Effect of Ammonium Concentration on N 2 O Emission During Autotrophic Nitritation Under Oxygen-Limited Conditions

Abstract

Nitrous oxide (N₂O) is one of the most powerful greenhouse gases, emitted by ammonia-oxidizing bacteria (AOB) and denitrifier during nitrogen transformation. A laboratory-scale sequencing batch reactor with enriched nitrifiers was developed under oxygen-limited conditions with synthetic wastewater (without organic carbon) to investigate the effect of ammonium (NH₄⁺) concentration on N₂O emission. The system achieved 70% conversion of the influent NH₄⁺ to nitrite (NO₂⁻) and the N₂O emission factor (ratio between N₂O nitrogen emitted and the NH₄⁺ oxidized) was about 17.0%. NH₄⁺ concentration was shown to have a major impact on N₂O emission. When influent NH₄⁺ concentrations were 60, 120, and 240 mg·N/L, total N₂O emissions were 3.24, 8.75, and 24.59 mg·N/L, respectively. Comprehensive analysis of N₂O emission rate on NO₂⁻ concentration (Fig. 5) together with the absence of a contribution from heterotrophic denitrifiers suggests that AOB denitrification is the main cause of N₂O emission during oxygen-limited autotrophic nitritation processes.

Introduction

Nitrous oxide (N₂O) is one of the greatest potential greenhouse gases, with an ∼265-fold stronger global warming effect than carbon dioxide in a 100-year perspective, and it is also considered to be the dominant stratospheric ozone depleting substance (Ravishankara et al., 2009; IPCC, 2013). A small amount of N₂O accumulation would exert a great negative effect on environment for its long atmospheric lifetime (131 ± 10 years) (IPCC, 2013). Therefore, great attention should be emphasized on the control of N₂O emission.

The United States Protection Agency reported that the amount of N₂O emitted from wastewater sector accounts for about 3% of the total global emissions, as the sixth largest contributor (USEPA, 2006). Nitrogen compounds in wastewater are mainly removed by nitrification and denitrification. And N₂O emission in the wastewater treatment process can result from the activity of denitrifying microorganisms and ammonia-oxidizing bacteria (AOB) (Firestone et al., 1979; Lipschultz et al., 1981). According to recent research, N₂O production by AOB in wastewater is through two main pathways: (1) the reduction of nitrite (NO₂⁻) to N₂O through nitric oxide (NO), known as nitrifier or AOB denitrification (Kim et al., 2010); (2) N₂O as a side product during incomplete oxidation of hydroxylamine (NH₂OH) to NO₂⁻ (Chandran et al., 2011; Stein, 2011; Law et al., 2012a).

Based on the anaerobic ammonia oxidation (anammox) process, innovative autotrophic biological nitrogen removal (BNR) technologies have been developed as the enhanced nutrient removal processes in the past decade. Autotrophic nitritation, the pretreatment step for the anammox process, is able to provide as an electron acceptor for subsequent anammox. Autotrophic nitritation can be achieved under oxygen-limited conditions by preventing NO₂⁻ oxidation. However, the accumulation of NO₂⁻ and low dissolved oxygen (DO) have been found to trigger N₂O production (Kong et al., 2013). The autotrophic nitritation process contributes 97.5% to the N₂O production during the innovative autotrophic BNR processes (Okabe et al., 2011).

Several factors have been reported to affect N₂O production by nitrifier, such as DO concentration, NO₂⁻ levels, and the ammonium (NH₄⁺) loading rate (Kim, 2011; Peng et al., 2014, 2015). DO is a very important factor affecting N₂O production. AOB can use NO₂⁻ rather than oxygen as the electron acceptor during the process of NH₄⁺ oxidation to NH₂OH under low oxygen conditions (Peng et al., 2014). The variation of DO has a direct effect on the relative contributions of NH₂OH oxidation pathway and AOB denitrification pathway to N₂O production during nitritation. NO₂⁻ is also thought to be a critical factor influencing N₂O production by AOB. It has been found that high NO₂⁻ concentration leads to a significant increase of N₂O production by stimulating AOB denitrification, but has no or negligible effects on the NH₂OH oxidation pathways (Peng et al., 2015).

NH₄⁺ is the substrate for nitrification and the electron donor of AOB denitrification. The variation of NH₄⁺ concentration has a distinct effect on N₂O production during biological wastewater treatment for the inhibition of free ammonia (NH₃) on nitrification and autotrophic denitrification (Kim et al., 2010). Kampschreur et al. (2008) reported that a NH₄⁺ plus in aerobic condition could increase the production of N₂O during biological wastewater treatment. Few studies, however, have been specially carried out on the effect of NH₄⁺ concentration on N₂O emission during autotrophic nitritation process.

