Higher N<sub>2</sub>O production in sequencing batch reactors compared to continuous stirred tank reactors: effect of feast-famine cycles

doi:10.1007/s11783-023-1650-z

Front. Environ. Sci. Eng.

2023, Vol. 17

Issue (4) : 50 https://doi.org/10.1007/s11783-023-1650-z

RESEARCH ARTICLE

Higher N₂O production in sequencing batch reactors compared to continuous stirred tank reactors: effect of feast-famine cycles

Xinjie Yan^1,², Xunyu Shen^1,², Jipeng Wang³, Jinlong Zhuang^1,², Yu Wang^1,², Jinchi Yao^1,², Hong Liu⁴, Yongdi Liu^1,^2,⁵, James P. Shapleigh⁶, Wei Li^1,^2,⁵(

)

¹. National Engineering Research Center of Industrial Wastewater Detoxication and Resource Recovery, East China University of Science and Technology, Shanghai 200237, China
². State Environmental Protection Key Laboratory of Environmental Risk Assessment and Control on Chemical Process, School of Resources and Environmental Engineering, East China University of Science and Technology, Shanghai 200237, China
³. School of Environmental and Safety Engineering, Changzhou University, Changzhou 213164, China
⁴. Shanghai Huayi Group Co. Ltd., Shanghai 201108, China
⁵. Shanghai Institute of Pollution Control and Ecological Security, Shanghai 200237, China
⁶. Department of Microbiology, Cornell University, Ithaca, NY 14850, USA

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Abstract

● N₂O emissions from a denitrifying SBR were 23 times higher than that of the CSTR.

● Feast famine conditions in SBR uniquely lead to producing undesirable levels of N₂O.

● An MAG closely related to previously identified Thauera is likely a major N₂O driver.

● Post-transcriptional regulation may be linked to higher N₂O production in SBR.

Nitrous oxide (N₂O) is a potent greenhouse gas that can be emitted during the biological treatment of wastewater. In this study, a comparison of the long-term performance characteristics and N₂O production of sequencing batch reactors (SBR) and continuous stirred tank reactors (CSTR) during nitrite-based denitrification was undertaken. It was found that both reactors had NO₂⁻-N removal efficiencies over 99.9 %, but the N₂O-N emissions from the SBR reached ~2.3 % of the removal nitrite-N load, while in the CSTR it never exceeded 0.1 %. High frequency sampling during one operation cycle of the SBR demonstrated that the N₂O accumulation ratio was ~0.1 % during the feast period, increased to ~1.9 % in the first five hours of the famine period, and then gradually reached ~2.3 % at the end of famine. Batch experiments showed that limiting extracellular electron donor is required for N₂O accumulation in cells from the SBR-famine period and that cells from the CSTR do not accumulate N₂O when either nitrite or carbon is limiting. Another notable difference in the two reactor communities was the high level of accumulation of intracellular granules, most likely polyhydroxybutyrate (PHB), in cells during the feast period in the SBR. Metagenome assembly and binning found that one genome (PRO1), which is a Thauera, accounted for over half the metagenomic reads in both reactors. Neither shifts in gene regulation nor community composition explained the observed differences in reactor performance suggesting some post-transcriptional regulation obligatorily linked to antecedent conditions underly increased N₂O production in the SBR.

Keywords Denitrifying N₂O mitigation SBR CSTR Meta-omics PHB

Corresponding Author(s): Wei Li

Issue Date: 28 November 2022

Cite this article:

Xinjie Yan,Xunyu Shen,Jipeng Wang, et al. Higher N₂O production in sequencing batch reactors compared to continuous stirred tank reactors: effect of feast-famine cycles[J]. Front. Environ. Sci. Eng., 2023, 17(4): 50.

URL:

https://academic.hep.com.cn/fese/EN/10.1007/s11783-023-1650-z
https://academic.hep.com.cn/fese/EN/Y2023/V17/I4/50

Tab.1 Experimental designs and descriptions

Fig.1 Variation of NO₂^?-N concentrations and N₂O production ratio during the long-term operation of SBR and CSTR. (a) Performance of the SBR; (b) Performance of the CSTR; (c) Performance of the SBR with coupled acetate-nitrite addition during one operation cycle at day 55 (24 h): variations of BOD, NO₂^?-N and N₂O concentration. (I: feast period; II: early famine period; III: late famine period).

