent work suggests that competition for ammonium (NH4 +) between ammonia oxidizers and cyanoHABs can help determine microbial community structure. Nitrification rates and ammonia-oxidizing archaeal (AOA) and bacterial (AOB) community composition and gene abundances were quantified in Lake Okeechobee and St. Lucie Estuary in southern Florida (United States). We sampled during cyanobacterial (Microcystis) blooms in July 2016 and August 2017 (2 weeks before Hurricane Irma) and 10 days after Hurricane Irma made landfall. Nitrification rates were low during cyanobacterial blooms in Lake Okeechobee and St. Lucie Estuary, while low bloom conditions in St. Lucie Estuary coincided with greater nitrification rates. Nitrification rates in the lake were correlated (R 2 = 0.94; p = 0.006) with AOA amoA abundance. Following the hurricane, nitrification rates increased by an order of magnitude, suggesting that nitrifiers outcompeted cyanobacteria for NH4 + under turbid, poor light conditions. After Irma, AOA and AOB abundances increased in St. Lucie Estuary, while only AOB increased in Lake Okeechobee. AOA sequences clustered into three major lineages: Nitrosopumilales (NP), Nitrososphaerales (NS), and Nitrosotaleales (NT). Many of the lake OTUs placed within the uncultured and uncharacterized NS δ and NT β clades, suggesting that these taxa are ecologically important along this eutrophic, lacustrine to estuarine continuum. After the hurricane, the AOA community shifted toward dominance by freshwater clades in St. Lucie Estuary and terrestrial genera in Lake Okeechobee, likely due to high rainfall and subsequent increased turbidity and freshwater loading from the lake into the estuary. AOB community structure was not affected by the disturbance. AOA communities were consistently more diverse than AOB, despite fewer sequences recovered, including new, unclassified, eutrophic ecotypes, suggesting a wider ecological biogeography than the oligotrophic niche originally posited. These results and other recent reports contradict the early hypothesis that AOB dominate ammonia oxidation in high-nutrient or terrestrial-influenced systems.

Dataset Information

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

Publications

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

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