Role of nitrogen oxides in the metabolism of ammonia-oxidizing bacteria

Kampschreur, Marlies J.; Tan, N.C.G.; Picioreanu, Cristian; Jetten, Mike S. M.; Schmidt, Ingo; Loosdrecht, M.C.M. van

doi:10.1042/bst0340179

Cited by 30 publications

(11 citation statements)

References 16 publications

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“…However, the proportion of NH 3 -N that accumulates as NO-N remains unknown in this study. Previous work showed that NH 3 -N can be directed to NO production, especially during IC limitation, which further supports our hypothesis (6,(40)(41)(42). Our gene expression data are in contrast with those in the previous study by Jiang et al (6), who showed increased expression of rh50, amo, and hao by qPCR, but these differences may be reflections of a different medium and different growth conditions in their study (6).…”

Section: Nitrosomonas Europaea Physiology Under Limiting Carboncontrasting

confidence: 57%

Steady-State Growth under Inorganic Carbon Limitation Conditions Increases Energy Consumption for Maintenance and Enhances Nitrous Oxide Production in Nitrosomonas europaea

Mellbye

Giguere

Chaplen

et al. 2016

Appl Environ Microbiol

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Nitrosomonas europaea is a chemolithoautotrophic bacterium that oxidizes ammonia (NH 3 ) to obtain energy for growth on carbon dioxide (CO 2 ) and can also produce nitrous oxide (N 2 O), a greenhouse gas. We interrogated the growth, physiological, and transcriptome responses of N. europaea to conditions of replete (>5.2 mM) and limited inorganic carbon (IC) provided by either 1.0 mM or 0.2 mM sodium carbonate (Na 2 CO 3 ) supplemented with atmospheric CO 2 . IC-limited cultures oxidized 25 to 58% of available NH 3 to nitrite, depending on the dilution rate and Na 2 CO 3 concentration. IC limitation resulted in a 2.3-fold increase in cellular maintenance energy requirements compared to those for NH 3 -limited cultures. Rates of N 2 O production increased 2.5-and 6.3-fold under the two IC-limited conditions, increasing the percentage of oxidized NH 3 -N that was transformed to N 2 O-N from 0.5% (replete) up to 4.4% (0.2 mM Na 2 CO 3 ). Transcriptome analysis showed differential expression (P < 0.05) of 488 genes (20% of inventory) between replete and IC-limited conditions, but few differences were detected between the two IC-limiting treatments. IC-limited conditions resulted in a decreased expression of ammonium/ ammonia transporter and ammonia monooxygenase subunits and increased the expression of genes involved in C 1 metabolism, including the genes for RuBisCO (cbb gene cluster), carbonic anhydrase, folate-linked metabolism of C 1 moieties, and putative C salvage due to oxygenase activity of RuBisCO. Increased expression of nitrite reductase (gene cluster NE0924 to NE0927) correlated with increased production of N 2 O. Together, these data suggest that N. europaea adapts physiologically during IC-limited steady-state growth, which leads to the uncoupling of NH 3 oxidation from growth and increased N 2 O production. IMPORTANCENitrification, the aerobic oxidation of ammonia to nitrate via nitrite, is an important process in the global nitrogen cycle. This process is generally dependent on ammonia-oxidizing microorganisms and nitrite-oxidizing bacteria. Most nitrifiers are chemolithoautotrophs that fix inorganic carbon (CO 2 ) for growth. Here, we investigate how inorganic carbon limitation modifies the physiology and transcriptome of Nitrosomonas europaea, a model ammonia-oxidizing bacterium, and report on increased production of N 2 O, a potent greenhouse gas. This study, along with previous work, suggests that inorganic carbon limitation may be an important factor in controlling N 2 O emissions from nitrification in soils and wastewater treatment. During nitrification in aerobic environments, ammonia (NH 3 ) oxidation to nitrite (NO 2 Ϫ ) is initiated by ammonia-oxidizing bacteria (AOB) and archaea (1). These microorganisms are predominantly chemolithoautotrophs that derive energy for growth from NH 3 and meet their carbon (C) needs by fixing carbon dioxide (CO 2 ) (1). All known AOB fix CO 2 via the CalvinBenson-Bassham (CBB) cycle for growth, utilizing ribulose bisphosphate carboxylase/oxygenase (RuB...