Fig.2 N₂O emission and denitrification rates of the different sludge types. (a₁) Sludge sampled from feast period in SBR; (a₂) Sludge sampled from early famine period in SBR; (a₃) Sludge sampled from late famine period in SBR; (b₁) Raw sludge sampled from CSTR; (b₂) Sludge sampled from CSTR and centrifuged at 5000 r/min for 10 min to remove extracellular organic substrates; (b₃) Sludge sampled from CSTR and aerated for 48 h to make conditions favorable for consumption of endogenous organic stores.

Fig.3 TEM observation of the different kinds of sludge. (a₁) Sludge sampled from feast period in SBR; (a₂) Sludge sampled from early famine period in SBR; (a₃) Sludge sampled from late famine period in SBR; (b₁) Raw sludge sampled from CSTR; (b₂) Sludge sampled from CSTR and centrifuged at 5000 r/min for 10 min to remove extracellular organic substrates; (b₃) Sludge sampled from CSTR and aerated for 48 h to make conditions favorable for consumption of endogenous organic stores.

Fig.4 Transcriptional behaviors of key genes for denitrifying N₂O reduction and PHB cycle in SBR feast, SBR early famine, SBR late famine periods and CSTR. (a) nirK, copper-containing nitrite reductase; nirS, cytochrome cd1 nitrite reductase; cnor/qnor, nitric oxide reductase cytochrome or quinol-dependent; nosZ_I and nosZ_II, nitrous oxide reductase clade I and II; (b) acs, acetyl-CoA synthetase; phaA, acetoacetyl-CoA thiolase; phaB, acetoacetyl-CoA reductase; phaC, PHB polymerase; (c) phaZ, PHB depolymerase; bdhA, d-3-hydroxybutyrate dehydrogenase. All data is shown as mean value ± standard deviation from three independent measurements.

MAGs ID	Phylum	Family	Genus	GC	Genome size (Mbp)	Completeness(%)	Contamination(%)	Abundance (%)		Relative expression (%)
MAGs ID	Phylum	Family	Genus	GC	Genome size (Mbp)	Completeness(%)	Contamination(%)	SBR	CSTR	$S B R a 1$	$S B R a 2$	$C S T R b 1$
PRO1	Proteobacteria	Rhodocyclaceae	Thauera	44.6	3.49	98.90	0.83	54.50	60.70	7.66	4.96	0.95	2.01
PRO2	Proteobacteria	Rhodocyclaceae	UBA2357	62.5	5.20	98.76	2.22	18.54	5.75	5.16	4.46	0.86	0.73
PRO3	Proteobacteria	Rhodobacteraceae	Gemmobacter_A	62.7	4.12	98.09	0.66	1.64	0.19	0.30	0.26	0.06	0.01
PRO4	Proteobacteria	Rhodocyclaceae	UBA2357	58.7	3.93	98.27	1.24	1.50	0.08	7.85	3.31	0.33	0.08
BAC1	Bacteroidota	F082	UBA6192	39.1	3.18	97.31	<0.01	0.84	0.26	5.82	9.34	2.21	1.98
PRO5	Proteobacteria	Rhodocyclaceae	Dechloromonas	64.5	3.61	96.85	0.47	0.63	0.02	0.22	0.21	0.03	<0.01
FIR1	Firmicutes	Erysipelotrichaceae	UBA2227	42.6	3.70	97.96	3.44	0.50	0.24	4.83	8.85	3.29	2.79
CHL1	Chloroflexota	Promineofilaceae	GCA-2746795	37.7	1.71	89.37	2.73	0.45	0.07	0.58	0.83	0.33	0.06
PRO6	Proteobacteria	Pseudomonadaceae	Pseudomonas_A	64.9	3.87	95.54	0.68	0.04	0.44	<0.01	0.01	<0.01	0.01
BAC2	Bacteroidota	Flavobacteriaceae	Flavobacterium	39.7	2.25	99.29	0.12	0.03	0.81	0.03	0.04	0.04	3.26
BAC3	Bacteroidota	Cyclobacteriaceae	Cecembia	66.4	4.04	91.86	1.63	0.02	0.34	0.09	0.39	0.13	2.39
BAC4	Bacteroidota	Flavobacteriaceae	Flavobacterium	59.2	5.35	82.00	2.33	0.02	0.17	0.08	0.04	0.02	0.28
FIR2	Firmicutes	Erysipelotrichaceae	UBA6182	65.3	6.21	96.54	1.42	< 0.01	0.28	0.06	0.14	0.05	6.65

