Enhanced Denitrification in Constructed Wetlands with Low Carbon/Nitrogen Ratios: Insights into Reallocation of Carbon Metabolism Based on Electron Utilization

Hong-Tao Shi, Xiao-Chi Feng, Zi-Jie Xiao, Chen-Yi Jiang, Wen-Qian Wang, Qin-Yao Zeng, Bo-Wen Yang, Qi-Shi Si, Qing-Lian Wu, Nan-Qi Ren

Engineering ›› 2025, Vol. 45 ›› Issue (2) : 222-233.

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Engineering ›› 2025, Vol. 45 ›› Issue (2) : 222-233. DOI: 10.1016/j.eng.2024.07.020
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Article

Enhanced Denitrification in Constructed Wetlands with Low Carbon/Nitrogen Ratios: Insights into Reallocation of Carbon Metabolism Based on Electron Utilization

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Abstract

Constructed wetlands (CWs) are a promising method to treat effluent from wastewater treatment plants (WWTPs). However, low carbon/nitrogen (C/N) ratios of the influent inhibit denitrification in CWs, resulting in poor nitrogen removal efficiency. Herein, we compared traditional (control), biochar (BC), and β-cyclodextrin-functionalized biochar (BC@β-CD) CW systems to investigate nitrogen removal from influent with low C/N ratios, and the mechanisms that enhance this process. The highest nitrogen removal rates were observed in the BC@β-CD group, with rates 45.89% and 42.48% higher than those of the control, accompanied by a 70.57% and 85.45% decrease in nitrous oxide release, when the C/N ratio decreased from 4 to 2, respectively. Metagenomic and enzymatic analyses indicated that BC@β-CD enhances nitrogen removal by coordinately promoting carbon metabolism and increasing denitrification enzyme activities, without affecting microbial species diversity in CWs. Structural equation modeling confirmed that the foremost advantages of BC@β-CD were effective electron generation and transportation resulting from increased activities of nicotinamide adenine dinucleotide (NADH) dehydrogenase and the electron transfer system (ETS), thereby strategically reallocating more carbon metabolic flow to support denitrification. Our results show that the application of BC@β-CD in CWs to optimize the reallocation of electrons from carbon metabolism is a feasible strategy to enhance denitrification under low C/N conditions.

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Keywords

Constructed wetland / β-Cyclodextrin / Biochar / Nitrogen removal / Carbon metabolism / Electron transfer efficiency

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Hong-Tao Shi, Xiao-Chi Feng, Zi-Jie Xiao, Chen-Yi Jiang, Wen-Qian Wang, Qin-Yao Zeng, Bo-Wen Yang, Qi-Shi Si, Qing-Lian Wu, Nan-Qi Ren. Enhanced Denitrification in Constructed Wetlands with Low Carbon/Nitrogen Ratios: Insights into Reallocation of Carbon Metabolism Based on Electron Utilization. Engineering, 2025, 45(2): 222‒233 https://doi.org/10.1016/j.eng.2024.07.020