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Section: Nitrosomonas Europaea Physiology Under Limiting Carboncontrasting

confidence: 57%

Steady-State Growth under Inorganic Carbon Limitation Conditions Increases Energy Consumption for Maintenance and Enhances Nitrous Oxide Production in Nitrosomonas europaea

Mellbye

Giguere

Chaplen

et al. 2016

Appl Environ Microbiol

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“…It is known that a large quantity of nitrous oxide (N 2 O) can be emitted during the process of biological denitrification if organic carbon is limited or during nitrification when oxygen is limited (Itokawa et al 2001;Kampschreur et al 2006). Recent studies showed that natural and artificial wetlands could be important emission sources of N 2 O (Wang et al 2006b;Søvik et al 2006).…”

Section: Potential Relationship To Nitrous Oxide (N 2 O) Emissionsmentioning

confidence: 99%

Potential roles of anaerobic ammonium and methane oxidation in the nitrogen cycle of wetland ecosystems

Zhu

Jetten

Kuschk

et al. 2010

Appl Microbiol Biotechnol

171

108

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Anaerobic ammonium oxidation (anammox) and anaerobic methane oxidation (ANME coupled to denitrification) with nitrite as electron acceptor are two of the most recent discoveries in the microbial nitrogen cycle. Currently the anammox process has been relatively well investigated in a number of natural and man-made ecosystems, while ANME coupled to denitrification has only been observed in a limited number of freshwater ecosystems. The ubiquitous presence of anammox bacteria in marine ecosystems has changed our knowledge of the global nitrogen cycle. Up to 50% of N 2 production in marine sediments and oxygendepleted zones may be attributed to anammox bacteria. However, there are only few indications of anammox in natural and constructed freshwater wetlands. In this paper, the potential role of anammox and denitrifying methanotrophic bacteria in natural and artificial wetlands is discussed in relation to global warming. The focus of the review is to explore and analyze if suitable environmental conditions exist for anammox and denitrifying methanotrophic bacteria in nitrogen-rich freshwater wetlands.

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“…Classically, ammonia oxidizers are known to use oxygen (i) for the oxidation of NH 3 to hydroxylamine (NH 2 OH) and (ii) as terminal electron acceptor in their electron transport chain. For oxidizing NH 3 , dinitrogen tetroxide (N 2 O 4 ), rather than O 2 , has been proposed to be the primary oxidant, as described in the NO x cycle hypothesis (Schmidt et al, 2001;Kampschreur et al, 2006;Schmidt, 2008) in which NO is an important intermediate: NO produced by NO 2 À reduction can feed into the NO x cycle and the nitrite reductase is thereby indirectly involved in ammonia oxidation. This is supported by lower growth yield and growth defects (Schmidt et al, 2004) and slower ammonia oxidation rate (Cantera and Stein, 2007a) in Nitrosomonas europaea nirK mutants.…”

Section: Introductionmentioning

confidence: 99%

Diversity, abundance and expression of nitrite reductase (nirK)-like genes in marine thaumarchaea

2012

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Ammonia-oxidizing archaea (AOA) are widespread and abundant in aquatic and terrestrial habitats and appear to have a significant impact on the global nitrogen cycle. Like the ammonia-oxidizing bacteria, AOA encode a gene homologous to copper-containing nitrite reductases (nirK), which has been studied very little to date. In this study, the diversity, abundance and expression of thaumarchaeal nirK genes from coastal and marine environments were investigated using two mutually excluding primer pairs, which amplify the nirK variants designated as AnirKa and AnirKb. Only the AnirKa variant could be detected in sediment samples from San Francisco Bay and these sequences grouped with the nirK from Candidatus Nitrosopumilus maritimus and Candidatus Nitrosoarchaeum limnia. The two nirK variants had contrasting distributions in the water column in Monterey Bay and the California Current. AnirKa was more abundant in the epi- to mesopelagic Monterey Bay water column, whereas AnirKb was more abundant in the meso- to bathypelagic California Current water. The abundance and community composition of AnirKb, but not AnirKa, followed that of thaumarchaeal amoA, suggesting that either AnirKa is not exclusively associated with AOA or that commonly used amoA primers may be missing a significant fraction of AOA diversity in the epipelagic. Interestingly, thaumarchaeal nirK was expressed 10–100-fold more than amoA in Monterey Bay. Overall, this study provides valuable new insights into the distribution, diversity, abundance and expression of this alternative molecular marker for AOA in the ocean.

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Role of nitrogen oxides in the metabolism of ammonia-oxidizing bacteria

Cited by 30 publications

References 16 publications

Steady-State Growth under Inorganic Carbon Limitation Conditions Increases Energy Consumption for Maintenance and Enhances Nitrous Oxide Production in Nitrosomonas europaea

Steady-State Growth under Inorganic Carbon Limitation Conditions Increases Energy Consumption for Maintenance and Enhances Nitrous Oxide Production in Nitrosomonas europaea

Potential roles of anaerobic ammonium and methane oxidation in the nitrogen cycle of wetland ecosystems

Diversity, abundance and expression of nitrite reductase (nirK)-like genes in marine thaumarchaea

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