Nitrification expanded: discovery, physiology and genomics of a nitrite-oxidizing bacterium from the phylum <i>Chloroflexi</i>

Sorokin, D. Yu.; Lücker, Sebastian; Vejmelková, Dana; Kostrikina, N. A.; Kleerebezem, Robbert; Rijpstra, W. Irene C.; Damsté, Jaap Sinninghe; Paslier, Denis Le; Muyzer, Gerard; Wagner, Michael; Loosdrecht, M.C.M. van; Daims, Holger

doi:10.1038/ismej.2012.70

Cited by 317 publications

(237 citation statements)

References 60 publications

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“…Nitrospina and Nitrospira with NXRs oriented towards the periplasm are more competitive at lower nitrite concentrations than Nitrobacter and Nitrococcus with cytoplasmically oriented NXRs (Sorokin et al 2012). The higher efficiency of periplasmic NXR conserves more energy per oxidized nitrite molecule.…”

Section: Inverse Kinetic Isotope Effects During Nitrite Oxidationmentioning

confidence: 96%

“…In cytoplasmically oriented NXR (Nitrobacter and Nitrococcus), transporters shuttle nitrite into and nitrate out of the cell (Spieck et al 1996, Starkenburg et al 2006, Sorokin et al 2012) to avoid accumulation of nitrate in the cell and potential unfavourable conditions. This transport can potentially be a bottleneck for oxidation, depending on the substrate affinity and activity of the transporter (Daims et al 2016).…”

Section: Inverse Kinetic Isotope Effects During Nitrite Oxidationmentioning

confidence: 99%

“…Nitrobacter (Winogradsky 1892, Woese et al 1984), Nitrococcus (Watson & Waterbury 1971, Woese et al 1985, and Nitrotoga (Alawi et al 2007) belong to the Alpha-, Gamma-or Betaproteobacteria, and Nitrolancea (Sorokin et al 2012) is a member of the phylum Chloroflexi.…”

Section: Introductionmentioning

confidence: 99%

“…NXR is a membrane-bound enzyme associated with the cytoplasmic membrane, and consists of 3 subunits: the catalytical NxrA, the electron-chanelling NxrB, and a putative NxrC as membrane anchor (Sundermeyer-Klinger et al 1984, Lücker et al 2010. The substrate-binding NxrA subunit faces the periplasmic space in Nitrospina , Lücker et al 2013 and Nitrospira (Spieck et al 1998, Lücker et al 2010, but is oriented towards the cytoplasm in Nitrobacter, Nitrococcus, and Nitrolancea (Spieck et al 1996, Sorokin et al 2012.…”

Section: Introductionmentioning

confidence: 99%

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Oxidation kinetics and inverse isotope effect of marine nitrite-oxidizing isolates

Jacob¹,

Nowka²,

Merten³

et al. 2017

Aquat. Microb. Ecol.

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Nitrification, the step-wise oxidation of ammonium to nitrite and nitrate, is important in the marine environment because it produces nitrate, the most abundant marine dissolved inorganic nitrogen (DIN) component and N-source for phytoplankton and microbes. This study focused on the second step of nitrification, which is carried out by a distinct group of organisms, nitrite-oxidizing bacteria (NOB). The growth of NOB is characterized by nitrite oxidation kinetics, which we investigated for 4 pure cultures of marine NOB (Nitrospina watsonii 347, Nitrospira sp. Ecomares 2.1, Nitrococcus mobilis 231, and Nitrobacter sp. 311). We further compared the kinetics to those of non-marine species because substrate concentrations in marine environments are comparatively low, which likely influences kinetics and highlights the importance of this study. We also determined the isotope effect during nitrite oxidation of a pure culture of Nitrospina (Nitrospina watsonii 347) belonging to one of the most abundant marine NOB genera, and for a Nitrospira strain (Nitrospira sp. Ecomares 2.1). The enzyme kinetics of nitrite oxidation, described by Michaelis-Menten kinetics, of 4 marine genera are rather narrow and fall in the low end of halfsaturation constant (K m ) values reported so far, which span over 3 orders of magnitude between 9 and >1000 μM NO 2 − . Nitrospina has the lowest K m (19 μM NO 2 − ), followed by Nitrobacter (28 μM NO 2 − ), Nitrospira (54 μM NO 2 − ), and Nitrococcus (120 μM NO 2 − ). The isotope effects during nitrite oxidation by Nitrospina watsonii 347 and Nitrospira sp. Ecomares 2.1 were 9.7 ± 0.8 and 10.2 ± 0.9 ‰, respectively. This confirms the inverse isotope effect of NOB described in other studies; however, it is at the lower end of reported isotope effects. We speculate that differences in isotope effects reflect distinct nitrite oxidoreductase (NXR) enzyme orientations.

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Section: Inverse Kinetic Isotope Effects During Nitrite Oxidationmentioning

confidence: 96%

Section: Inverse Kinetic Isotope Effects During Nitrite Oxidationmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Oxidation kinetics and inverse isotope effect of marine nitrite-oxidizing isolates

Jacob¹,

Nowka²,

Merten³

et al. 2017

Aquat. Microb. Ecol.

