Abiotic nitrous oxide production from hydroxylamine in soils and their dependence on soil properties
Introduction
Nitrous oxide (N2O) is an important greenhouse gas. It has an about 300 times higher global warming potential than carbon dioxide (CO2) over a time frame of 100 years and contributes approximately 6% to anthropogenic radiative forcing, making it the third-most important contributor after CO2 and methane (WMO, 2013). Furthermore, N2O is known to be partly responsible for the catalytic destruction of ozone in the stratosphere (Crutzen, 1970). While other historically dominant ozone depleting substances have been successfully regulated by the Montreal Protocol, N2O is still unregulated and, if present trends continue, will become the dominant ozone depleting substance in the 21st century (Ravishankara et al., 2009). The atmospheric mixing ratio of N2O has increased by 20% from a pre-industrial level of 270 ppb–325 ppb in 2012 at a rate of 0.80 ppb yr−1 over the last decade (WMO, 2013). The increase in atmospheric N2O is tightly coupled to increasing anthropogenic nitrogen (N) fixation, mainly applied as fertilizer and manure on agricultural fields.
Soils have been identified as the major source of N2O, contributing an estimated 50–60% to global N2O emissions (USEPA, 2010). However, there is still a large uncertainty associated with estimates of global N2O emissions from natural and anthropogenic sources, ranging from 8.1 to 30.7 Tg N yr−1 (Ciais et al., 2013). This great range of estimated values is mainly a reflection of the great uncertainty of the individual source and sink strengths of the diverse processes involved in N2O formation and consumption in soils (Billings, 2008).
Two microbial N transformation processes, autotrophic nitrification and heterotrophic denitrification, are considered the major N2O sources, contributing an estimated 70% of the global N2O emissions from soils (Butterbach-Bahl et al., 2013). N2O release during both processes has been described by Firestone and Davidson (1989) in their conceptual ‘hole-in-the-pipe’ model, but N2O production in soils, especially during nitrification, is far from completely understood. The model attributes N2O emissions from soils during nitrification and denitrification to leaks in the N transformation from ammonium to nitrate, and to the incomplete sequential reduction of nitrate via N2O to elementary nitrogen (N2). However, this model is over simplistic, as it is known that there are a variety of processes and metabolic pathways involved in soil N2O production. Because denitrification can both produce and consume N2O, an imbalance between N2O formation and reduction, depending on enzyme regulation, can make denitrifying bacteria net N2O producers or consumers. The fact that soils can, at least temporarily, function as significant N2O sinks has been reported recently (Chapuis-Lardy et al., 2007, Goldberg and Gebauer, 2009).
Apart from soil bacteria, fungi can also denitrify, but largely lack N2O reductase and therefore produce N2O (Laughlin and Stevens, 2002). Fungi are also involved in a hybrid reaction, called co-denitrification, in which inorganic and organic N precursors lead to N2O formation (Spott et al., 2011). Nitrifying bacteria produce N2O as a side product during the oxidation of NH2OH, but can also reduce nitrite under oxygen-limiting conditions or at elevated nitrite concentrations in a process similar to denitrification known as nitrifier denitrification (Poth and Focht, 1985, Wrage et al., 2001). There are more alternative processes potentially involved in N2O formation in soils, such as heterotrophic nitrification, dissimilatory nitrate reduction to ammonium (DNRA), nitrification by archaea, but also abiotic pathways (Bremner, 1997, Stevens et al., 1998, Santoro et al., 2011). Abiotic N2O formation pathways include (i) chemodenitrification, i.e., the decomposition of soil nitrite with NO as main product, but N2O as minor product (van Cleemput and Samater, 1996), (ii) the abiotic decomposition of ammonium nitrate on reactive surfaces in the presence of light (Rubasinghege et al., 2011), and (iii) the oxidation of the nitrification intermediate hydroxylamine (NH2OH) that can be oxidized by several soil constituents to form N2O (Bremner, 1997).
