The importance of abiotic reactions for nitrous oxide production ...

Biogeochemistry (2015) 126:251–267 DOI 10.1007/s10533-015-0166-4

SYNTHESIS AND EMERGING IDEAS

The importance of abiotic reactions for nitrous oxide production Xia Zhu-Barker . Amanda R. Cavazos . Nathaniel E. Ostrom . William R. Horwath . Jennifer B. Glass

Received: 13 May 2015 / Accepted: 17 November 2015 / Published online: 25 November 2015 Ó Springer International Publishing Switzerland 2015

Abstract The continuous rise of atmospheric nitrous oxide (N2O) is an environmental issue of global concern. In biogeochemical studies, N2O production is commonly assumed to arise solely from enzymatic reactions in microbes and fungi. However, iron, manganese and organic compounds readily undergo redox reactions with intermediates in the nitrogen cycle that produce N2O abiotically under relevant environmental conditions at circumneutral pH. Although these abiotic N2O production pathways have been known to occur for close to a century, they are often neglected in modern ecological studies. In this Synthesis and Emerging Ideas paper, we highlight the defining characteristics, environmental controls, and isotopic signatures of abiotic reactions between nitrogen cycle intermediates (hydroxylamine, nitric oxide, and nitrite), redox-active metals (iron and manganese) and organic matter (humic and fulvic acids) that can lead to N2O Responsible Editor: R. Kelman Wieder. X. Zhu-Barker W. R. Horwath Department of Land, Air, and Water Resources, University of California Davis, Davis, CA 95616, USA A. R. Cavazos J. B. Glass (&) School of Earth and Atmospheric Sciences, Georgia Institute of Technology, Atlanta, GA 30332, USA e-mail: [email protected] N. E. Ostrom Department of Integrative Biology, Michigan State University, East Lansing, MI 48824, USA

production. We also discuss the emerging idea that abiotic reactions coupled to biotic processes have widespread ecological relevance and encourage consideration of abiotic production mechanisms in future biogeochemical investigations of N2O cycling. Keywords Nitrous oxide Iron Manganese Soils Redox Metals Isotopes Site Preference

Introduction Nitrous oxide (N2O) is a potent greenhouse gas that contributes to positive radiative forcing and ozone destruction in the stratosphere (Montzka et al. 2011; Ravishankara et al. 2009; Stein and Yung 2003). Atmospheric N2O has risen from its pre-industrial concentration of 270 ppb at a linear rate of 0.75 ppb year-1 (IPCC 2014). The current global rate of N2O emissions is *18 Tg N year-1, with soil and aquatic systems accounting for 37 and 25 % of sources, respectively (IPCC 2014). The long atmospheric residence time of N2O (114 years; IPCC 2007) necessitates a detailed understanding of the mechanisms underlying its environmental sources and sinks. Nitrous oxide is produced from enzymatic processes, including nitrification, nitrifier denitrification and denitrification mediated by microbes and fungi (Conrad 1996; Firestone and Davidson 1989; Robertson 1987; Schreiber et al. 2012; Stein 2011; Thomson

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et al. 2012; Wrage et al. 2001). The factors that regulate the activity of nitrogen-cycling microorganisms—pH, organic matter, oxygen availability, soil water content, soil texture, and supply of inorganic nitrogen—are often assumed to be the same factors that regulate N2O emissions (Azam et al. 2002; Bouwman et al. 2002; De Bie et al. 2002; Linn and Doran 1984; Stark and Firestone 1995; Stevens et al. 1998; Venkiteswaran et al. 2014; Williams et al. 1992; Zhu et al. 2013a). However, abiotic reactions between redox-active metals (e.g. iron (Fe) and manganese (Mn)), organic matter, and enzymatically-derived reactive intermediates in the nitrogen cycle (e.g. hydroxylamine (NH2OH), nitric oxide (NO), and nitrite (NO2-)) can be significant and often overlooked sources of natural N2O emissions in both terrestrial and aquatic systems. The connection between metals and N2O has most likely been neglected because metals have not figured prominently in routine ecological evaluations of soil. Moreover, low environmental concentrations of reactive nitrogen intermediates—NH2OH, NO and NO2-— and soluble redox-active metals are assumed to limit their importance in abiotic reactions. However, the scarcity of nitrogen intermediates is likely due to their high reactivity in ‘‘cryptic’’ abiotic reactions, which may be coupled to enzymatic processes whereby one reactant is produced enzymatically and then undergoes further abiotic reactions to produce N2O or vice versa. Electron acceptors for abiotic N2O production are often elevated in mineral-rich soils, river discharge and dust inputs, and electron donors (e.g. Fe(II) and organic matter) can accumulate under anoxic conditions, suggesting that the substrates for abiotic N2O production are present in diverse soil and aquatic systems. Here, we champion the emerging idea that abiotic N2O production occurs via cryptic coupling to enzymatic sources of reactive nitrogen and may contribute significantly to N2O emissions in diverse ecosystems.

Thermodynamics and kinetics of abiotic nitrous oxide production in artificial solutions In this section we synthesize current knowledge on the thermodynamics and kinetics of the chemical reactions for abiotic N2O production and experimental findings from artificial solutions as a foundation for understanding the environmental distribution and

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Biogeochemistry (2015) 126:251–267

controls on these processes. Previous measurements of abiotic N2O production in sterile aqueous solutions and bacterial cultures are compiled in Table 1. Readers are also referred to Chao and Kroontje (1966; Table 1) for a complete list of possible inorganic nitrogen transformations from redox reactions with iron. Hydroxylamine decomposition Abiotic production of N2O can occur via NH2OH oxidation (hereafter referred to as NH2OH decomposition) by oxidized iron (Fe(III); Eq. 1) or manganese (Mn(IV); Eq. 2). Balanced redox reactions are shown below with DGr°0 values at standard state (1 atm, 25 °C, 1 M) and pH 7, assuming Fe(III) is present as goethite (a-FeOOH) and Mn(IV) is present as birnessite (MnO2). All DG°f values were from Stumm and Morgan (1996), with the exception of NH2OH (-23.4 kJ mol-1), which was calculated from standard electrode potentials (Latimer 1952). 2NH2 OH þ 4aFeOOH þ 8Hþ ! N2 O þ 4Fe2þ þ 9H2 O DG 0 ¼ 6:3 kJ mol e1

