The importance of abiotic reactions for nitrous oxide production

Zhu‐Barker, Xia; Cavazos, Amanda R.; Ostrom, Nathaniel E.; Horwáth, William R.; Glass, Jennifer B.

doi:10.1007/s10533-015-0166-4

Cited by 186 publications

(184 citation statements)

References 127 publications

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“…AMO/Cu-MMO, ammonia monooxygenase; c552, cytochrome c redox carrier; CytS: cytochrome c'-beta (see Simon and Klotz, 2013, and references therein); HAO, hydroxylamine dehydrogenase; HCO, heme-copper oxidase; HURM, hydroxylamine:ubiquinone redox module (see Simon and Klotz, 2013, and references therein); NirK, Cu-containing NO-forming nitrite reductase; NOR, nitric oxide reductase; P460, tetraheme cytochrome c protein P460 (CytL; see Simon and Klotz, 2013, and references therein); pcy, plastocyanin; pmf, proton-motive force; Q/QH 2 , quinone/ quinol pool. (Zhu-Barker et al, 2015). Due to the relatively high abundance and activity of Thaumarchaea across terrestrial, freshwater, and marine environments (Zhang et al, 2010;Pratscher et al, 2011;French et al, 2012;Berg et al, 2015) and their established tolerance of low ammonium and oxygen environments (Martens-Habbena et al, 2009), their contributions to NOx emissions is likely of high global significance (Babbin et al, 2015).…”

Section: Resultsmentioning

confidence: 99%

“…Yet, control experiments to verify or falsify chemical formation of N 2 O facilitated by interaction of Thaumarchaeotal metabolites with components of the cultivation or incubation media or assay solutions remain absent from the literature. It should be noted that interactions of ammonia oxidation intermediates with iron, manganese, and organic compounds could generate substantial amounts of N 2 O under environmentally relevant conditions (Zhu-Barker et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

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Pathways and key intermediates required for obligate aerobic ammonia-dependent chemolithotrophy in bacteria and Thaumarchaeota

et al. 2016

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Chemolithotrophic ammonia-oxidizing bacteria and Thaumarchaeota are central players in the global nitrogen cycle. Obligate ammonia chemolithotrophy has been characterized for bacteria; however, large gaps remain in the Thaumarchaeotal pathway. Using batch growth experiments and instantaneous microrespirometry measurements of resting biomass, we show that the terrestrial Thaumarchaeon Nitrososphaera viennensis EN76 T exhibits tight control over production and consumption of nitric oxide (NO) during ammonia catabolism, unlike the ammonia-oxidizing bacterium Nitrosospira multiformis ATCC 25196 T . In particular, pulses of hydroxylamine into a microelectrode chamber as the sole substrate for N. viennensis resulted in iterative production and consumption of NO followed by conversion of hydroxylamine to nitrite. In support of these observations, oxidation of ammonia in growing cultures of N. viennensis, but not of N. multiformis, was inhibited by the NO-scavenger PTIO. When based on the marginal nitrous oxide (N 2 O) levels detected in cell-free media controls, the higher levels produced by N. multiformis were explained by enzyme activity, whereas N 2 O in N. viennensis cultures was attributed to abiotic reactions of released N-oxide intermediates with media components. Our results are conceptualized in a pathway for ammonia-dependent chemolithotrophy in Thaumarchaea, which identifies NO as an essential intermediate in the pathway and implements known biochemistry to be executed by a proposed but still elusive copper enzyme. Taken together, this work identifies differences in ammonia-dependent chemolithotrophy between bacteria and the Thaumarchaeota, advances a central catabolic role of NO only in the Thaumarchaeotal pathway and reveals stark differences in how the two microbial cohorts contribute to N 2 O emissions.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Pathways and key intermediates required for obligate aerobic ammonia-dependent chemolithotrophy in bacteria and Thaumarchaeota

et al. 2016

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“…Although biological N 2 O production has received much attention, abiotic production of N 2 O is also widely documented, typically via reactions involving intermediates such as NH 2 OH and NO 2 − —though its environmental role remains unclear (Zhu-Barker et al 11,. and references therein).…”

Section: Discussionmentioning

confidence: 99%

“…While yields of N 2 O from both AMO and bDNF are low (<1% in terms of total moles of N converted), their magnitude and ubiquity across ecosystems translates into major atmospheric fluxes. Increasingly, however, the potential for other N 2 O production processes has become apparent, including production of N 2 O by fungi and/or abiotic reactions coupled to redox cycling of metals such as iron101112. In particular, the organic-rich and redox-dynamic regimes of estuarine and coastal sediments may promote both fungal activity and rapid redox cycling of iron.…”