Lately, stable isotope techniques have developed great potential for disentangling the variety of different N2O formation processes; especially the intramolecular distribution of 15N in N2O, the so-called site preference (SP), has been in the focus of recent research (Decock and Six, 2013). The site-specific isotopic signature of N2O produced by several microbial pathways has been studied (Sutka et al., 2006, Sutka et al., 2008, Well et al., 2006, Opdyke et al., 2009, Frame and Casciotti, 2010, Wunderlin et al., 2013) as well as for abiotic N2O production via NH2OH oxidation (Heil et al., 2014). However, until now it is impossible to unambiguously differentiate between N2O production and consumption processes using SP information (Ostrom and Ostrom, 2011).
For better N2O mitigation strategies it is vital to understand the multitude of underlying microbial and abiotic processes of N2O production in the terrestrial N cycle and their controlling factors, as it is likely that N2O emissions from soils will increase at an ever growing rate due to an increasing demand for food, accompanied by an increased use of N fertilizer (Ciais et al., 2013). A better understanding is also prerequisite for lowering the high model uncertainty related to N2O emissions that is caused by the multitude of simultaneous processes involved in N2O formation, but also by the high temporal and spatial variability of these processes.
The chemical oxidation of NH2OH in the presence of several transitions metals commonly found in soils was recognized more than 30 years ago (Bremner et al., 1980), but is still neglected in most current N trace gas studies. The present study was designed to test for the potential of a coupled biotic–abiotic mechanism of N2O production under aerobic conditions, in which NH2OH microbiologically produced during nitrification is leaking to a certain extent out of autotrophic and heterotrophic nitrifiers into the soil matrix, where it is readily oxidized to N2O by transition metals, such as manganese or iron, or by nitrite, which is also excreted by ammonium oxidizers. To test for this potential mechanism, we added NH2OH to soil samples from different ecosystems (forest, grassland, cropland), both under non-sterile conditions and after sterilization with three different sterilization methods. The guiding hypothesis of the study was that at least in some soils this coupled biotic–abiotic mechanism might play a significant role in aerobic N2O formation during nitrification.
Section snippets
Sample collection
Soil samples were collected from three field sites (cropland, grassland, coniferous forest) that are part of the TERENO network, and additionally from a deciduous forest on the campus of Forschungszentrum Jülich (50°54′38″N, 6°24′44″E). The coniferous forest site (Wüstebach; 50°30′15″N, 6°18′15″E) was situated in the low mountain ranges of the Eifel National Park. The main vegetation at this site is Norway spruce (Picea abies (L.) Karst.). The soil type was a Cambisol with a loamy silt texture.
Soil incubation experiments
While neither the L nor the Oh horizon of the spruce forest soil showed significantly higher N2O evolution upon the addition of NH2OH compared to the H2O only treatment, the Ah horizon exhibited N2O formation only after NH2OH addition, while in the H2O treatment there was no N2O formed at all (Fig. 1.). In contrast, N2O formation in the deciduous forest soil could be observed for both treatments, but significantly more with NH2OH than with H2O only. The strongest reaction to NH2OH addition was
Abiotic N2O formation from different soils
There has been some controversy in the past about exclusively microbial formation of N2O during nitrification (Beaumont et al., 2002, Arp and Stein, 2003, Schmidt et al., 2004, Yu et al., 2010). However, most studies relate N2O production during nitrification to microbial pathways. Positive correlations between high ammonia oxidation activity and N2O production in chemostat and mixed culture experiments have been found (Yu et al., 2010, Wunderlin et al., 2012). Although it is believed that the
Conclusions
Our study showed that at least some soils have the potential to oxidize NH2OH to N2O in a purely abiotic reaction, which emphasizes the possibility of a coupled biotic–abiotic production of N2O during nitrification. We found this potential to be highly dependent on soil properties. Three factors that were found to possibly explain the capacity of the different soils to oxidize NH2OH to N2O were pH, C/N ratio, and Mn content, but further research is needed to evaluate the influence of the single
Acknowledgments
The authors would like to thank Holger Wissel for technical assistance in isotope-ratio mass spectrometry analysis, Dr. Andreas Lücke for laboratory support, and Dr. Daniel Weymann for his help with operating the GC instrument. J.H. acknowledges funding by the Faculty of Agriculture, University of Bonn, and S.L. was supported by the Chinese Scholarship Council (scholarship no. 201206760007).