Tab.2 Characteristics of the 13 high-quality draft genomes obtained in this study

Fig.5 Proposed metabolic model of the connection between PHB metabolism and denitrification in PRO1 inferred from its draft genome and transcriptional patterns. Gene expression during different phases is indicated in the shaded boxes with (a) being SBR feast period, (b) SBR early-famine period, (c) SBR late-famine period, and (d) CSTR. acs, acetyl-CoA synthetase; phaA, acetoacetyl-CoA thiolase; phaB, acetoacetyl-CoA reductase; phaC, PHB polymerase; nirS, nitrite reductase; cNorB, nitric oxide reductase; nosZ_I, nitrous oxide reductase clade I. The gene assignment for phaZ, PHB depolymerase, is uncertain given its weak homology to known depolymerases and poor expression.

1	P Anburajan , A Naresh Kumar , P C Sabapathy , G B Kim , R D Cayetano , J J Yoon , G Kumar , S H Kim . (2019). Polyhydroxy butyrate production by Acinetobacter junii BP25, Aeromonas hydrophila ATCC 7966, and their co-culture using a feast and famine strategy. Bioresource Technology, 293: 122062 https://doi.org/10.1016/j.biortech.2019.122062 pmid: 31494436
2	APHA (1998). Standard Methods for the Examinations of Water and Wastewater. Washington, DC: American Public Health Association
3	A P Arkin , R W Cottingham , C S Henry , N L Harris , R L Stevens , S Maslov , P Dehal , D Ware , F Perez , S Canon . et al.. (2018). KBase: The United States department of energy systems biology knowledgebase. Nature Biotechnology, 36(7): 566–569 https://doi.org/10.1038/nbt.4163 pmid: 29979655
4	L Bergaust , J Shapleigh , A Frostegård , L Bakken . (2008). Transcription and activities of NOx reductases in Agrobacterium tumefaciens: the influence of nitrate, nitrite and oxygen availability. Environmental Microbiology, 10(11): 3070–3081 https://doi.org/10.1111/j.1462-2920.2007.01557.x pmid: 18312398
5	A S Bhattacharjee , S Wu , C E Lawson , M S M Jetten , V Kapoor , J W S Domingo , K D McMahon , D R Noguera , R Goel . (2017). Whole-community metagenomics in two different anammox configurations: process performance and community structure. Environmental Science & Technology, 51(8): 4317–4327 https://doi.org/10.1021/acs.est.6b05855 pmid: 28306234
6	J Bollon , A Filali , Y Fayolle , S Guerin , V Rocher , S Gillot . (2016). N2O emissions from full-scale nitrifying biofilters. Water Research, 102: 41–51 https://doi.org/10.1016/j.watres.2016.05.091 pmid: 27318446
7	B Buchfink , C Xie , D H Huson . (2015). Fast and sensitive protein alignment using DIAMOND. Nature Methods, 12(1): 59–60 https://doi.org/10.1038/nmeth.3176 pmid: 25402007
8	D I Colpa , W Zhou , J P Wempe , J Tamis , M C A Stuart , J Krooneman , G W Euverink . (2020). Thauera aminoaromatica MZ1T identified as a polyhydroxyalkanoate-producing bacterium within a mixed microbial consortium. Bioengineering (Basel, Switzerland), 7(1): 19 https://doi.org/10.3390/bioengineering7010019 pmid: 32098069
9	M Conthe , P Lycus , M O Arntzen , da Silva A Ramos , Å Frostegård , L R Bakken , R Kleerebezem , Loosdrecht M C M van . (2019). Denitrification as an N2O sink. Water Research, 151: 381–387 https://doi.org/10.1016/j.watres.2018.11.087 pmid: 30616050
10	M Conthe , L Wittorf , J G Kuenen , R Kleerebezem , M C M van Loosdrecht , S Hallin . (2018). Life on N2O: deciphering the ecophysiology of N2O respiring bacterial communities in a continuous culture. ISME Journal, 12(4): 1142–1153 https://doi.org/10.1038/s41396-018-0063-7 pmid: 29416125
11	S F Corsino , R Campo , G Di Bella , M Torregrossa , G Viviani . (2016). Study of aerobic granular sludge stability in a continuous-flow membrane bioreactor. Bioresource Technology, 200: 1055–1059 https://doi.org/10.1016/j.biortech.2015.10.065 pmid: 26526094
