Research article
Impact of anaerobic digestion on reactive nitrogen gas emissions from dairy slurry storage

https://doi.org/10.1016/j.jenvman.2022.115306Get rights and content

Highlights

  • BS emitted lower NH3 (50%) but higher N2O (24.4 times) and NO (2.9 times) than RS.

  • Low slurry OM was key reason for DO increase and N2O emissions in BS.

  • amoA gene functioned to N2O emission with correlation factor of 0.54 (p < 0.01).

  • Nitrification and incomplete denitrification dominated N2O emission in BS.

  • Nitrosomonas and Vulcanibacillus were key bacteria functioned in N2O emission.

Abstract

Biogas digesters are commonly used to treat animal manure/slurry, and abundant digested slurry is generated during the digestion process. Gas emissions from digested and raw slurry may vary with the change in slurry parameters after digestion, but the mechanism is not well understood. Gas emissions from raw dairy slurry (RS) and digested dairy slurry (BS) during 98 days of storage were investigated in this study to evaluate the effects of anaerobic digestion on reactive nitrogen emissions from slurry storage. Results showed that much higher N2O and NO emission and lower NH3 emission was achieved in BS than in RS. The mean gaseous emission of RS and BS accounted for 27.8% ± 6.9% and 17.1% ± 2.3% of the initial TN for NH3, 0.1% ± 0.1% and 3.5% ± 1.6% of the initial TN for N2O, and 0.0% ± 0.0% and 0.2% ± 0.0% of the initial TN for NO, respectively. Among all detected N2O-forming and reducing microbial genes, the abundance of amoA genes was the most closely related to N2O flux (r = 0.54, p < 0.01). More aerobic conditions occurred in BS, and dissolved oxygen (DO) increased to 0.4–1.6 mg L−1 after 35 days because the low organic matter of BS resulted in good infiltration of surface air into the slurry. The increased DO stimulated the growth of Nitrosomonas and the increase in amoA gene copies and contributed to the high N2O and NO emissions in BS through the nitrification process. Vulcanibacillus, Thauera, Castellaniella, and Thermomonas were the major denitrifying bacteria that occurred in BS and caused an incomplete denitrification process, which could be another reason for the increase in N2O and NO emissions from BS. Our study indicated that anaerobic digestion reduced the organic matter content of the slurry and caused an active microbial environment that facilitated the transformation of slurry N to N2O in BS storage, thus lowering the NH3 emission compared with RS storage. Therefore, aside from NH3, N2O should also be preferentially mitigated during BS storage because N2O is a greenhouse gas with high global warming potential.

Introduction

Reactive N-related gas emissions (i.e., ammonia (NH3), nitrous oxide (N2O), and nitric oxide (NO)) is an important issue that may cause damage to human health and the global environment (Cui et al., 2013). NH3 is one of the most hazardous gases. Massive NH3 emission can cause water eutrophication and soil acidification and supports haze formation (Liu et al., 2019). N2O is a primary and powerful non-CO2 greenhouse gas (GHG) whose per unit radiative forcing is 265 times that of CO2 (IPCC, 2013). The importance of controlling non-CO2 GHG emission for combating climate change has been increasing based on the current global climate action. As one of the primary components of air pollution, NO is a prominent cause of premature death of human beings and universal biodiversity decline (Almaraz et al., 2018). Animal manure management is considered a vital source of reactive nitrogen gases because the proportions of NH3 and N2O from livestock production could reach 60% and 21% of the global emission, respectively (Uwizeye et al., 2020; Tian et al., 2020). Animal slurry is largely produced from dairy and pig farms. It cannot be discharged directly because it would degrade water quality due to the abundant organic matter, nitrogen, phosphorous, saline elements, and pathogens; meanwhile, slurry treatment, such as organic matter removal, disinfection, and desalination, usually brings additional costs to farmers (Panagopoulos, 2022; Duerschner et al., 2020). For simplicity, animal slurry is usually stored for several months before it is finally applied to land. With the abundant nitrogen content and liquid management form of animal slurry, animal slurry storage has been found to be related with high NH3 emission, and N2O and NO emissions occur simultaneously during the transformation of the nitrogen component for nitrification and denitrification processes (Wang et al., 2016, 2017; Zhang et al., 2022).

Anaerobic digestion systems have been broadly applied to treat animal manure due to the benefit of biogas production and organic matter removal, and they produce large amounts of digested slurry (Mancini and Raggi, 2021). Digestion leads to a substantial change in the major substrate parameters of the slurry, such as pH, viscosity, organic matter content, and ammonia concentration (Clemens et al., 2006; Page et al., 2015). Modifications in slurry composition are likely to affect C and N dynamics during the subsequent slurry storage and the soil after land application and ultimately influence reactive nitrogen emissions.