ð1Þ

2NH2 OH þ 2MnO2 þ 4Hþ ! N2 O þ 2Mn2þ þ 5H2 O DG 0 ¼ 106:2 kJ mol e1 :

ð2Þ

The more negative DG°0 indicates that NH2OH oxidation is more thermodynamically favorable with Mn(IV) (Eq. 2) than Fe(III) (Eq. 1). While both reactions as written are predicted to be more thermodynamically favorable at lower pH, the higher stability of the protonated form of NH2OH (NH3OH?; pKa 5.95) results in slower NH2OH oxidation at pH \6. Therefore, most kinetic experiments have been performed at low pH to facilitate measurement (Table 1). At low pH, N2O was the major product when Fe(III) [ NH2OH (Bray et al. 1919), whereas N2 was the major product when NH2OH C Fe(III) (Bengtsson et al. 2002). Rates of NH2OH oxidation by Fe(III) increased with temperature (Q10: 5.0) (Bray et al. 1919; Butler and Gordon 1986b). The reaction was first order with respect to total Fe(III) and NH2OH and inversely proportional to [H?]2.5, enabling derivation of a rate law based on total concentrations of reactants for Fe(III) concentrations:

Anoxic lab-scale reactor

Anoxic, precipitate-free Fe(II) medium, Acidovorax sp. BoFeN1

Ultrapure water, phosphate-citrate, tris-maleate

Kampschreur et al. (2011) Klu¨glein and Kappler 2013

Heil et al. (2014)

a

N2O production maximum is given in parentheses

Anoxic distilled deionized water, 10 mM NaCl, 30 mM PIPES

6–8 mM Fe(II)

0.5–8 mM NO2-

Anoxic, artificial groundwater medium, Shewanella putrefaciens

Coby and Picardal (2005)

Jones et al. (2015)

10 mM Fe(II)

0–43 mM NO2-

Anoxic, artificial groundwater medium, Shewanella putrefaciens, goethite

2.5–40 mM NO2-

0.25–2 mM NO2-

0.25–2 mM NH2OH,

10 mM NO3-

3 mM NO2-

0–5 mM NO2-

0–5 mM NO3-

5–10 mM Fe(III)

0.5–5 mM Fe(III)

3 mM Fe(II)

50 mM Fe(III) (goethite)

Fe(III) (goethite)

0.3 mM Fe(II)

0.2 mM Fe(III)

Cooper et al. (2003)

50 mM NH2OH

Oxic, 1 M ClO4

Bengtsson et al. (2002)

0.2 mM Fe(II)

0.2 mM NO2-

Anoxic, 30 mM K2SO4, Fe(III) oxyhydroxide

80 nM to 1.2 mM Fe(III)

80 nM to 4 lM NH2OH

Sørensen and Thorling (1991)

Butler and Gordon (1986b)

1.7 mM Cu(II) Distilled deionized water

0.6 mM Hg(II),

Distilled deionized water, natural and artificial seawater,

0.2 mM Fe(III)

14 mM Fe(II)

0.5 mM NO2-

Anoxic, distilled water,

Moraghan and Buresh (1977) 5 mM NH2OH

14, 21 mM Fe(II)

0.5 mM NO3-

Anoxic, distilled water, 0.002 or 0.2 mM Cu(II)

Buresh and Moraghan (1976)

Butler and Gordon (1986a)

0.4–25 mM Fe(II)

1 mM NO2-

Anoxic, 1 M NaAc

Nelson and Bremner (1970b)

80 nM Cu(II)

50 mM Fe(II) 40–50 mM Fe(III)

140 mM NO270 mM NH2OH

Chao and Kroontje (1966)

Fe(II) or Fe(III) concentrations 10 mM Fe(III)

H2SO4, KMnO4

Bray et al. (1919)

Nitrogen substrate concentrations 10 mM NH2OH

Experiment conditions, buffer (if described) and bacterial species (if any)

References

Table 1 Abiotic nitrous oxide (N2O) production in artificial solutions and pure bacterial cultures

7

3–8

5.6–7.6 (7.6)

0.7–1.3

6–8.5 (8.5)

1–2.6

2.5–9.5

6, 8 (8)

6–10 (8.5)

5

5–8

pHa

26

22

35

22

22

25

22

1.8, 20.4 (20.4)

22

26

26

25

22–100 (100)

T (°C)a

Chemodenitrification

NH2OH decomposition, chemodenitrification





NH2OH decomposition


NH2OH decomposition

NH2OH decomposition




Chemodenitrification, NH2OH decomposition

NH2OH decomposition

Abiotic process observed

Biogeochemistry (2015) 126:251–267 253

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. d½N2 O=dt ¼ k0 ½FeðIIIÞ ½NH2 OHT ½Hþ 2:5 ;

ð3Þ

where the rate constant k0 is 0.025 M1.5 h-1 (Butler and Gordon 1986b). However, this rate expression is only applicable at pH\2, and thus not relevant in most natural environments. Kinetic studies of NH2OH oxidation to N2O at more ecologically important circumneutral pH conditions are lacking, likely because this reaction occurs rapidly and thus can only be studied with highly sensitive N2O microelectrodes (Schreiber et al. 2012) instead of the more widely available gas chromatographic methods for N2O quantification. Chemodenitrification Abiotic production of N2O and N2 also occurs via chemodenitrification (Chalk and Smith 1983; Picardal 2012; Van Cleemput 1998) in which the reduction of NO3- (Eq. 4), NO2- (Eq. 5), or NO (Eq. 6) or N2O (Eq. 7) is coupled to the oxidation of Fe(II). These reactions are shown with DG°0 values calculated from thermodynamic data from Stumm and Morgan (1996) at standard state (1 atm, 25 °C, 1 M) and pH 7 assuming goethite (a-FeOOH) is the product of Fe(II) oxidation. 2þ þ NO þ 3H2 O ! NO 3 þ 2Fe 2 þ 2aFeOOH þ 4H