12	M D'Alessio , R Nordeste , A C Doxey , T C Charles . (2017). Transcriptome analysis of polyhydroxybutyrate cycle mutants reveals discrete loci connecting nitrogen utilization and carbon storage in Sinorhizobium meliloti. mSystems, 2(5): e00035–17 https://doi.org/10.1128/mSystems.00035-17 pmid: 28905000
13	K Dircks , M Henze , M C M van Loosdrecht , H Mosbaek , H Aspegren . (2001). Storage and degradation of poly-β-hydroxybutyrate in activated sludge under aerobic conditions. Water Research, 35(9): 2277–2285 https://doi.org/10.1016/S0043-1354(00)00511-X pmid: 11358308
14	D R H Graf , C M Jones , S Hallin . (2014). Intergenomic comparisons highlight modularity of the denitrification pathway and underpin the importance of community structure for N2O emissions. PLoS One, 9(12): e114118 https://doi.org/10.1371/journal.pone.0114118 pmid: 25436772
15	T W Hegarty . (1973). Temperature coefficient (Q10), seed germination and other biological processes. Nature, 243: 305–306 https://doi.org/10.1038/243305a0
16	Henze M, Gujer W, Mino T, Van Loosedrecht M (2000). Activated Sludge Models ASM1, ASM2, ASM2d and ASM3. Scientific & Technical Report IWA Publishing, 9. Diepoldsau, Switzerland: IWA Publishing ISBN: 9781900222242 https://doi.org/10.2166/9781780402369
17	S Heo , Y Q Liu . (2021). Dependence of poly-β-hydroxybutyrate accumulation in sludge on biomass concentration in SBRs. Science of the Total Environment, 797: 149138 https://doi.org/10.1016/j.scitotenv.2021.149138 pmid: 34346384
18	Q Hu , L R Fan , D W Gao . (2017). Pilot-scale investigation on the treatment of cellulosic ethanol biorefinery wastewater. Chemical Engineering Journal, 309: 409–416 https://doi.org/10.1016/j.cej.2016.10.066
19	W Huang , J Zhou , X He , L He , Z Lin , S Shi , J Zhou . (2021). Simultaneous nitrogen and phosphorus removal from simulated digested piggery wastewater in a single-stage biofilm process coupling anammox and intracellular carbon metabolism. Bioresource Technology, 333: 125152 https://doi.org/10.1016/j.biortech.2021.125152 pmid: 33872997
20	D Hyatt , G L Chen , P F Locascio , M L Land , F W Larimer , L J Hauser . (2010). Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics, 11(1): 119 https://doi.org/10.1186/1471-2105-11-119 pmid: 20211023
21	IPCC . (2019). 2019 Refinement to the 2006 IPCC Guidelines for National Greenhouse Gas Inventories, Chapter 6: Wastewater Treatment and Discharge. Bangkok: IPCC, 72
22	Y Jia , M Zhou , Y Chen , Y Hu , J Luo . (2020). Insight into short-cut of simultaneous nitrification and denitrification process in moving bed biofilm reactor: effects of carbon to nitrogen ratio. Chemical Engineering Journal, 400: 125905 https://doi.org/10.1016/j.cej.2020.125905
23	X Jiang , D Mira , D L Cluff . (2018). The combustion mitigation of methane as a non-CO2 greenhouse gas. Progress in Energy and Combustion Science, 66: 176–199 https://doi.org/10.1016/j.pecs.2016.06.002
24	C M Jones , D R Graf , D Bru , L Philippot , S Hallin . (2013). The unaccounted yet abundant nitrous oxide-reducing microbial community: a potential nitrous oxide sink. ISME Journal, 7(2): 417–426 https://doi.org/10.1038/ismej.2012.125 pmid: 23151640
25	M Jones , T Stephenson . (1996). The effects of temperature on enhanced biological phosphate removal. Environmental Technology, 17(9): 965–976 https://doi.org/10.1080/09593331708616465
26	D D Kang , J Froula , R Egan , Z Wang . (2015). MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. PeerJ, 3(8): e1165 https://doi.org/10.7717/peerj.1165 pmid: 26336640
27	T R Kent , C B Bott , Z W Wang . (2018). State of the art of aerobic granulation in continuous flow bioreactors. Biotechnology Advances, 36(4): 1139–1166 https://doi.org/10.1016/j.biotechadv.2018.03.015 pmid: 29597030