Abundant information has been presented for the comparison of N2O emission from the land application of slurry before and after digestion. The results vary, and the mechanism has been deeply discussed. Some studies found a lower N2O emission from digested slurry than raw slurry due to the low labile C input necessary to support heterotrophic microbial activity (Grave et al., 2018; Rodhe et al., 2015). An opposite result was reported by Saunders et al. (2012), that is, digested slurry increases nitrifier and denitrifier gene copies that are correlated with N2O production. Meanwhile, some studies have reported comparable results for the two types of slurry (Amon et al., 2006; Clemens et al., 2006; Thomsen et al., 2010). With regard to the slurry storage process, Holly et al. (2017) and Koirala et al. (2013) reported that anaerobic fermentation may increase the NH4+ + NH3 concentration in digested slurry; as a result, higher NH3 emission was obtained from stored digested slurry than raw slurry. However, an opposite result was derived by Amon et al. (2006) and Wang et al. (2014), who reported that NH4+-N transformation to NO3-N leads to a lower NH3 emission but higher N2O emission during digested slurry storage than raw slurry storage. In addition, Clemens et al. (2006) also reported that digestion leads to a higher N2O emission than raw slurry. They also stated that the slurry structure changes, thus influencing the potential for nitrification and denitrification. However, some studies have reported only negligible N2O emission from slurry storage possibly because a short storage period (12 days) is not enough to trigger the growth of nitrifying microbials (Pereira et al., 2012). In addition, information on NO emission sourcing from the manure management sector is scarce, but NO is an important component of nitrification and denitrification and can help explain the N transformation mechanism (Liao et al., 2020). Therefore, the digestion process seems to make digested slurry achieve a higher N2O emission potential than raw slurry, but further data are needed to confirm this hypothesis, and the key internal slurry property that triggers the difference is yet to be explored. Meanwhile, the microbiological processes regulating the emissions from stored slurry still remain poorly understood.

Nitrifiers and denitrifiers are the key microbials in determining N transformation. N2O, as a by-product, can be emitted during the process of nitrification and nitrifier denitrification, which is completed primarily by ammonia-oxidizing bacteria (AOB) (Law et al., 2012). N2O is a well-known essential intermediate in the heterotrophic denitrification pathway. By quantifying the evolution of functional genes involved in nitrification (amoA, hao, and nxrA) and denitrification (narG, nirS, nirK, norB, and nosZ), the key microbial processes that regulate N2O emissions in a wide range of conditions, such as compost, water treatment, and soil, have been identified (Lin et al., 2017; Sui et al., 2020; Zhang et al., 2017; Grave et al., 2018). For animal slurry storage, only a few studies have monitored the change in amoA gene copies (Hansen et al., 2009; Nielsen et al., 2010), and literature on exploring the possible microbial pathways via a systematic study of the functional genes is still unavailable.

The primary aim of this study is to assess the characteristics of the three reactive nitrogen gases (NH3, N2O, and NO) emitted from dairy slurry storage before and after digestion. We hypothesized that the reactive nitrogen gas emissions from digested slurry are higher than those from raw slurry because anaerobic digestion changes the internal slurry properties and thus influences the microbiological processes involved in nitrogen transformation. Emphasis was placed on identifying the key slurry property parameters and the dominant microbial pathway in determining N emissions via the quantification of functional genes.

Section snippets

Raw dairy slurry and digested dairy slurry

Collection of raw dairy slurry (RS) and digested dairy slurry (BS) was completed in a commercial dairy farm in Miyun District of Beijing, China. The manure on the dairy barn floor was scraped out frequently to an outdoor storage tank, and scraping was followed by water flushing to clean the residuals remaining on the floor. The manure and flushing water were mixed in the storage tank and used as an influent for a mesophilic up-flow anaerobic sludge blanket reactor with a working volume of 5000 m

Chemical properties of RS and BS during storage

Much lower organic matter content was contained in the initial BS than RS because the anaerobic fermentation in the biogas digester decomposed much of the organic matter to CH4 and CO2, causing the related indices, such as COD, DM, and VS, to be 26%–43% lower than those in the initial RS. A relatively lower TN concentration was detected in the initial BS than in RS. The TN concentrations of RS and BS decreased by 27.5% and 40.3%, respectively, after 98 days of storage, indicating a large loss

Conclusion

Reactive nitrogen gas emission differed significantly between RS and BS slurry storage, with higher N2O and NO emission and lower NH3 emission in BS than in RS. The mean (±SD) emission fluxes over the 98-day storage period for RS and BS were 2.8 ± 0.6 and 1.4 ± 0.2 g NH3 m−2 d−1, 15.1 ± 16.8 and 368.0 ± 159.2 mg N2O m−2 d−1, and 8.5 ± 6.4 and 25.0 ± 3.8 mg NO m−2 d−1, respectively. The emission from RS and BS accounted for 27.8% ± 6.9% and 17.1% ± 2.3% of the initial TN for NH3, 0.1% ± 0.1% and

CRediT authorship contribution statement

Yue Wang: Conceptualization, Investigation, Writing – original draft. Lina Liang: Investigation. Jingyi Liu: Investigation. Dongpo Guo: Writing – review & editing. Zhiping Zhu: Funding acquisition, Writing – review & editing. Hongmin Dong: Funding acquisition, Supervision.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

This work was supported by National Natural Science Foundation of China [grant number 32172778], Central Public-interest Scientific Institution Basal Research Fund, Chinese Academy of Agricultural Sciences (No. Y2022QC07), International Science & Technology Innovation Program of Chinese Academy of Agricultural Sciences (CAASTIP) [grant number CAAS-ZDRW202110], Young Elite Scientists Sponsorship Program by CAST, China [grant number 2020QNRC001].

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