DG 0 ¼ 96:8 kJ mol e1

ð4Þ

2þ þ H2 O ! NO þ aFeOOH þ Hþ NO 2 þ Fe

DG 0 ¼ 88:7 kJ mol e1

ð5Þ

2NO þ 2Fe2þ þ 3H2 O ! N2 O þ 2aFeOOH þ Hþ

DG 0 ¼ 168:3 kJ mol e1 N2 O þ Fe2þ þ H2 O ! N2 þ aFeOOH þ Hþ DG 0 ¼ 316:7 kJ mol e1 :

ð6Þ ð7Þ

All four reactions shown above are thermodynamically favorable as indicated by negative DG°0 values. In artificial aqueous solutions at circumneutral pH, abiotic reduction of NO3- to NO2- (Eq. 4) is relatively slow (Buresh and Moraghan 1976; Table 1), implying that this process may have limited ecological relevance. However, NO2- reduction to NO (Eq. 5) and NO reduction to N2O (Eq. 6) by Fe(II) are

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predicted to occur in nature because N2O is the major product of chemodenitrification of NO2- at circumneutral pH (Moraghan and Buresh 1977). Nitrous oxide yield is stimulated by addition of copper (Moraghan and Buresh 1977), increasing pH and Fe(II) (Nelson and Bremner 1970b), and the presence of Fe(III)-oxyhydroxide minerals (Coby and Picardal 2005; Cooper et al. 2003; Jones et al. 2015; Kampschreur et al. 2011; Sørensen and Thorling 1991). Since N2O, not N2, is the major product of chemodenitrification in artificial solutions, abiotic N2O reduction by Fe(II) to N2 (Eq. 7) may be kinetically hindered, while this reaction occurs enzymatically at low O2 (Fig. 1). In sum, thermodynamic calculations and kinetic experiments in artificial solutions suggest that abiotic N2O-yielding reactions are favorable and likely to occur at circumneutral pH in soil and waters if chemical substrates are present. The availability of these substrates for abiotic N2O production in natural systems is discussed in the next section.

Substrates for abiotic N2O production in natural ecosystems Concentrations of the three enzymatically-produced nitrogen intermediates involved in abiotic N2O production—NH2OH, NO and NO2-—are typically low in natural ecosystems due to their high reactivity. Below we briefly discuss the major substrates (NH2OH, NO, NO2-, Fe, Mn and organic matter) involved in abiotic N2O production, summarize methods for their detection, and provide typical concentration ranges in the environment. Hydroxylamine, a key intermediate in bacterial and archaeal ammonia oxidation, is difficult to measure in natural samples due to its instability at pH [ 6. Micro-molar NH2OH concentrations in microbial cultures and wastewaters can be quantified using a spectrophotometric method (Frear and Burrell 1955), but measurement of trace NH2OH in natural samples typically requires a more sensitive technique. The most commonly used method for quantification of nanomolar NH2OH is oxidation to N2O with ferric ammonium sulfate (FAS) in acidic solution (*pH 3) followed by gas chromatography with an electron capture detector (Butler and Gordon 1986a; Von Breymann et al.


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Fig. 1 Schematic representation of the various processes in which iron, manganese and organic matter interact with nitrogen species in soils. Black arrows represent biotic processes and gray arrows represent abiotic processes. Biological processes are labeled with numbers: 1 ? 2 ? 3 = Nitrification; 1 ? 2 ? 5 ? 6 = Nitrifier denitrification; 1 ? 2 ? 3 ? 4 ? 5 ?

6 ? 7 = Nitrification-coupled denitrification; 4 ? 5 ? 6 ? 7 = Denitrification; 8 = Hydroxylamine oxidation. Abiotic processes that produce N2O (hydroxylamine decomposition and chemodenitrification) are labeled and outlined in dashed boxes. See text for balanced redox equations. Reactive intermediates in the nitrogen cycle are bolded

1982). This method has been used to detect NH2OH in coastal seawater, where highest concentrations occur in regions of nitrification activity (Table 2; Butler and Gordon 1986a; Butler et al. 1987, 1988; Gebhardt et al. 2004; Schweiger et al. 2007; Von Breymann et al. 1982) as well as in archaeal cultures (Vajrala et al. 2013). However, the presence of NO2- interferes with

NH2OH quantification by the FAS conversion method; at pH 3, NO2- is largely present as the protonated form nitrous acid (HNO2, pKa = 3.398), which decomposes to N2O (Kock and Bange 2013). Therefore, Kock and Bange (2013) recommended addition of sulfanilamide before sample acidification to remove the NO2- interference. Optimization of the

Table 2 Environmental hydroxylamine (NH2OH) concentrations

References

Location

Concentrations measured

von Breymann et al. (1982)

Oregon coast

\1–8 nM

Butler et al. (1987)

Yaquina Bay, Oregon

\1–250 nM

Butler et al. (1988)

Big Lagoon, California

\1–175 nM

Gebhardt et al. (2004)

Baltic Sea

2–179 nM

Schweiger et al. (2007)

Southwestern Baltic Sea

\19 nM

Liu et al. (2014)

Norway spruce forest

0.3–35 lg N kg-1 dry soil

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Table 3 Environmental nitric oxide (NO) concentrations Reference

Location/condition

NO concentrations

Zafiriou et al. (1980)

Seawater, central equatorial Pacific spiked with up to 0.8 lM NO2-

0–3 9 10-8 atm

Ward and Zafiriou 1988

Seawater, Eastern Tropical North Pacific Ocean

0–70 pM

Skiba and Ball (2002) Akiyama and Tsuruta 2003

Crop field, East Lothian, Scotland, UK Upland soil, Tsukuba, Japan

0–0.2 mg N m-2 10–148 mg N m-2

Schreiber et al. (2008)