28	B Langmead , S L Salzberg . (2012). Fast gapped-read alignment with Bowtie 2. Nature Methods, 9(4): 357–359 https://doi.org/10.1038/nmeth.1923 pmid: 22388286
29	O Larriba , E Rovira-Cal , Z Juznic-Zonta , A Guisasola , J A Baeza . (2020). Evaluation of the integration of P recovery, polyhydroxyalkanoate production and short cut nitrogen removal in a mainstream wastewater treatment process. Water Research, 172: 115474 https://doi.org/10.1016/j.watres.2020.115474 pmid: 31958593
30	D Li , C M Liu , R Luo , K Sadakane , T W Lam . (2015). MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics (Oxford, England), 31(10): 1674–1676 https://doi.org/10.1093/bioinformatics/btv033 pmid: 25609793
31	W Li , Z Y Cai , Z J Duo , Y F Lu , K X Gao , G Abbas , M Zhang , P Zheng . (2017). Heterotrophic ammonia and nitrate bio-removal over nitrite (Hanbon): performance and microflora. Chemosphere, 182: 532–538 https://doi.org/10.1016/j.chemosphere.2017.05.068 pmid: 28521169
32	W Li , H Li , Y D Liu , P Zheng , J P Shapleigh . (2018a). Salinity-aided selection of progressive onset denitrifiers as a means of providing nitrite for anammox. Environmental Science & Technology, 52(18): 10665–10672 https://doi.org/10.1021/acs.est.8b02314 pmid: 30148965
33	W Li , S Liu , M Zhang , H P Zhao , P Zheng . (2018b). Oxidation of organic electron donor by denitratation: performance, pathway and key microorganism. Chemical Engineering Journal, 343: 554–560 https://doi.org/10.1016/j.cej.2018.02.112
34	W Li , J L Zhuang , Y Y Zhou , F G Meng , D Kang , P Zheng , J P Shapleigh , Y D Liu . (2020). Metagenomics reveals microbial community differences lead to differential nitrate production in anammox reactors with differing nitrogen loading rates. Water Research, 169: 115279 https://doi.org/10.1016/j.watres.2019.115279 pmid: 31734392
35	B Liu , Y Mao , L Bergaust , L R Bakken , A Frostegård . (2013). Strains in the genus Thauera exhibit remarkably different denitrification regulatory phenotypes. Environmental Microbiology, 15(10): 2816–2828 pmid: 23663391
36	M L D Lopez , Y Y Lin , M Sato , C H Hsieh , F K Shiah , R J Machida . (2022). Using metatranscriptomics to estimate the diversity and composition of zooplankton communities. Molecular Ecology Resources, 22(2): 638–652 https://doi.org/10.1111/1755-0998.13506 pmid: 34555254
37	P Lycus , Bøthun K Lovise , L Bergaust , Shapleigh J Peele , Bakken L Reier , Å Frostegård . (2017). Phenotypic and genotypic richness of denitrifiers revealed by a novel isolation strategy. ISME Journal, 11(10): 2219–2232 https://doi.org/10.1038/ismej.2017.82 pmid: 28696424
38	C Ma , M M Jensen , B F Smets , B Thamdrup . (2017). Pathways and controls of N2O production in nitritation-anammox biomass. Environmental Science & Technology, 51(16): 8981–8991 https://doi.org/10.1021/acs.est.7b01225 pmid: 28669192
39	S Nurk , D Meleshko , A Korobeynikov , P A Pevzner . (2017). metaSPAdes: a new versatile metagenomic assembler. Genome Research, 27(5): 824–834 https://doi.org/10.1101/gr.213959.116 pmid: 28298430
40	S Obruca, P Sedlacek, F Mravec, V Krzyzanek, J Nebesarova, O Samek, D Kucera, P Benesova, K Hrubanova, M Milerova, I Marova (2017). The presence of PHB granules in cytoplasm protects non-halophilic bacterial cells against the harmful impact of hypertonic environments. New Biotechnology, 39(Pt A): 68–80 https://doi.org/10.1016/j.nbt.2017.07.008 pmid: 28736192
41	M R Olm , C T Brown , B Brooks , J F Banfield . (2017). dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication. ISME Journal, 11(12): 2864–2868 https://doi.org/10.1038/ismej.2017.126 pmid: 28742071