In this study, the main objective is to clarify the characteristics of N₂O emission during autotrophic nitritation under oxygen-limited conditions, as well as the effect of NH₄⁺ concentration on N₂O emission with synthetic wastewater. For these purposes, a laboratory-scale partial nitrification sequencing batch reactor (PN-SBR) was operated and N₂O emissions were measured at different NH₄⁺ concentrations. The obtained results are expected to improve the current understanding of N₂O emission in an autotrophic partial nitrifying system.

Materials and Methods

Seed and synthetic wastewater

The laboratory-scale PN-SBR system was inoculated with the activated sludge collected from the oxidation ditch of a full-scale municipal wastewater treatment plant in Xi'an, China. The concentrations of the mixed liquor suspended solids (MLSS) and mixed liquor volatile suspended solids (MLVSS) during the stable-running phase were about 1,000 and 654 mg/L, respectively. To meet the need of nutrient for AOB cultivation during the startup phase of PN, the synthetic wastewater contained mineral compounds as follows: NH₄HCO₃ (677 mg/L), KH₂PO₄ (330 mg/L), MgSO₄·7H₂O (50 mg/L), CaCl₂ (16 mg/L), NaHCO₃ (1,500 mg/L), and 1 mL of trace element stock solution per liter (Lovley and Phillips, 1988). No organic carbon was added in this experiment.

System setup and operational strategy

Experiments were performed in a cylindrical laboratory-scale SBR, which was made of plexiglass with a working volume of 7 L (40 cm in height, 16 cm in diameter). Compressed air was supplied to the reactor by an air pump through a porous stone diffuser. The air flow rate was kept constant at 60 mL/min by a flow meter to keep DO low (0.1 mg O₂/L). A magnetic stirrer was applied to guarantee the sludge and oxygen fully mixed in the reactor. The temperature of the sludge suspension was controlled at 30°C ± 1°C by using a water bath, as shown in Fig. 1. The SBR was operated in a 12-h cycle during the startup period, which consisted of four successive phases including feeding (10 min), aerating (550 min), settling (30 min), and discharging (10 min). At the end of each settle phase, 3 L of the sludge supernate was decanted from the reactor, resulting in a hydraulic retention time of 28 h. No excess sludge was discharged over the entire experiment in consideration of the long-time multiplication of autotrophic bacteria. Most of the automatic operations and online monitoring of parameters during the experiment were undertaken by several programmable timers (CHINT KG316T, China). After 2 months of cultivation, the system achieved the target of autotrophic PN (70% of the influent NH₄⁺ was converted into NO₂⁻).

FIG. 1.

Schematic diagram of sequencing batch reactor system.

Analytical methods

NH₄⁺, NO₂⁻, nitrate (NO₃⁻), MLSS, and MLVSS were analyzed according to the standard methods (APHA, 2005). Online data were continuously monitored by corresponding meters for pH (INESA PHS-3C, China), temperature (siEval TC-05B, China), and DO (HACH HQ30d). A dissolved N₂O microsensor (Unisence, Denmark) with date logged every second was adopted for online N₂O measurement in the liquid phase.

Calculations of N₂O emission rate and emission quantity

Dissolved N₂O in the liquid phase emitted to the atmosphere through diffusion and air stripping across air–water interface. Previous studies have shown that the profiles of the diffusion and air striping (diffusion was included) rates of N₂O can be described using linear equations with respect to the dissolved N₂O concentration (Zhang et al., 2012; Ge et al., 2016; Zhao et al., 2016). \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document} \begin{align*} r_{e} = KC_{{{N}_2}O}, \tag {1} \end{align*} \end{document}

where r_e is the N₂O emission rate [mg N₂O-N/(L·min)], C_N2O is the soluble N₂O concentration (mg N₂O-N/L), and K is the N₂O emission coefficient (1/min).

The N₂O emission coefficients were calculated according to the method described by Zhang et al. (2012). First, the mixed liquor in the reactor was replaced with tap water at the end of the experiment; then moderate N₂O gas was ingested into the tap water of the reactor and the decrease of N₂O concentrations was measured. The r_e under a certain condition (nonaeration/aeration) was determined by calculation of the N₂O reduction per second; finally, K was obtained by a linear fitting of r_e and C_N2O.

Results showed that the N₂O emission coefficient K in this study was 0.0032/min (coefficient of determination: R² = 0.8705) for N₂O emissions through diffusion (in the nonaeration condition) and 0.0087/min through air stripping (including diffusion, in the aeration of 60 mL/min, coefficient of determination: R² = 0.9503).

From the N₂O emission rate, the N₂O emission quantity during the period t₁–t₂ can be calculated from the following equation: \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document} \begin{align*} { \rm Q} = { \rm V} \int \limits_{ \rm t_1}^{ \rm t_2} { \rm r_e dt}, \tag{2} \end{align*} \end{document}

where Q is the N₂O emission quantity during the period t₁–t₂ (mg N₂O-N) and V is the effective liquid volume (L).