References

[1]
Luo F, Zhang J, Wei Q, Jiang Z, Jiang D, Liu S, et al.Insights into the relationship between denitrification and organic carbon release of solid-phase denitrification systems: mechanism and microbial characteristics.Bioresour Technol 2022; 364:128044.
[2]
Chen J, Guo F, Wu F, Bryan BA.Costs and benefits of constructed wetlands for meeting new water quality standards from China’s wastewater treatment plants.Resour Conserv Recycling 2023; 199:107248.
[3]
Wang X, Liu J, Ren N, Yu H, Lee D, Guo X.Assessment of multiple sustainability demands for wastewater treatment alternatives: a refined evaluation scheme and case study.Environ Sci Technol 2012; 46(10):5542-5549.
[4]
Zhang Y, Zhang C, Qiu Y, Li B, Pang H, Xue Y, et al.Wastewater treatment technology selection under various influent conditions and effluent standards based on life cycle assessment.Resour Conserv Recycling 2020; 154:104562.
[5]
He T, Guan W, Luan Z, Xie S.Spatiotemporal variation of bacterial and archaeal communities in a pilot-scale constructed wetland for surface water treatment.Appl Microbiol Biotechnol 2016; 100(3):1479-1488.
[6]
Liang Y, Wang Q, Huang L, Liu M, Wang N, Chen Y.Insight into the mechanisms of biochar addition on pollutant removal enhancement and nitrous oxide emission reduction in subsurface flow constructed wetlands: microbial community structure, functional genes and enzyme activity.Bioresour Technol 2020; 307:123249.
[7]
Wan R, Li X, Wang L, Yang G, Zheng X, Zha Y, et al.Ionic copper strengthens the toxicity of tetrabromobisphenol A (TBBPA) to denitrification by decreasing substrate transport and electron transfer.J Hazard Mater 2021; 416:126203.
[8]
Wang H, Li Y, Zhang S, Li D, Liu X, Wang W, et al.Effect of influent feeding pattern on municipal tailwater treatment during a sulfur-based denitrification constructed wetland.Bioresour Technol 2020; 315:123807.
[9]
Yan Y, Jin K, Huang H, Wang Y, Li T, Wang L, et al.Estrogen toxicity reduction of industrial biochemical tailwater by electrolysis biofilters with ceramsite–sulfur–siderite fillers.Sci Total Environ 2023; 864:161103.
[10]
Wang H, Liu Y, Yang Y, Fang Y, Luo S, Cheng H, et al.Element sulfur-based autotrophic denitrification constructed wetland as an efficient approach for nitrogen removal from low C/N wastewater.Water Res 2022; 226:119258.
[11]
Li Y, Han Q, Li B.Engineering-scale application of sulfur-driven autotrophic denitrification wetland for advanced treatment of municipal tailwater.Bioresour Technol 2023; 379:129035.
[12]
Li M, Su Y, Chen Y, Wan R, Zheng X, Liu K.The effects of fulvic acid on microbial denitrification: promotion of NADH generation, electron transfer, and consumption.Appl Microbiol Biotechnol 2016; 100(12):5607-5618.
[13]
Zhang Y, Xie Z, Lu C, Guo J, Chen Z, Li H, et al.Study on the electron transfer capability of porphyrin ring and the mechanisms in the catalytic denitrification.Biochem Eng J 2021; 175:108010.
[14]
Deng S, Chen J, Chang J.Application of biochar as an innovative substrate in constructed wetlands/biofilters for wastewater treatment: performance and ecological benefits.J Clean Prod 2021; 293:126156.
[15]
Guo F, Zhang J, Yang X, He Q, Ao L, Chen Y.Impact of biochar on greenhouse gas emissions from constructed wetlands under various influent chemical oxygen demand to nitrogen ratios.Bioresour Technol 2020; 303:122908.
[16]
Shi S, He L, Zhou Y, Fan X, Lin Z, He X, et al.Response of nitrogen removal performance and microbial community to a wide range of pH in thermophilic denitrification system.Bioresour Technol 2022; 352:127061.
[17]
Shi H, Feng X, Xiao Z, Jiang C, Wang W, Zhang X, et al.How β-cyclodextrin-functionalized biochar enhanced biodenitrification in low C/N conditions via regulating substrate metabolism and electron utilization.Environ Sci Technol 2023; 57(30):11122-11133.
[18]
Rice E, Baird R, Eaton A.Standard methods for the examination of water & wastewater. (23st ed.), American Public Health Association, Washington, DC (2017)
[19]
Rosamond MS, Thuss SJ, Schiff SL.Dependence of riverine nitrous oxide emissions on dissolved oxygen levels.Nat Geosci 2012; 5(10):715-718.
[20]
Wan R, Chen Y, Zheng X, Su Y, Li M.Effect of CO2 on microbial denitrification via inhibiting electron transport and consumption.Environ Sci Technol 2016; 50(18):9915-9922.
[21]
Qu J, Yuan Y, Meng Q, Zhang G, Deng F, Wang L, et al.Simultaneously enhanced removal and stepwise recovery of atrazine and Pb(II) from water using β–cyclodextrin functionalized cellulose: characterization, adsorptive performance and mechanism exploration.J Hazard Mater 2020; 400:123142.
[22]
Qu J, Dong M, Wei S, Meng Q, Hu L, Hu Q, et al.Microwave-assisted one pot synthesis of β-cyclodextrin modified biochar for concurrent removal of Pb(II) and bisphenol a in water.Carbohydr Polym 2020; 250:117003.
[23]
Wang H, Liu Y, Zeng G, Hu X, Hu X, Li T, et al.Grafting of β-cyclodextrin to magnetic graphene oxide via ethylenediamine and application for Cr(VI) removal.Carbohydr Polym 2014; 113:166-173.
[24]
