Nitric oxide preferentially inhibits nitrite oxidizing communities with high affinity for nitrite

Courtens, Emilie; Clippeleir, Haydée De; Vlaeminck, Siegfried E.; Jordaens, Robin; Park, Hongkeun; Chandran, Kartik; Boon, Nico

doi:10.1016/j.jbiotec.2014.11.021

Cited by 29 publications

(8 citation statements)

References 11 publications

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“…4). To our knowledge, NO production in Nitrospira has not been investigated previously but previous work has shown that NO (65 nM NO in the liquid phase) inhibits NO 2 − oxidation to NO 3 − in Nitrospira dominated sludge 55 . The more distantly related proteobacterial nitrite-oxidizer, Nitrobacter winogradskyi produces 38 and consumes NO 36,38 in a NO 2 − -dependent manner during normal aerobic growth.…”

Section: Resultsmentioning

confidence: 98%

Low yield and abiotic origin of N2O formed by the complete nitrifier Nitrospira inopinata

et al. 2019

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Nitrous oxide (N 2 O) and nitric oxide (NO) are atmospheric trace gases that contribute to climate change and affect stratospheric and ground-level ozone concentrations. Ammonia oxidizing bacteria (AOB) and archaea (AOA) are key players in the nitrogen cycle and major producers of N 2 O and NO globally. However, nothing is known about N 2 O and NO production by the recently discovered and widely distributed complete ammonia oxidizers (comammox). Here, we show that the comammox bacterium Nitrospira inopinata is sensitive to inhibition by an NO scavenger, cannot denitrify to N 2 O, and emits N 2 O at levels that are comparable to AOA but much lower than AOB. Furthermore, we demonstrate that N 2 O formed by N. inopinata formed under varying oxygen regimes originates from abiotic conversion of hydroxylamine. Our findings indicate that comammox microbes may produce less N 2 O during nitrification than AOB.

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Section: Resultsmentioning

confidence: 98%

Low yield and abiotic origin of N2O formed by the complete nitrifier Nitrospira inopinata

et al. 2019

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“…As a result, in a complete mixed nitrifying culture diffusion of NO from AOB to NOB would be rapid, therefore enabling mutualistic NO oxidation by NOB. In addition, as NO is cytotoxic (Richardson et al, ) and may inhibit nitrite oxidation by NOB (Courtens et al, ), therefore it is possible that survival may require detoxification by these organisms via production enzymes to actively reduce or oxidize NO. Therefore, the occurrence of NO oxidation reactions in AOB and NOB would provide an advantage by extracting electron equivalents while reducing toxic damage by this molecule.…”

Section: Resultsmentioning

confidence: 99%

“…would be better at mitigating N 2 O emission during ammonium oxidation to nitrate; the presence of genes encoding for NirK and Cyt P460 in their genomes suggests that this genus can catalyse more diverse reactions for oxidizing NO to NO 2 − . Indeed, Courtens et al () showed that NO 2 − oxidization in sludge dominated by Nitrobacter spp. shows lower inhibition by NO in comparison to Nitrospira spp.…”

Section: Resultsmentioning

confidence: 99%

Assessment of nitric oxide (NO) redox reactions contribution to nitrous oxide (N₂O) formation during nitrification using a multispecies metabolic network model

Perez-Garcia

Chandran

Villas‐Bôas

et al. 2015

Biotech & Bioengineering

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Over the coming decades nitrous oxide (N2O) is expected to become a dominant greenhouse gas and atmospheric ozone depleting substance. In wastewater treatment systems, N2O is majorly produced by nitrifying microbes through biochemical reduction of nitrite (NO2(-)) and nitric oxide (NO). However it is unknown if the amount of N2O formed is affected by alternative NO redox reactions catalyzed by oxidative nitrite oxidoreductase (NirK), cytochromes (i.e., P460 [CytP460] and 554 [Cyt554 ]) and flavohemoglobins (Hmp) in ammonia- and nitrite-oxidizing bacteria (AOB and NOB, respectively). In this study, a mathematical model is developed to assess how N2O formation is affected by such alternative nitrogen redox transformations. The developed multispecies metabolic network model captures the nitrogen respiratory pathways inferred from genomes of eight AOB and NOB species. The performance of model variants, obtained as different combinations of active NO redox reactions, was assessed against nine experimental datasets for nitrifying cultures producing N2O at different concentration of electron donor and acceptor. Model predicted metabolic fluxes show that only variants that included NO oxidation to NO2(-) by CytP460 and Hmp in AOB gave statistically similar estimates to observed production rates of N2O, NO, NO2(-) and nitrate (NO3(-)), together with fractions of AOB and NOB species in biomass. Simulations showed that NO oxidation to NO2(-) decreased N2O formation by 60% without changing culture's NO2(-) production rate. Model variants including NO reduction to N2O by Cyt554 and cNor in NOB did not improve the accuracy of experimental datasets estimates, suggesting null N2O production by NOB during nitrification. Finally, the analysis shows that in nitrifying cultures transitioning from dissolved oxygen levels above 3.8 ± 0.38 to <1.5 ± 0.8 mg/L, NOB cells can oxidize the NO produced by AOB through reactions catalyzed by oxidative NirK.