Marine sediments, Spiekeroog Island, North Sea, Germany

0–1 lM

Schreiber et al. (2008, 2009)

Biofilm enrichment culture, sewage treatment plant, Seehausen, Germany

0.03–2.3 lM

Zhu et al. (2013a)

Agricultural soils, California

0–0.07 mg N kg-1 dry soil

Schreiber et al. (2014)

Sediment, Weser River, Germany

0–1.5 lM

FAS method with extraction of hydroxylamine in pH 1.7 solution containing 0.02 M HCl and 2 mM sulfanilamide has enabled NH2OH detection in soils down to 0.3 mg N kg-1 dry soil (Table 2; Liu et al. 2014). Nitric oxide is an intermediate in both nitrification and denitrification and can also be produced chemically (Ludwig et al. 2001; Medinets et al. 2015; Venterea and Rolston 2000). Since NO is very reactive and turns over rapidly, its concentrations in environmental settings are highly variable and often extremely low (Table 3). Chemiluminescent detection of NO down to 10-13 M concentrations (Zafiriou and McFarland 1980) revealed that NO was elevated in the zone of highest nitrification above a marine oxygen minimum zone (Ward and Zafiriou 1988; Zafiriou et al. 1980). Subsequent development of NO microelectrode sensors has enabled measurement of this trace gas in situ in diverse ecosystems (Table 3; Jenni et al. 2012; Schreiber et al. 2012). Nitrite is also an intermediate in nitrification and denitrification, and thus NO2- production occurs in oxic and anoxic environments and at their interface. Nitrite can accumulate in soil and aquatic systems depending on environmental conditions such as inorganic nitrogen availability, nitrification activity, pH, organic matter content, temperature and moisture content (Burns et al. 1995, 1996; Nelson and Bremner 1969; Shen et al. 2003; Smith et al. 1997; Van Cleemput and Samater 1996). In seawater, primary and secondary NO2- maxima occur in the water column due to phytoplankton excretion and nitrification (Lomas and Lipschultz 2006) and denitrification (Lam et al. 2011), respectively. Iron is the most prevalent redox-active metal in the biosphere and an essential element for nearly all life

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forms (Melton et al. 2014). Two redox states exist in natural environments: Fe(III), poorly soluble at circumneutral pH, and soluble Fe(II). Environmental Fe concentrations vary widely depending on redox, pH and source material composition. Soils typically contain ppm to weight percent Fe (Shacklette and Boerngen 1984). Oxic seawater contains vanishingly low (picomolar to nanomolar) Fe concentrations (Johnson et al. 1997), while acid mine drainage can possess hundreds of millimolar Fe (Druschel et al. 2004). In anoxic soils and sediments, microbes reduce Fe(III) to Fe(II) while oxidizing organic matter or hydrogen (Lovley 1991; Weber et al. 2006). Reduced Fe(II) is oxidized to Fe(III) in the presence of O2 or under anoxic conditions by nitrate-reducing bacteria through a combination of biotic and abiotic reactions (e.g. Carlson et al. 2013; Chakraborty and Picardal 2013; Klu¨glein and Kappler 2013; Picardal 2012). Manganese is typically less abundant than Fe in soil (Adriano 1986; Aubert and Pinta 1980) while its concentration in aquatic ecosystems is comparable to that of Fe. Manganese exists in three oxidation states—II, III, and IV—in natural ecosystems. Insoluble Mn(IV) oxides are strong oxidants (Luther and Popp 2002; Luther et al. 1997; Thamdrup and Dalsgaard 2000) that are reduced by many of the same bacteria that perform Fe(III) reduction (Lovley 1991). Soluble Mn(II) is oxidized by physiologically diverse microbes either enzymatically (Tebo et al. 2005) or via chemical reactions with enzymaticallyproduced reactive oxygen species (Learman et al. 2011a, b, 2013). Organic ligands stabilize Mn(III), accounting for up to 90 % of the dissolved Mn pool in anoxic sediments (Madison et al. 2013).


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Table 4 Nitrous oxide (N2O) production in natural samples via reactions with iron, manganese and organic matter Reference

Environment

Sterilization method

Substrates

pHa

T (°C)a

Abiotic process observed/ assumed

Porter (1969)

Soil extracts

Extraction

Oximes, NO2-

5, 6

23, 50 (50)


Stevenson and Swaby (1964)

Soil extracts

Extraction

Humic acids, fulvic acids, lignin, polyphenols, HNO2

Stevenson et al. (1970)

Soil extracts, silt loam soil

Extraction

Humic acids, fulvic acids, lignin, polyphenols, NO2-

6, 7

Nelson and Bremner (1970a)

Silty loam/clay soils

Autoclaving

Humic acid, lignin, NO2-

5–7

25


Bremner et al. (1980)

Diverse soils

Autoclaving

NH2OH, NO2-, Fe(III), Mn(IV)

3.6–8.2

30

NH2OH decomposition

Van Cleemput and Baert (1984)

Silty loam soil

None

NO2-, Fe(II)

3.8–6 (6)

25


Li et al. (1988)

Rice paddy soil

60

NH4?, Fe(III)

28

Feammox

Law and Ling (2001)

Southern Ocean

None

Fe(II)

*8

2

NH2OH decomposition (?)

Samarkin et al. (2010)

Soil brine, Antarctica

NO2-, NO3-, Fe(II)

5.6

-20 to 27 (27)


Yang et al. (2012)

Forest soil

None (no biological activity detected) None (C2H2 as inhibitor)

NH4?, Fe(III)

5–6

Zhu et al. (2013b)

Agricultural soils

None

NH4?, NO3-

4.2–7.5

22

Heil et al. (2015)

Coniferous forest soil, deciduous forest soil, grassland soil, cropland soil

Autoclaving chloroform, methyl iodide

NH2OH

3.4–6.4 (6.4)

10–50 (50)

a

Coirradiation



Feammox Ammonia oxidation/ NH2OH decomposition, (chemo)denitrification NH2OH decomposition

N2O production maximum is given in parentheses

Extractable organic matter in soils and natural waters is operationally defined as fulvic and humic acids (Stevenson 1994). Fulvic acids tend to be enriched in carboxyl and phenolic hydroxyl functional groups resulting in relatively high total acidity, while humic acids typically contain more methoxy functional groups. Fulvic acids have considerably lower molecular weights compared to humic acids and

therefore dominate the dissolved organic matter phase in soil solution and natural waters.