References (54)
- et al.
Formation of nitrous oxide and dinitrogen by chemical decomposition of hydroxylamine in soils
Soil Biology & Biochemistry
(1980) - et al.
How reliable is the intramolecular distribution of 15N in N2O to source partition N2O emitted from soil?
Soil Biology & Biochemistry
(2013) - et al.
Ammonia oxidation in Nitrosomonas at NH3 concentrations near Km: effects of pH and temperature
Water Research
(1994) - et al.
Development of nitrification inhibition assays using pure cultures of Nitrosomonas and Nitrobacter
Water Research
(2001) - et al.
Site-specific 15N isotopic signatures of abiotically produced N2O
Geochimica Et Cosmochimica Acta
(2014) - et al.
The effects of biocidal treatments on metabolism in soil—V: a method for measuring soil biomass
Soil Biology & Biochemistry
(1976) - et al.
Moderately thermophilic nitrifying bacteria from a hot spring of the Baikal rift zone
FEMS microbiology ecology
(2005) - et al.
A highly sensitive method for the determination of hydroxylamine in soils
Geoderma
(2014) - et al.
Formation of hybrid N2O and hybrid N2 due to codenitrification: first review of a barely considered process of microbially mediated N-nitrosation
Soil Biology & Biochemistry
(2011) - et al.
Soil pH affects the processes reducing nitrate to nitrous oxide and di-nitrogen
Soil Biology & Biochemistry
(1998)
Fractionation of N2O isotopomers during production by denitrifier
Soil Biology & Biochemistry
isotopomer signatures of soil-emitted N2O under different moisture conditions—A microcosm study with arable loess soil
Soil Biology & Biochemistry
Role of nitrifier denitrification in the production of nitrous oxide
Soil Biology & Biochemistry
Mechanisms of N2O production in biological wastewater treatment under nitrifying and denitrifying conditions
Water Research
Metabolism of inorganic N compounds by ammonia-oxidizing bacteria
Critical Reviews in Biochemistry and Molecular Biology
A review of stable isotope techniques for N2O source partitioning in soils: recent progress, remaining challenges and future considerations
Rapid Communications in Mass Spectrometry
Nitrite reductase of Nitrosomonas europaea is not essential for production of gaseous nitrogen oxides and confers tolerance to nitrite
Journal of Bacteriology
Biogeochemistry: nitrous oxide in flux
Nature
Sources of nitrous oxide in soils
Nutrient Cycling in Agroecosystems
Rates of nitrous oxide production in the oxidation of hydroxylamine by iron(III)
Inorganic Chemistry
Nitrous oxide emissions from soils: how well do we understand the processes and their controls
Philosophical Transactions of the Royal Society B: Biological Sciences
Selective dissolution of manganese oxides from soils and sediments with acidified hydroxylamine hydrochloride
Soil Science Society of America Proceedings
Soils, a sink for N2O? A review
Global Change Biology
Carbon and other biogeochemical cycles
The influence of nitrogen oxides on atmospheric ozone content
Quarterly Journal of the Royal Meteorological Society
Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol
Environmental Microbiology
Microbiological basis of NO and N2O production and consumption in soil
Cited by (103)
Lower soil nitrogen-oxide emissions associated with enhanced denitrification under replacing mineral fertilizer with manure in orchard soils
2024, Science of the Total EnvironmentNitrite stimulates HONO and NO<inf>x</inf> but not N<inf>2</inf>O emissions in Chinese agricultural soils during nitrification
2023, Science of the Total Environment