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“…Anammox bacteria thrive at oxic–anoxic interfaces because of their dependence on

{NO}_{2}^{‐}

production by AOB or AOA (Thamdrup, 2012). Anammox and NOB compete for

{NO}_{2}^{‐}

in the 0.1–1 mg N L –1 range, and this is especially true for Nitrospira NOB, which share a homologous form of the key enzyme catalyzing

{NO}_{2}^{‐}

oxidation with anammox (Ali et al, 2018; Courtens et al, 2015; Lücker et al, 2010; Maixner et al, 2006; Zhang et al, 2017). Recently, an N‐cycling enrichment culture revealed comammox bacteria co‐occurring with anammox bacteria in the genus Candidatus Brocadia, presumably enhanced by the ability of comammox organisms to oxidize NH 3 in low oxygen conditions (<3.1 µM) (van Kessel et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Impacts of ammonia loading and biofilm age on the prevalence of nitrogen‐cycling microorganisms in a full‐scale submerged attached‐growth reactor

Zhao

Vermace

Mattes

et al. 2020

Water Environment Research

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This study reports the impacts of seasonal ammonia load changes and biofilm age on the quantity of biomass and on the prevalence of ammonia‐ and nitrite‐metabolizing organisms within a submerged attached‐growth reactor (SAGR™) following lagoon treatment. Ammonia (NH3) loadings (0.12–3.17 kg/d) in the primary SAGR were measured over 223 days from May to December in 2017. Adjustment of the wastewater flow path on September 1 successfully increased NH3 loading to the primary SAGR, which subsequently caused reactor biomass to increase. The NH3 removal rate in October (0.5 kg/d) was greater than rates in June and July (0.3 and 0.2 kg/d) despite a water temperature decrease from >24 to 15.6°C. This elevated removal rate in October, and the sustained removal rate in December (0.4 kg/d, 5.3°C) were associated with a measured increase in microbial biomass. The relative abundance of the anammox organism C. Brocadia was 5 times greater in the mature biofilm after 686 days of growth, and the genus Pseudomonas increased sevenfold. The presence of Pseudomonas, which contains denitrifying species, and anammox suggests a high potential for removal of total nitrogen in SAGRs. Practitioner points Pseudomonas prevalence and the presence of anammox suggest a high potential for total nitrogen removal in mature SAGR biofilms. The abundance of the anammox microorganism C. Brocadia was greater after 686 days of biofilm growth compared with 33 days. Simple operational changes can increase biomass in the SAGR to maintain, or even increase, NH3 transformation rates during cold weather.

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Nitric oxide preferentially inhibits nitrite oxidizing communities with high affinity for nitrite

Cited by 29 publications

References 11 publications

Low yield and abiotic origin of N2O formed by the complete nitrifier Nitrospira inopinata

Low yield and abiotic origin of N2O formed by the complete nitrifier Nitrospira inopinata

Assessment of nitric oxide (NO) redox reactions contribution to nitrous oxide (N₂O) formation during nitrification using a multispecies metabolic network model

Impacts of ammonia loading and biofilm age on the prevalence of nitrogen‐cycling microorganisms in a full‐scale submerged attached‐growth reactor

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Nitric oxide preferentially inhibits nitrite oxidizing communities with high affinity for nitrite

Cited by 29 publications

References 11 publications

Low yield and abiotic origin of N2O formed by the complete nitrifier Nitrospira inopinata

Low yield and abiotic origin of N2O formed by the complete nitrifier Nitrospira inopinata

Assessment of nitric oxide (NO) redox reactions contribution to nitrous oxide (N2O) formation during nitrification using a multispecies metabolic network model

Impacts of ammonia loading and biofilm age on the prevalence of nitrogen‐cycling microorganisms in a full‐scale submerged attached‐growth reactor

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Assessment of nitric oxide (NO) redox reactions contribution to nitrous oxide (N₂O) formation during nitrification using a multispecies metabolic network model