Abiotic N2O production in soils In previous reports of soil abiotic N2O production (compiled in Table 4) abiotic processes were

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distinguished from biotic processes by soil sterilization. It is important to consider that most sterilization techniques will alter physical and chemical soil properties, thereby stimulating or suppressing abiotic processes. Autoclaving and cobalt-60 gamma irradiation increase extractable Mn and NH3/NH4? and would therefore be expected to promote abiotic N2O production, while the chemical disinfectants propylene oxide and sodium azide increase soil pH and, in the case of azide, also extractable N (McNamara et al. 2003; Skipper and Westermann 1973). Toxic metal salts such as mercuric chloride appear to have fewer effects on soil chemical factors (Wolf et al. 1989), but may promote abiotic N2O production in aquatic systems (see below). Hydroxylamine decomposition Abiotic N2O production from oxidation of NH2OH by Fe(III) (Eq. 1) and Mn(IV) (Eq. 2) was first reported in natural soils by Bremner et al. (1980). At soil pH *4 to 7, N2O was the dominant gaseous product and its abiotic production was positively correlated with soil Mn(IV) content. Moreover, abiotic NH2OH decomposition was not stimulated by NO2-, but was by Fe(III) and Mn(IV) amendments (Bremner et al. 1980; Minami and Fukushi 1986). Despite the strong evidence for the importance of abiotic NH2OH decomposition in soil N2O emissions, Bremner (1997) concluded that this process was likely unimportant for global soil N2O emissions due to the lack of evidence for extracellular release of NH2OH during nitrification. Since that report, most soil research has focused on enzymatic N2O production, leaving abiotic N2O emission processes largely ignored until recently. Current interest in cryptic elemental cycling has reinvigorated the study of highly reactive N species and their role in soil N2O production. In a recent study, N2O production from sterilized cropland soil was found to positively correlate with soil pH and Mn content and negatively correlate with C/N ratio (Heil et al. 2015). The negative correlation with C/N ratio was explained by a competitive reaction of NH2OH with carbonyl groups in soil to form oximes (Bremner et al. 1980), which are fixed into secondary organic compound (Porter 1969; Thorn and Mikita 2000). Ferric iron may also be an important driver of NH2OH decomposition; extractable Fe(III) ranked higher than any other intrinsic soil property in explaining soil N2O

123


emissions from California agricultural soils (Zhu et al. 2013b). In contrast to previous assumptions, Liu et al. (2014) used a modification of the FAS method to show that NH2OH does indeed accumulate during soil nitrification, albeit at low concentrations (0.3–35 lg N kg-1 dry soil; Table 2) and is linearly correlated with soil N2O concentration. Rapid decomposition of NH2OH by Fe(III) or Mn(IV) makes this process a potentially significant as a source of N2O under environmentally favorable conditions (Fig. 1). In the Heil et al. (2015) study, *40 ng N-N2O was produced per 5 nmol (70 ng) of NH2OH added per gram of sterilized cropland soil. Although NH2OH concentrations are not yet available for cropland soils, assuming that concentrations were equal to those of forest soils (0.3–35 lg N kg-1 dry soil), N2O emissions might be as high as *20 ng N-N2O g-1 soil, similar to those previously reported for agricultural soils under oxic conditions (Zhu et al. 2013a). Thus, coupled biotic-abiotic production of N2O from enzymatically-produced NH2OH may be more widespread than previously considered, particularly in soils with high nitrification activity. Chemodenitrification Soil N2O yield from NO2- reduction by Fe(II) (Eqs. 5 and 6) is stimulated by decreasing O2 (Nelson and Bremner 1970a), increasing Fe(II) (Nelson and Bremner 1970b) and the presence of organic matter (Van Cleemput and Baert 1984). Therefore, N2O production from chemodenitrification is predicted to be most environmentally relevant in anoxic habitats with high organic supply (e.g. wetlands and waterlogged soils) where bacterial denitrification leads to the accumulation of reactive NO2- and NO and soluble Fe(II) diffuses in zones of Fe(III) reduction (Van Cleemput 1998; Van Cleemput and Baert 1984). Significant abiotic N2O production from NO2- (31–75 % total emissions) has also been reported for aerated soils (Venterea 2007). Interestingly, there is no direct evidence of participation of Mn(II) in soil chemodenitrification (Nelson and Bremner 1970b) despite the thermodynamic favorability of these reactions (Luther 2010). Another related soil pathway, the anaerobic oxidation of ammonium with Fe(III)—or Feammox— is not further discussed here because its major product is not N2O but N2, NO2- or NO3- (Cle´ment et al.