Li C, Zhang L, Zhang S, Gholizadeh M, Hu X.Impacts of temperature on hydrophilicity/functionalities of char and evolution of bio-oil/gas in pyrolysis of pig manure.Fuel 2022; 323:124330.
[25]
Jiang Y, Khan A, Huang H, Tian Y, Yu X, Xu Q, et al.Using nano-attapulgite clay compounded hydrophilic urethane foams (AT/HUFs) as biofilm support enhances oil-refinery wastewater treatment in a biofilm membrane bioreactor.Sci Total Environ 2019; 646:606-617.
[26]
Fu X, Hou R, Yang P, Qian S, Feng Z, Chen Z, et al.Application of external carbon source in heterotrophic denitrification of domestic sewage: a review.Sci Total Environ 2022; 817:153061.
[27]
Shao Q, Zhang Y, Liu Z, Long L, Liu Z, Chen Y, et al.Phosphorus and nitrogen recovery from wastewater by ceramsite: adsorption mechanism, plant cultivation and sustainability analysis.Sci Total Environ 2022; 805:150288.
[28]
Zhao Z, Wang B, Zhang X, Xu H, Cheng N, Feng Q, et al.Release characteristics of phosphate from ball-milled biochar and its potential effects on plant growth.Sci Total Environ 2022; 821:153256.
[29]
He Y, Liu Y, Yan M, Zhao T, Liu Y, Zhu T, et al.Insights into N2O turnovers under polyethylene terephthalate microplastics stress in mainstream biological nitrogen removal process.Water Res 2022; 224:119037.
[30]
Wu Z, Xu F, Yang C, Su X, Guo F, Xu Q, et al.Highly efficient nitrate removal in a heterotrophic denitrification system amended with redox-active biochar: a molecular and electrochemical mechanism.Bioresour Technol 2019; 275:297-306.
[31]
Zheng F, Fang J, Guo F, Yang X, Liu T, Chen M, et al.Biochar based constructed wetland for secondary effluent treatment: waste resource utilization.Chem Eng J 2022; 432:134377.
[32]
Al-Hazmi HE, Maktabifard M, Grubba D, Majtacz J, Hassan GK, Lu X, et al.An advanced synergy of partial denitrification–anammox for optimizing nitrogen removal from wastewater: a review.Bioresour Technol 2023; 381:129168.
[33]
Idbella M, Bonanomi G.Uncovering the dark side of agriculture: how land use intensity shapes soil microbiome and increases potential plant pathogens.Appl Soil Ecol 2023; 192:105090.
[34]
Xu L, Su J, Li K, Hu R, Yan H, Liang E, et al.Performance of hydrogel immobilized bioreactors combined with different iron ore wastes for denitrification and removal of copper and lead: optimization and possible mechanism.Water Res 2022; 225:119196.
[35]
Wang G, Yu G, Chi T, Li Y, Zhang Y, Wang J, et al.Insights into the enhanced effect of biochar on cadmium removal in vertical flow constructed wetlands.J Hazard Mater 2023; 443:130148.
[36]
Zhang T, Cao J, Zhang Y, Fang F, Feng Q, Luo J.Achieving efficient nitrite accumulation in glycerol-driven partial denitrification system: insights of influencing factors, shift of microbial community and metabolic function.Bioresour Technol 2020; 315:123844.
[37]
Li S, Liao Y, Pang Y, Dong X, Strous M, Ji G.Denitrification and dissimilatory nitrate reduction to ammonia in long-term lake sediment microcosms with iron (II).Sci Total Environ 2022; 807:150835.
[38]
Chen L, Chen H, Hu Z, Tian Y, Wang C, Xie P, et al.Carbon uptake bioenergetics of PAOs and GAOs in full-scale enhanced biological phosphorus removal systems.Water Res 2022; 216:118258.
[39]
Guo M, Yang G, Meng X, Zhang T, Li C, Bai S, et al.Illuminating plant–microbe interaction: how photoperiod affects rhizosphere and pollutant removal in constructed wetland?.Environ Int 2023; 179:108144.
[40]
Yang X, He Q, Guo F, Sun X, Zhang J, Chen Y.Impacts of carbon-based nanomaterials on nutrient removal in constructed wetlands: microbial community structure, enzyme activities, and metabolism process.J Hazard Mater 2021; 401:123270.
[41]
Su Y, Wang W, Wu D, Huang W, Wang M, Zhu G.Stimulating ammonia oxidizing bacteria (AOB) activity drives the ammonium oxidation rate in a constructed wetland (CW).Sci Total Environ 2018; 624:87-95.
[42]
Shi H, Feng X, Xiao Z, Wang W, Wang Y, Zhang X, et al.Analysis of the β-cyclodextrin enhancing bio-denitrification from the perspective of substrate metabolism, electron transfer, and iron acquisition.Chem Eng J 2022; 446:137358.
[43]
Wang C, He T, Zhang M, Zheng C, Yang L, Yang L.Review of the mechanisms involved in dissimilatory nitrate reduction to ammonium and the efficacies of these mechanisms in the environment.Environ Pollut 2024; 345:123480.
[44]
Jiang M, Zheng X, Chen Y.Enhancement of denitrification performance with reduction of nitrite accumulation and N2O emission by Shewanella oneidensis MR-1 in microbial denitrifying process.Water Res 2020; 169:115242.
[45]
Bian J, Liao Y, Liu R, An X, Hu C, Liu H, et al.Synergy of cyano groups and cobalt single atoms in graphitic carbon nitride for enhanced bio-denitrification.Water Res 2022; 218:118465.
[46]
Mendoza-Hoffmann F, ÁP érez-Oseguera, MÁCevallos , Zarco-Zavala M, Ortega R, Peña-Segura C, et al.The biological role of the ζ subunit as unidirectional inhibitor of the F1FO-ATPase of Paracoccus denitrificans.Cell Rep 2018; 22(4):1067-1078.
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