Results and Discussion

N₂O emission characteristics in a typical cycle

Figure 2 shows the profiles of NH₄⁺, NO₂⁻, NO₃⁻, N₂O, and DO concentrations and pH level in a typical cycle (NH₄⁺ of 120 mg·N/L) during the stable operation period. As shown in Fig. 2A, NH₄⁺ concentration decreased and NO₂⁻ concentration increased after the commencement of aeration. At the end of the aeration stage, the concentrations of NH₄⁺ and NO₂⁻ varied from 52.32 and 25.25 mg·N/L to 0.87 and 61.10 mg·N/L, respectively. About 98% of the NH₄⁺ was oxidized and 70% of it was converted into NO₂⁻. The NO₃⁻ concentration was lower than 11.7 mg·N/L at all times, indicating that the nitrite-oxidizing bacteria activity was at a minimal in this experiment.

FIG. 2.

Dynamics of nitrogen pollutants (A, B and D), pH and DO (C) in a typical cycle of autotrophic nitritation. DO, dissolved oxygen.

The variation of pH corresponded to the decrease of NH₄⁺ concentration (Fig 2C). The pH decreased gradually for the consumption of alkalinity result from the NH₄⁺ oxidation during this autotrophic nitritation process. When the NH₄⁺ was completely depleted, the pH increased for the rise of HCO₃⁻/CO₂ caused by continuous stripping of CO₂. The DO concentration stayed at a plateau of 0.1 mg O₂/L for the balance of oxygen delivery and consumption during the process of NH₄⁺ oxidation. When the NH₄⁺ was exhausted, DO breakthrough occurred for the rapid reduction of oxygen consumption, which implied the end of the autotrophic nitritation (Wang et al., 2003; Peng et al., 2004).

N₂O can be produced through the endogenous denitrification in the anoxic phase under the limited availability of biodegradable carbon conditions (Itokawa et al., 2001). It is known that the presence of DO has an inhibitory effect on the heterotrophic bacteria activity (Law et al., 2012b). As shown in Fig. 2D, the dissolved N₂O concentration dropped after the commencement of aeration and lasted for 1.8 h, indicating that the generation rate of N₂O was lower than the emission rate in the initial aeration stage. DO affects the activities of both AOB and heterotrophic denitrifier. N₂O emission rate from the AOB denitrification pathway and NH₂OH oxidation pathway increased as DO increased from 0 to 0.1 mg O₂/L (Peng et al., 2014). After 1.8 h of the influent injection, dissolved N₂O concentration increased for the consumption of NH₄⁺ and increase of DO concentration. NH₄⁺ is the electron donor of AOB denitrification and substrate for nitritation. The dissolved N₂O concentration decreased again when NH₄⁺ was lower than 20 mg·N/L. N₂O generation rate was dynamic during the process of autotrophic nitritation (Ju et al., 2015). Figure 2B shows that the quantity of N₂O emission grew quickly at the beginning of PN and then slowed at the end of the cycle operation. The total N₂O emission was 8.75 mg·N/L during this nitritation, accounting for about 17.0% of the NH₄⁺ oxidized.

N₂O emissions under different feed ammonium concentrations

Figure 3 shows the characteristics of nitrogen pollutants when the influent NH₄⁺ concentration increased from 60 to 240 mg·N/L. As presented in Fig. 3A, the NH₄⁺ oxidizing rates maintained constant under the different NH₄⁺ concentrations injection. It implied that the NH₄⁺ oxidation was a zero order reaction in autotrophic PN under oxygen-limited conditions. Nitritation was controlled by the limited supply of oxygen to the reactor (Kim, 2011), DO concentrations under those three conditions all maintained at 0.08 ± 0.02 mg/L. Longer reaction time is needed at a higher NH₄⁺ concentration for complete PN.

FIG. 3.

Comparisons of NH₄⁺ concentration (A), N₂O emission rate (B), N₂O emission quantity (C) and NO₂⁻ concentration (D) for R1-3 (influent NH₄⁺ concentrations: R1, 240 mg·N/L; R2, 120 mg·N/L; R3, 60 mg·N/L). N₂O, nitrous oxide.

There were 3.24, 8.75, and 24.59 mg·N/L N₂O emissions at the influent NH₄⁺ concentrations of 60, 120, and 240 mg·N/L, respectively (Fig. 3C). That means N₂O emission increased with the rise of influent NH₄⁺ concentration. Besides, the N₂O emission factor increased from 12.0% for the NH₄⁺ concentration of 60 mg·N/L to 17.0% for 120 mg·N/L and 21.7% for 240 mg·N/L. In summary, higher NH₄⁺ concentration in oxygen-limited autotrophic nitritation led to higher N₂O emissions.