259

2005; Huang and Jaffe´ 2015; Li et al. 1988; Shrestha et al. 2009; Yang et al. 2012). Renewed interest in chemodenitrification with Fe(II) has been generated by the recent discovery that abiotic N2O production is an important process in the McMurdo Dry Valleys of East Antarctica (Murray et al. 2012; Peters et al. 2014; Samarkin et al. 2010). Substrates for abiotic N2O production are abundant in the Dry Valleys, where exceptionally high concentrations of NO3-, NO2- and NH4? are in contact with Fe(II) minerals (Murray et al. 2012; Samarkin et al. 2010). Samarkin et al. (2010) documented large fluxes of N2O from soils taken from Don Juan Pond in Southern Victoria Land, Antarctica. Chemodenitrification may be the only mechanism for N2O production in this hypersaline brine ecosystem where high salt content appears to inhibit microbial activity (Peters et al. 2014; Samarkin et al. 2010). In addition to Fe(II), organic matter can also act as a reductant during chemodenitrification to N2O. Under anoxic and circumneutral pH conditions, humic acids reduce NO to N2O (Stevenson et al. 1970) and diverse organic molecules—including humic and fulvic acids, lignins, and phenols—reduce nitrous acid (HNO2) to N2 and N2O (Stevenson and Swaby 1964). The occurrence of the latter reaction in natural soils is suggested by the high correlation between rates of abiotic N2O production and HNO2 content in California agricultural soils (Venterea and Rolston 2000). In soils with pH [5, the reaction of NO2- with oximes formed through the reaction of NH2OH with organic matter can produce trace N2O, with yields increasing with temperature (Porter 1969). In peat soils with pH \4.5, the primary product of abiotic NO2- reduction was NO, not N2O (McKenney et al. 1990). Black carbon (biochar) has been shown to reduce agricultural soil N2O emissions via stimulation of complete denitrification to N2 (Fig. 1). No impact on N2O levels was observed in autoclaved soil with or without added biochar (Cayuela et al. 2013), suggesting that biological reactions are key for this pathway.

minimum zones (Babbin et al. 2015; Naqvi et al. 2010). Previous studies of N2O in seawater have attributed its production to microbial nitrification, denitrification or a combination thereof (Freing et al. 2012; Ostrom et al. 2000; Zamora and Oschlies 2014). Large-scale seawater Fe fertilization experiments reported N2O production inside an iron-fertilized patch of water and postulated its source as Fe stimulation of nitrification (Law 2008; Law and Ling 2001). An alternative interpretation is that Fe added to seawater as acidified Fe(II) reduced NO2- to N2O, and/or Fe(III) (either produced by chemodenitrification or oxidized by O2 in surface water) oxidized NH2OH to N2O. These are both examples of coupled biotic-abiotic N2O production processes mediated by rapid iron redox cycling (Glass et al. in review). Novel isotopic signatures of N2O produced by enrichment cultures of marine ammonia-oxidizing archaea suggest that they are the major source of marine N2O (Santoro et al. 2011), but it is still unknown whether this N2O production occurs by purely enzymatic reactions or coupled biotic-abiotic reactions between microbially-produced nitrification intermediates such as NH2OH and chemical oxidants in seawater (Glass et al. in review; Jung et al. 2014; Stieglmeier et al. 2014). High salinity has also been shown to favor N2O relative to other products during NH2OH decomposition (Butler and Gordon 1986b). Thus, it is possible that marine environments could support abiotic N2O production in regions where metals and reactive nitrogen intermediates accumulate, such as the secondary nitrite maximum where both Fe(II) and NO2- peak (Glass et al. 2015; Moffett et al. 2007). Assuming a yield of 0.04–0.08 % N2O per NO2- produced (Santoro et al. 2011; Stieglmeier et al. 2014) and NH3 oxidation rates of *10 nmol kg-1 day-1 at oxic-anoxic interfaces (Ward and Zafiriou 1988), these coupled biotic-abiotic reactions could produce *1 to 3 nmol kg-1 year-1, consistent with *3 nmol kg-1 year-1 for globally integrated rates of subsurface N2O production (Freing et al. 2012).

Abiotic N2O production in aquatic environments

Isotopic evaluation of abiotic N2O production

The potential for abiotic reactions to produce N2O in aquatic systems has received much less attention than in soils. Highest N2O concentrations in seawater are found at oxic-anoxic interfaces overlying oxygen

While abiotic N2O production in natural environments has been recognized as potentially important for several decades, discriminating abiotic from enzymatic N2O production remains challenging. This

123

123 Artificial solution Cropland soil Anoxic artificial solution Anoxic artificial solution

Heil et al. (2014)

Heil et al. (2015) Jones et al. (2015)

Glass et al. (in review)

7.5 7.5–7.7 7.5

NO3NO3-

NH2OH NH4?

Pseudomonas chlororaphis Pseudomonas aureofaciens

Sutka et al. (2006)

Sutka et al. (2006)

3.1

NH2OH, soil NH2OH, soil NH2OH, soil NH2OH, soil

Nitrosomonas marina Coniferous forest soil Deciduous forest soil Grassland soil Cropland soil

Frame and Casciotti (2010)

Heil et al. (2015)

Heil et al. (2015)

Heil et al. (2015)

Heil et al. (2015)

6.4

3.6

4.9

7.5

NH4?

Nitrosomonas europaea Nitrosomonas marina

Sutka et al. (2006)

Frame and Casciotti (2010)

7.5

7.0–7.2

C2H2

NO3-, NO2-, NO2-,

Paracoccus denitrificans

7.0–7.2

Toyoda et al. (2005)

6.9-7.1

7.5-7.7

7.8

6.4 7.0

3.0-8.0

5.6

1.0

pH

NH2OH

NO2-

NO, Fe(II)

NH2OH, sterile soil NO2-, Fe(II)

NH2OH, NO2-, Fe(III), Fe(II), Cu(II)

NH2OH, MnO2

NO2-, (CH3)3NBH3

Substrates

NO3-, C2H2

Methylococcus capsulatus Pseudomonas fluorescens

Sutka et al. (2003, 2004)


Nitrosomonas europaea

Sutka et al. (2003, 2004)

Biotic

Artificial solution Don Juan Pond brine


Peters et al. (2014)

Artificial solution

Sample or species


Abiotic

Reference

Table 5 Site preference (SP) values for abiotic and biotic N2O production processes

20

20

20

20

25

25

25

27

27

40

27

25

20 26

-20

27

27

T (°C)

35.66 ± 1.56

35.21 ± 1.94

33.02 ± 4.63 31.81 ± 14.93

-10.7 ± 2.9

36.3 ± 2.4

33.5 ± 1.2

-0.5 ± 1.9

-0.6 ± 1.9

-5.1 ± 1.8

23.3 ± 4.2

30.8 ± 5.9

-0.8 ± 5.8

15.9 ± 3.2

34.1 ± 1.9 10.0–22.0

34.0–35.6

0.7 ± 6.5

29.5 ± 1.1

30.1 ± 1.7

SP (%)