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confidence: 99%

Evidence for fungal and chemodenitrification based N2O flux from nitrogen impacted coastal sediments

et al. 2017

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Although increasing atmospheric nitrous oxide (N2O) has been linked to nitrogen loading, predicting emissions remains difficult, in part due to challenges in disentangling diverse N2O production pathways. As coastal ecosystems are especially impacted by elevated nitrogen, we investigated controls on N2O production mechanisms in intertidal sediments using novel isotopic approaches and microsensors in flow-through incubations. Here we show that during incubations with elevated nitrate, increased N2O fluxes are not mediated by direct bacterial activity, but instead are largely catalysed by fungal denitrification and/or abiotic reactions (e.g., chemodenitrification). Results of these incubations shed new light on nitrogen cycling complexity and possible factors underlying variability of N2O fluxes, driven in part by fungal respiration and/or iron redox cycling. As both processes exhibit N2O yields typically far greater than direct bacterial production, these results emphasize their possibly substantial, yet widely overlooked, role in N2O fluxes, especially in redox-dynamic sediments of coastal ecosystems.

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“…In this process, reduced metal species, particularly Fe 2+ (and possibly also Mn 2+ ) are oxidized, and NO, N 2 O, and N 2 are produced (Picardal, 2012). This pathway has a recognized importance in soils (Zhu-Barker et al, 2015), but is less studied in seawater and eutrophic lake water, which typically have much lower metal concentrations (Morel et al, 2003) than soil. Reducing sediments along productive continental margins may support significant rates of chemodenitrification (Scholz et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

Acidification Enhances Hybrid N2O Production Associated with Aquatic Ammonia-Oxidizing Microorganisms

et al. 2017

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Ammonia-oxidizing microorganisms are an important source of the greenhouse gas nitrous oxide (N2O) in aquatic environments. Identifying the impact of pH on N2O production by ammonia oxidizers is key to understanding how aquatic greenhouse gas fluxes will respond to naturally occurring pH changes, as well as acidification driven by anthropogenic CO2. We assessed N2O production rates and formation mechanisms by communities of ammonia-oxidizing bacteria (AOB) and archaea (AOA) in a lake and a marine environment, using incubation-based nitrogen (N) stable isotope tracer methods with 15N-labeled ammonium (15NH4+) and nitrite (15NO2−), and also measurements of the natural abundance N and O isotopic composition of dissolved N2O. N2O production during incubations of water from the shallow hypolimnion of Lake Lugano (Switzerland) was significantly higher when the pH was reduced from 7.54 (untreated pH) to 7.20 (reduced pH), while ammonia oxidation rates were similar between treatments. In all incubations, added NH4+ was the source of most of the N incorporated into N2O, suggesting that the main N2O production pathway involved hydroxylamine (NH2OH) and/or NO2− produced by ammonia oxidation during the incubation period. A small but significant amount of N derived from exogenous/added 15NO2− was also incorporated into N2O, but only during the reduced-pH incubations. Mass spectra of this N2O revealed that NH4+ and 15NO2− each contributed N equally to N2O by a “hybrid-N2O” mechanism consistent with a reaction between NH2OH and NO2−, or compounds derived from these two molecules. Nitrifier denitrification was not an important source of N2O. Isotopomeric N2O analyses in Lake Lugano were consistent with incubation results, as 15N enrichment of the internal N vs. external N atoms produced site preferences (25.0–34.4‰) consistent with NH2OH-dependent hybrid-N2O production. Hybrid-N2O formation was also observed during incubations of seawater from coastal Namibia with 15NH4+ and NO2−. However, the site preference of dissolved N2O here was low (4.9‰), indicating that another mechanism, not captured during the incubations, was important. Multiplex sequencing of 16S rRNA revealed distinct ammonia oxidizer communities: AOB dominated numerically in Lake Lugano, and AOA dominated in the seawater. Potential for hybrid N2O formation exists among both communities, and at least in AOB-dominated environments, acidification may accelerate this mechanism.

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The importance of abiotic reactions for nitrous oxide production

Cited by 186 publications

References 127 publications

Pathways and key intermediates required for obligate aerobic ammonia-dependent chemolithotrophy in bacteria and Thaumarchaeota

Pathways and key intermediates required for obligate aerobic ammonia-dependent chemolithotrophy in bacteria and Thaumarchaeota

Evidence for fungal and chemodenitrification based N2O flux from nitrogen impacted coastal sediments

Acidification Enhances Hybrid N2O Production Associated with Aquatic Ammonia-Oxidizing Microorganisms

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