42	M R Olm , A Crits-Christoph , K Bouma-Gregson , B A Firek , M J Morowitz , J F Banfield . (2021). inStrain profiles population microdiversity from metagenomic data and sensitively detects shared microbial strains. Nature Biotechnology, 39(6): 727–736 https://doi.org/10.1038/s41587-020-00797-0 pmid: 33462508
43	P Pagáčová , K Galbová , M Drtil , I Jonatová . (2010). Denitrification in USB reactor with granulated biomass. Bioresource Technology, 101(1): 150–156 https://doi.org/10.1016/j.biortech.2009.08.021 pmid: 19716692
44	M Pertea , G M Pertea , C M Antonescu , T C Chang , J T Mendell , S L Salzberg . (2015). StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nature Biotechnology, 33(3): 290–295 https://doi.org/10.1038/nbt.3122 pmid: 25690850
45	L Philippot , J Andert , C M Jones , D Bru , S Hallin . (2011). Importance of denitrifiers lacking the genes encoding the nitrous oxide reductase for N2O emissions from soil. Global Change Biology, 17(3): 1497–1504 https://doi.org/10.1111/j.1365-2486.2010.02334.x
46	S J Qiu , J J Liu , L Zhang , Q Zhang , Y Z Peng . (2021). Sludge fermentation liquid addition attained advanced nitrogen removal in low C/N ratio municipal wastewater through short-cut nitrification-denitrification and partial anammox. Frontiers of Environmental Science & Engineering, 15(2): 26 https://doi.org/10.1007/s11783-020-1318-x
47	J C Quagliano , S S Miyazaki . (1997). Effect of aeration and carbon/nitrogen ratio on the molecular mass of the biodegradable polymer poly-β-hydroxybutyrate obtained from Azotobacter chroococcum 6B. Applied Microbiology and Biotechnology, 48(5): 662–664 https://doi.org/10.1007/s002530051112
48	T Ren , Y Chi , Y Wang , X Shi , X Jin , P Jin . (2021). Diversified metabolism makes novel Thauera strain highly competitive in low carbon wastewater treatment. Water Research, 206: 117742 https://doi.org/10.1016/j.watres.2021.117742 pmid: 34653797
49	C A Roco , L L Bergaust , L R Bakken , J B Yavitt , J P Shapleigh . (2017). Modularity of nitrogen-oxide reducing soil bacteria: linking phenotype to genotype. Environmental Microbiology, 19(6): 2507–2519 https://doi.org/10.1111/1462-2920.13250 pmid: 26914200
50	J L Rombouts , G Mos , D G Weissbrodt , R Kleerebezem , M C M Van Loosdrecht . (2019). Diversity and metabolism of xylose and glucose fermenting microbial communities in sequencing batch or continuous culturing. FEMS Microbiology Ecology, 95(2): fiy233 https://doi.org/10.1093/femsec/fiy233 pmid: 30508079
51	R A Sanford , D D Wagner , Q Wu , J C Chee-Sanford , S H Thomas , C Cruz-García , G Rodríguez , A Massol-Deyá , K K Krishnani , K M Ritalahti , S Nissen , K T Konstantinidis , F E Löffler . (2012). Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils. Proceedings of the National Academy of Sciences of the United States of America, 109(48): 19709–19714 https://doi.org/10.1073/pnas.1211238109 pmid: 23150571
52	P D Sarmiento-Pavía, M E Sosa-Torres (2021). Bioinorganic insights of the PQQ-dependent alcohol dehydrogenases. European Journal of Biochemistry, 26(2–3): 177–203 https://doi.org/10.1007/s00775-021-01852-0 pmid: 33606117
53	S Schalk-Otte , R J Seviour , J G Kuenen , M S M Jetten . (2000). Nitrous oxide (N2O) production by Alcaligenes faecalis during feast and famine regimes. Water Research, 34(7): 2080–2088 https://doi.org/10.1016/S0043-1354(99)00374-7
54	Y D Scherson , G F Wells , S G Woo , J Lee , J Park , B J Cantwell , C S Criddle . (2013). Nitrogen removal with energy recovery through N2O decomposition. Energy & Environmental Science, 6(1): 241–248 https://doi.org/10.1039/c2ee22487a
55	Y D Scherson , S G Woo , C S Criddle . (2014). Production of nitrous oxide from anaerobic digester centrate and its use as a co-oxidant of biogas to enhance energy recovery. Environmental Science & Technology, 48(10): 5612–5619 https://doi.org/10.1021/es501009j pmid: 24780056