NH2OH oxidation

NH2OH oxidation

NH2OH oxidation

NH2OH oxidation

Nitrifier-denitrification

NH2OH oxidation

NH2OH oxidation

NO3-/NO2- denitrification

NO3-/NO2- denitrification

NO3- denitrification

NO3- denitrification

NH2OH oxidation

NO2- reduction

NO reduction

NH2OH oxidation NO2- reduction

NH2OH oxidation


NH2OH oxidation

NO2- reduction

Process observed

260 Biogeochemistry (2015) 126:251–267


challenge, in part, reflects a paucity of studies evaluating the isotope effects associated with abiotic N2O production as well as the high likelihood that environmental N2O production arises from coupled biotic-abiotic reactions. Stable isotope ratios have a long history of resolving molecular production pathways and thus hold promise for N2O, a remarkably simple molecule that contains great isotopic complexity. Nitrous oxide isotope systematics include bulk d15N and d18O signals, site specific isotopic information (because the two N atoms in N2O have unique covalent bonds), and may also contain unique mass-independent 17O and ‘‘clumped’’ isotope (e.g. 15N14N18O) values. In particular, site preference (SP: the difference in d15N between the central, a, and outer, b, N atoms in N2O) has emerged as a strong indicator of microbial production pathways because it is independent of the isotopic composition of the inorganic N substrates of nitrification and denitrification. In the Dry Valleys of Antarctica, where abiotic N2O production is likely a significant source of N2O (see above), SP has not yet proven insightful in resolving abiotic and microbial N2O production. The soils surrounding Don Juan Pond were found to evolve N2O with a markedly large range in SP of -45 to ?4 % (Samarkin et al. 2010). While the N2O in Lake Vida is expected to be abiotic in origin (Ostrom et al. 2015), a SP value of approximately -4 % was determined, which is within the range associated with microbial denitrification of -10 to 0 % (Frame and Casciotti 2010; Murray et al. 2012; Sutka et al. 2006). Within other Dry Valley environments (Don Juan Pond, a pond in the Labyrinth, Lake Vanda and Lake Bonney), N2O SP values encompassed the range expected for microbial nitrification (33–37 %) and denitrification (-10 to 0 %) (Peters et al. 2014; Priscu et al. 2008). The wide range in SP and overlap with microbial SP values led Peters et al. (2014) to conclude that SP cannot be used to distinguish abiotic and microbial N2O production pathways. In one sense, this conclusion should not be surprising as a single isotope tracer can only resolve the contribution from two sources and resolution requires that those sources be isotopically distinct (Macko and Ostrom 1994). Nonetheless, the wide range of SP values in the Dry Valleys does not negate the potential for stable isotopes to provide insight into production pathways; particularly if the source signals can be better constrained by novel isotope tracers (e.g. d17O or

261

clumped isotopes) and a study approach chosen that narrows the number of possible sources. Evidence for a narrowing of the SP values expected from abiotic N2O production pathways is emerging, as shown in Table 5. In a series of experiments monitoring abiotic N2O production from NH2OH in combination with NO2-, Fe(III), and Cu(II), Heil et al. (2014) found consistent SP values of 34 to 35 % regardless of reaction conditions. Similarly, Toyoda et al. (2005) reported a SP value of *30 % for N2O produced by reactions of NO2- with trimethylamineborane ((CH3)3NBH3) and NH2OH oxidation by MnO2. Nitrous oxide produced abiotically upon addition of NH2OH to tap water also had a SP of *30 % (Heil et al. 2014; Wunderlin et al. 2013). Reactions of Fe(III) with NH2OH and NO yielded SP values of approximately 30 and 16 %, respectively (Glass et al. in review). Jones et al. (2015) recently reported SP values between 10 and 22 % for reduction of NO2- to N2O in the presence of Fe(II), similar to the SP reported by for NO reduction. Thus the variable SP values for NO2- reduction by Fe(II) (Jones et al. 2015) may reflect fractionation both during abiotic NO2reduction to NO and NO reduction to N2O, with the latter step as the dominant control on the observed fractionation. Collectively, these results indicate that biotic and abiotic production of N2O from NH2OH yields SP values of 30 to 35 %, distinct from N2O produced abiotically from NO as well as microbial denitrification. While identification of distinct isotopic values of biological and abiotic N2O production remains elusive, there are additional lines of evidence to distinguish these pathways. Abiotic production of N2O via chemodenitrification from Fe(II) minerals also produces H2 (Samarkin et al. 2010). Consequently, the high level of H2 present in Lake Vida provides compelling evidence for the occurrence of chemodenitrification in this system (Murray et al. 2012). Chemodenitrification strongly reduces NO2-, while NO3- is weakly if at all reduced (Samarkin et al. 2010; Ostrom et al. 2015). Furthermore, abiotic NH2OH decomposition in sterilized soils produced higher yields of N2O than N2 (Bremner et al. 1980), while enzymatic denitrification often proceeds all the way to N2 (Fig. 1). Similarly, in a series of experiments with additions of 15N-enriched NO2- to Lake Vida brine incubated in the presence of toxic concentrations of zinc chloride as a biocide, Ostrom et al. (2015)

123

262

observed an N2O/(N2 ? N2O) production ratio of *20, markedly higher than that associated with microbial N2O production in soils (Schlesinger 2009) and coastal marine ecosystems (Seitzinger 1988). Recent evidence has revealed another potential isotopic signature of abiotic N2O production: very rapid transitions from kinetic to equilibrium isotope effects. In abiotic N2O production experiments, Heil et al. (2014) observed kinetic isotope behavior (e.g. d15N of N2O increasing with time) only within the first few hours of N2O production, after which isotope values stabilized. Similarly, constant isotope values were observed over several days of abiotic N2O production from NH2OH; a kinetic isotope effect was only evident in the d18O of N2O associated with production from NO (Glass et al. in review). Equilibrium isotopic behavior was obtained within 2 days during abiotic NO2- reduction to N2O, suggesting that rapid exchange of N and O isotopes may be characteristic of chemodenitrification (Jones et al. 2015). In summary, overall isotopic equilibrium fractionation behavior can be expected for abiotic N2O production from NO and NH2OH, with the exception that a kinetic isotope effect for d18O may enable distinction of abiotic production of N2O from NO.