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“…In addition to the importance of activated sludge in modern sanitation, these systems are uniquely suited for whole-ecosystem scale experimentation due to the tight controls on chemical, physical and biological processes (Daims et al, 2006). As a model system for microbial ecology, research on activated sludge has greatly informed our understanding of microbe-microbe interactions (Wagner ,2002;Daims et al, 2006;Maixner et al, 2006), undiscovered biochemistry (Strous et al, 2006;Maixner et al, 2008;Lü cker et al, 2010;He and McMahon, 2011;Sorokin et al, 2012) and community assembly theory (Sloan et al, 2007;Ofiteru et al, 2010). However, little work has focused on the ecological consequences of press (that is, prolonged) disturbances on microbial diversity and the extent of compositional versus environmental effects on ecosystem function (Allison and Martiny, 2008).…”

Section: Introductionmentioning

confidence: 99%

Disturbance and temporal partitioning of the activated sludge metacommunity

et al. 2014

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The resilience of microbial communities to press disturbances and whether ecosystem function is governed by microbial composition or by the environment have not been empirically tested. To address these issues, a whole-ecosystem manipulation was performed in a full-scale activated sludge wastewater treatment plant. The parameter solids retention time (SRT) was used to manipulate microbial composition, which started at 30 days, then decreased to 12 and 3 days, before operation was restored to starting conditions (30-day SRT). Activated sludge samples were collected throughout the 313-day time series in parallel with bioreactor performance ('ecosystem function'). Bacterial small subunit (SSU) rRNA genes were surveyed from sludge samples resulting in a sequence library of 4417 000 SSU rRNA genes. A shift in community composition was observed for 12-and 3-day SRTs. The composition was altered such that r-strategists were enriched in the system during the 3-day SRT, whereas K-strategists were only present at SRTsX12 days. This shift corresponded to loss of ecosystem functions (nitrification, denitrification and biological phosphorus removal) for SRTsp12 days. Upon return to a 30-day SRT, complete recovery of the bioreactor performance was observed after 54 days despite an incomplete recovery of bacterial diversity. In addition, a different, yet phylogenetically related, community with fewer of its original rare members displaced the pre-disturbance community. Our results support the hypothesis that microbial ecosystems harbor functionally redundant phylotypes with regard to general ecosystem functions (carbon oxidation, nitrification, denitrification and phosphorus accumulation). However, the impacts of decreased rare phylotype membership on ecosystem stability and micropollutant removal remain unknown.

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Nitrification

Stein

Nicol

2018

Encyclopedia of Life Sciences

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The global nitrogen cycle is initiated by the fixation of atmospheric N 2 , by either natural or chemical processes, to bioavailable ammonium (NH 4 + ). Nitrification is the oxidative process that transforms this ammonium to nitrate, via a nitrite intermediate. Nitrification is performed solely by microorganisms: ammonia‐oxidising bacteria and archaea oxidise ammonia to nitrite, nitrite‐oxidising bacteria oxidise nitrite to nitrate and comammox bacteria oxidise ammonia to nitrate. Nitrifiers (and anammox) are distinguished from other microorganisms as they can grow solely from the oxidation of inorganic nitrogenous molecules and fix carbon dioxide as their sole carbon source, although many can also grow using alternative catabolic processes, by cross‐feeding, and/or by mixotrophy. Key enzymes to the nitrification process include ammonia monooxygenase, hydroxylamine dehydrogenase and nitrite oxidoreductase. A putative enzyme catalysing nitric oxide oxidation to nitrite is currently uncharacterised. Essential intermediates to nitrification include hydroxylamine, nitric oxide and nitrite. As well as performing a required component of the global nitrogen cycle, nitrifying microorganisms are also responsible for the loss of nitrogen‐based fertilisers in soil and play a critical role in emission of the potent greenhouse gas, nitrous oxide, as mediated by production and consumption of nitric oxide in their metabolism. Key Concepts Nitrification is an oxidative process that transforms reduced nitrogen, primarily ammonia, to nitrate. Fluxes in nitrogen transformations associated with nitrification activity have accelerated greatly over the past century owing to the production and application of inorganic ammonium‐based fertilisers. Microorganisms involved in nitrification are ubiquitously distributed in nature and found virtually everywhere that ammonia and oxygen are present. Nitrification is mediated by bacteria and archaea and is performed by either two (ammonia and nitrite oxidisers) or one (comammox) canonical functional group. Autotrophic pathways of ammonia‐ and nitrite‐oxidising bacteria are the Calvin cycle or reverse TCA cycle; ammonia‐oxidising archaea assimilate carbon dioxide via the 3‐hydroxypropionate/4‐hydroxybutyrate pathway. Key enzymes of nitrification are ammonia monooxygenase, hydroxylamine dehydrogenase, nitric oxide oxidase (putative) and nitrite oxidoreductase. Methanotrophic and heterotrophic microorganisms can carry out parts of nitrification but cannot grow from oxidising reduced nitrogen compounds. Mechanisms for the production of nitric oxide and nitrous oxide are distinct among nitrifying microorganisms. Comparative genome analysis and the use of differential inhibitors can assist in determining differences in physiology and niche preference among nitrifying microorganisms. There is substantial physiological diversity within individual functional groups (e.g. ammonia oxidisers) which results in niche differentiation both within and between taxonomic groups of nitrifiers.

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Nitrification expanded: discovery, physiology and genomics of a nitrite-oxidizing bacterium from the phylum Chloroflexi

Cited by 317 publications

References 60 publications

Oxidation kinetics and inverse isotope effect of marine nitrite-oxidizing isolates

Oxidation kinetics and inverse isotope effect of marine nitrite-oxidizing isolates

Disturbance and temporal partitioning of the activated sludge metacommunity

Nitrification

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