56	X Y Shen , Y Y Zhuge , Y D Liu , J P Shapleigh , W Li . (2021). Long-term effects of acetylene on denitrifying N2O production: Biomass performance and microbial community. Journal of Water Process Engineering, 42: 102137 https://doi.org/10.1016/j.jwpe.2021.102137
57	Y Sun , B Angelotti , M Brooks , Z W Wang . (2021). Feast/famine ratio determined continuous flow aerobic granulation. Science of the Total Environment, 750: 141467 https://doi.org/10.1016/j.scitotenv.2020.141467 pmid: 32853933
58	H Tian , R Xu , J G Canadell , R L Thompson , W Winiwarter , P Suntharalingam , E A Davidson , P Ciais , R B Jackson , G Janssens-Maenhout . et al.. (2020). A comprehensive quantification of global nitrous oxide sources and sinks. Nature, 586(7828): 248–256 https://doi.org/10.1038/s41586-020-2780-0 pmid: 33028999
59	M A Trainer , D Capstick , A Zachertowska , K N Lam , S R D Clark , T C Charles . (2010). Identification and characterization of the intracellular poly-3-hydroxybutyrate depolymerase enzyme PhaZ of Sinorhizobium meliloti. BMC Microbiology, 10(1): 92 https://doi.org/10.1186/1471-2180-10-92 pmid: 20346169
60	J P Wang , Y D Liu , F G Meng , W Li . (2020). The short- and long-term effects of formic acid on rapid nitritation start-up. Environment International, 135: 105350 https://doi.org/10.1016/j.envint.2019.105350 pmid: 31812826
61	Q Wang , J He . (2020). Complete nitrogen removal via simultaneous nitrification and denitrification by a novel phosphate accumulating Thauera sp. strain SND5. Water Research, 185: 116300 https://doi.org/10.1016/j.watres.2020.116300 pmid: 32823196
62	Z Xu , X Dai , X Chai . (2018). Effect of different carbon sources on denitrification performance, microbial community structure and denitrification genes. Science of the Total Environment, 634: 195–204 https://doi.org/10.1016/j.scitotenv.2018.03.348 pmid: 29627542
63	Q Yang , B Cui , Y Zhou , J Li , Z Liu , X Liu . (2020). Impact of gas-water ratios on N2O emissions in biological aerated filters and analysis of N2O emissions pathways. Science of the Total Environment, 723: 137984 https://doi.org/10.1016/j.scitotenv.2020.137984 pmid: 32213406
64	J Zhang , Y Zhang , X Quan . (2012). Electricity assisted anaerobic treatment of salinity wastewater and its effects on microbial communities. Water Research, 46(11): 3535–3543 https://doi.org/10.1016/j.watres.2012.03.059 pmid: 22516174
65	F Zhou , W Z Xiao , K Y Zhou , J L Zhuang , X Zhang , Y D Liu , B J Ni , J P Shapleigh , M Zhou , X Z Luo , W Li . (2022). Performance characteristics and community analysis of a single-stage partial nitritation, anammox and denitratation (SPANADA) integrated process for treating low C/N ratio wastewater. Chemical Engineering Journal, 433: 134452 https://doi.org/10.1016/j.cej.2021.134452
66	J L Zhuang , X Sun , W Q Zhao , X Zhang , J J Zhou , B J Ni , Y D Liu , J P Shapleigh , W Li . (2022). The anammox coupled partial-denitrification process in an integrated granular sludge and fixed-biofilm reactor developed for mainstream wastewater treatment: Performance and community structure. Water Research, 210: 117964 https://doi.org/10.1016/j.watres.2021.117964 pmid: 34959064
67	J L Zhuang , Y Y Zhou , Y D Liu , W Li . (2020). Flocs are the main source of nitrous oxide in a high-rate anammox granular sludge reactor: insights from metagenomics and fed-batch experiments. Water Research, 186: 116321 https://doi.org/10.1016/j.watres.2020.116321 pmid: 32861184
68	Y Y Zhuge , X Y Shen , Y D Liu , J Shapleigh , W Li . (2020). Application of acidic conditions and inert-gas sparging to achieve high-efficiency nitrous oxide recovery during nitrite denitrification. Water Research, 182: 116001 https://doi.org/10.1016/j.watres.2020.116001 pmid: 32544733