Summary and future directions for N2O research There is mounting evidence for the importance of abiotic and coupled biotic-abiotic N2O production pathways in addition to the better-characterized biotic pathways. The environmental controls on the two major abiotic N2O production pathways described above are summarized in in Fig. 1: abiotic NH2OH decomposition to N2O at circumneutral pH is favored by high Mn(IV), temperature and salinity, and low organic carbon, while chemodenitrification of NO and NO2- to N2O is favored by high pH, low O2 and solid Fe(III) or Cu(II) catalysts. Since that enzymatic denitrification can reduce N2O to N2 under anoxic conditions (Fig. 1), it is likely that N2O as an end product of chemodenitrification is limited to extreme environments where life cannot persist (e.g. Antarctic hypersaline ponds), whereas abiotic NH2OH decomposition may be more widespread in environments with high rates of NH2OH production during nitrification.

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The reactivity of intermediates in the nitrogen cycle with redox-active metals and organic matter challenges biogeochemists to distinguish between biotic and abiotic N2O production. A recent study suggests that abiotic N2O production may also be important in wastewater treatment with activated sludge (Harper et al. 2015), suggesting that future studies of wastewater N2O emissions should also take abiotic processes into consideration. Because quantification of the significance of abiotic, biotic, and coupled abioticbiotic pathways is necessary to fully understand the magnitude and environmental impact of sources of N2O, we encourage characterization of the rates, mechanisms, environmental controls and global importance of all three N2O production pathways in future research. Below, we briefly highlight several directions for future research in this emerging topic. In the study of abiotic N2O processes, the choice of sterilization method is essential to minimize changes to ambient chemical and physical properties in the study system. A recent study revealed that abiotic N2O emissions after autoclaving were significantly lower than after chloroform or methyl iodide fumigation (Heil et al. 2015). Azide is not recommended due to its nitrogen content. Toxic metal additions are more commonly used in aquatic studies, but may catalyze abiotic reactions. Comparison of several applicable methods for the study system is recommended for strictly abiotic studies, but even the least invasive sterilization methods will inherently remove the prospect of studying coupled biotic-abiotic processes. Therefore, alternative methods are required to characterize hybrid pathways. Characterization of cryptic abiotic and coupled biotic-abiotic reactions could greatly benefit from next-generation DNA, RNA and protein sequencing methods (metagenomics, metatranscriptomics and metaproteomics) coupled to rate measurements. Omics methods enable characterization of the metabolic potential and/or functional gene/transcript expression in environmental samples and are useful hypothesis generators. For instance, the absence of characteristic genes encoding the catalytic subunit of the nitric oxide reductase in ammonia-oxidizing archaea (Santoro et al. 2015; Walker et al. 2010) suggests that either a novel enzyme in this organism produces N2O or else that coupled biotic-abiotic reactions may be responsible for N2O accumulation in nitrifying archaeal cultures (Glass et al. in review).


Clark-type microelectrode sensors have enabled dissolved N2O (and NO) measurements in aquatic systems at millimeter-scale spatial and second-scale temporal resolution (Schreiber et al. 2012). However, users are warned that environmental N2O concentrations are often below the detection limit of commercially available microelectrodes, and significant interferences exist for NO and H2S. In well-defined systems, these interferences can be removed with correction factors (Jenni et al. 2012). New N2O isotope systems, including site specific, mass independent and clumped isotope analyses, are innovative approaches with the potential to contribute insights on the nature of abiotic N2O production processes (Heil et al. 2014; Ostrom and Ostrom 2012); readers are referred to Schreiber et al. (2012) for a review of instrumentation. While there remains no definitive isotopic ‘‘smoking gun’’ to distinguish abiotic from biotic N2O production, we emphasize the utility of coupling multiple geochemical and isotopic markers of abiotic N2O production including concurrent evidence of H2 production during chemodenitrification, preferential reduction of NO2- relative to NO3-, preferential production of N2O relative to N2, and equilibrium rather than kinetic isotope fractionation behavior. Finally, we emphasize that the pathways and lowtemperature soil and aquatic ecosystems discussed here are almost certainly not the sole contributors to abiotic N2O production. Future investigations should consider understudied abiotic N2O sources, including the potential for chemodenitrification with Mn(II) and organic matter as the electron donor, as well as completely novel pathways, such as photochemical N2O production that occurs in the atmosphere (Rubasinghege et al. 2011), and may also be widespread on the Earth’s surface. Given that higher temperatures accelerate reaction rates, anoxic groundwaters and hydrothermal environments are promising ecosystems for further exploration of abiotic N2O reactions. Acknowledgments We thank Martin Klotz, Lisa Stein, Nicolas Bru¨ggemann, Bess Ward, and Fourth International Conference on Nitrification (ICoN4) participants for helpful discussions. We also thank Timothy A. Doane, G. Philip Robertson, associate editor R. Kelman Wieder, and four anonymous reviewers for thoughtful comments on earlier versions of this manuscript. WRH and XZB acknowledge support provided by the J. G. Boswell Endowed Chair in Soil Science and USDA National Institute of Food and Agriculture (NIFA; Grant Number: 2011-67003-30371). ARC

263 acknowledges support from the NSF Graduate Research Fellowship Program and the Georgia Institute of Technology Goizueta Foundation Fellowship. NEO acknowledges support from the NSF Geobiology and Low Temperature Geochemistry program (Grants 1053432 and 1348935). JBG acknowledges support from NASA Exobiology Grant NNX14AJ87G and a Center for Dark Energy Biosphere Investigations (NSF-CDEBI OCE-0939564) Small Research Grant.

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