It has been widely known that there are three main routes for N₂O production during the process of biological wastewater treatment: heterotrophic denitrification, NH₂OH oxidation, and AOB denitrification (Kampschreur et al., 2009).

Although the presence of a relatively small amount of heterotrophic bacteria was expected (growing on cell lysate), their effects on N₂O emission were identified through a control test. During the control test, no NH₄⁺ was added, DO was controlled at 0.1 mg O₂/L, and NO₂⁻ was kept in normal range. Therefore, the N₂O emission in this control test can be attributed to the heterotrophic activity. As shown in Fig. 4, the dissolved N₂O concentration nearly remained constant at zero after the commencement of aeration, indicating that the heterotrophic denitrification was very limited as the synthetic wastewater contains no extra organic compound at the DO concentration of 0.1 mg O₂/L.

FIG. 4.

Profile of dissolved N₂O concentration in the control test (no NH₄⁺ added at DO level of 0.1 mg O₂/L, NO₂⁻ in a normal range).

During this experiment, the N₂O emission rate from the NH₂OH oxidation pathway maintained constant for the same NH₄⁺ oxidation rate (Fig. 3A). In a similar nitrifying culture studied by Peng et al. (2014), the N₂O emission rate from the NH₂OH oxidation pathway is in positive correlation with DO concentration in the DO range of 0 to 3.0 mg O₂/L, and the N₂O emission rate through NH₂OH oxidation pathway is about 0.15 mg N/h·g VSS at DO of 0.5 mg O₂/L. Based on the N₂O emission rate through NH₂OH oxidation (0.15 mg N/h·g VSS at DO of 0.5 mg O₂/L) in the reference, the N₂O emissions through NH₂OH oxidation in this experiment were calculated as 0.83, 1.56, and 3.44 mg·N/L for the influent NH₄⁺ concentrations of 60, 120, and 240 mg·N/L, respectively. Considering the DO level in this study (0.1 mg O₂/L) was lower than 0.5 mg O₂/L, we may deduce that the N₂O emissions through NH₂OH oxidation during this experiment were less than 0.83, 1.56, and 3.44 mg·N/L at corresponding influent NH₄⁺ concentrations. That is, the ratios between the N₂O emitted by NH₂OH oxidation and the total N₂O emission were less than 25.6%, 17.8%, and 14.0% at the influent NH₄⁺ of 60, 120, and 240 mg·N/L, respectively.

Besides, NO₂⁻ is considered to be an important factor affecting N₂O production through AOB denitrification during nitritation (Peng et al., 2015). Figure 5 shows the dependency of N₂O emission rate on NO₂⁻ concentration at DO level of 0.1 mg O₂/L (during periods where NH₄⁺ was not limiting). N₂O emission rate increased linearly relative to NO₂⁻ concentration. The large N₂O emission rate at high NH₄⁺ concentration may be due to the accumulation of NO₂⁻, which has been demonstrated to have a stimulating effect on AOB denitrification by promoting the expression of the nirK gene (Beaumont et al., 2004). By the comprehensive analysis of N₂O emission rate on NO₂⁻ concentration (Fig. 5) and the absence of a contribution from heterotrophic denitrifiers, we can draw the conclusion that AOB denitrification is the main cause of N₂O emission during the oxygen-limited autotrophic nitritation process.

FIG. 5.

Effect of NO₂⁻ concentration on N₂O emission rate during oxygen-limited autotrophic nitritation (during periods where NH₄⁺ was not limiting).

Conclusions

A laboratory-scale SBR for autotrophic PN treating synthetic wastewater without organic carbon was operated to investigate the N₂O emission characteristics under oxygen-limited conditions. It could be concluded that:

• NH₄⁺ oxidation is a zero order reaction and N₂O emission significantly increased with the increase of influent NH₄⁺ concentration due to the large accumulation of NO₂⁻ under low oxygen conditions.

• AOB denitrification is the main cause of N₂O emission during the oxygen-limited autotrophic nitritation process.

Footnotes

Acknowledgment

This work was supported by the Shaanxi Province Science & Technology Development Program (Grant No. 2014K15-03-02).

Author Disclosure Statement

No competing financial interests exist.

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Effect of Ammonium Concentration on N 2 O Emission During Autotrophic Nitritation Under Oxygen-Limited Conditions

Abstract

Abstract

Introduction

Materials and Methods

Seed and synthetic wastewater

System setup and operational strategy

Analytical methods

Calculations of N2O emission rate and emission quantity

Results and Discussion

N2O emission characteristics in a typical cycle

N2O emissions under different feed ammonium concentrations

Conclusions

Footnotes

Acknowledgment

Author Disclosure Statement

References

Calculations of N₂O emission rate and emission quantity

N₂O emission characteristics in a typical cycle

N₂O emissions under different feed ammonium concentrations