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[3]	Xiaoyan Song, Rui Liu, Lujun Chen, Baogang Dong, Tomoki Kawagishi. Advantages of intermittently aerated SBR over conventional SBR on nitrogen removal for the treatment of digested piggery wastewater[J]. Front. Environ. Sci. Eng., 2017, 11(3): 13-.
[4]	Di CUI,Ang LI,Tian QIU,Rui CAI,Changlong PANG,Jihua WANG,Jixian YANG,Fang MA,Nanqi REN. Improvement of nitrification efficiency by bioaugmentation in sequencing batch reactors at low temperature[J]. Front. Environ. Sci. Eng., 2014, 8(6): 937-944.
[5]	Xinyan ZHANG, Binbin WANG, Qingqing HAN, Hongmei ZHAO, Dangcong PENG. Effects of shear force on formation and properties of anoxic granular sludge in SBR[J]. Front Envir Sci Eng, 2013, 7(6): 896-905.
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[9]	YANG Qing, PENG Yongzhen, YANG Anming, LI Jianfeng, GUO Jianhua. Advanced nitrogen removal by pulsed sequencing batch reactors (SBR) with real-time control[J]. Front.Environ.Sci.Eng., 2007, 1(4): 488-492.
[10]	YANG Qing, WANG Shuying, YANG Anming, GUO Jianhua, BO Fengyang. Advanced nitrogen removal using pilot-scale SBR with intelligent control system built on three layer network[J]. Front.Environ.Sci.Eng., 2007, 1(1): 33-38.
[11]	ZENG Wei, PENG Yongzhen, WANG Shuying. Process evaluation of an alternating aerobic-anoxic process applied in a sequencing batch reactor for nitrogen removal[J]. Front.Environ.Sci.Eng., 2007, 1(1): 28-32.
[12]	YUAN Linjiang, HAN Wei, WANG Lei, YANG Yongzhe, WANG Zhiying. Simultaneous denitrifying phosphorus accumulation in a sequencing batch reactor[J]. Front.Environ.Sci.Eng., 2007, 1(1): 23-27.

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