Hematite-facilitated microbial ammoxidation for enhanced nitrogen removal in constructed wetlands

Abstract

● H-CWs synergistically eliminate NH₄⁺ and NO₃⁻ while reducing N₂O emissions.

● Inhibitors and isotope incubations are used to prove the Feammox process.

● Feammox contributes approximately 40% to ammonia removal in H-CWs.

● Nanowires on the hematite suggest ammoxidation likely linked to EET.

● H-CWs enhance the abundance of nitrogen-metabolizing microorganisms and genes.

Constructed wetlands (CWs) are widely applied for decentralized wastewater treatment. However, achieving efficient removal of ammonia (NH₄⁺–N) has proven challenging due to insufficient oxygen. In this study, natural hematite (Fe₂O₃) was employed as a CW substrate (H-CWs) for the first time to drive anaerobic ammonia oxidation coupled with iron(III) reduction (Feammox). Compared to gravel constructed wetlands (G-CWs), ammonia removal was enhanced by 38.14% to 54.03% and nitrous oxide (N₂O) emissions were reduced by 34.60% in H-CWs. The synergistic removal of ammonia and nitrate by H-CWs also resulted in the absence of ammoxidation by-products. Inhibitor and ¹⁵N isotope tracer incubations showed that Feammox accounting for approximately 40% of all ammonia removal in the H-CWs. The enrichment of iron phosphate (Fe₃Fe₄(PO₄)₆) promoted the accumulation of the Feammox intermediate compound FeOOH. Microbial nanowires were observed on the surface of H-CW substrates as well, suggesting that the observed biological ammoxidation was most likely related to extracellular electron transfer (EET). Microbial and metagenomics analysis revealed that H-CWs elevated the integrity and enhanced the abundance of functional microorganisms and genes associated with nitrogen metabolism. Overall, the efficient ammonia removal in the absence of O₂ together with a reduction in N₂O emissions as described in this study may provide useful guidance for hematite-mediated anaerobic ammonia removal in CWs.

Graphical abstract

Keywords

Constructed wetlands / Nitrogen removal / Feammox / Hematite / Iron cycle

References

[1] Bardon C , Poly F , Piola F , Pancton M , Comte G , Meiffren G , Haichar F Z . (2016). Mechanism of biological denitrification inhibition: procyanidins induce an allosteric transition of the membrane-bound nitrate reductase through membrane alteration. FEMS Microbiology Ecology, 92(5): fiw034

[2] Boog J , Nivala J , Aubron T , Wallace S , van Afferden M , Muller R A . (2014). Hydraulic characterization and optimization of total nitrogen removal in an aerated vertical subsurface flow treatment wetland. Bioresource Technology, 162: 166–174

[3] Bose H , Sahu R P , Sar P . (2022). Impact of arsenic on microbial community structure and their metabolic potential from rice soils of West Bengal, India. Science of the Total Environment, 841: 156486

[4] Chan S Y , Tsang Y F , Cui L H , Chua H . (2008). Domestic wastewater treatment using batch-fed constructed wetland and predictive model development for NH₃–N removal. Process Biochemistry, 43(3): 297–305

[5] Chen Y , Shao Z , Kong Z , Gu L , Fang J , Chai H . (2020). Study of pyrite based autotrophic denitrification system for low-carbon source stormwater treatment. Journal of Water Process Engineering, 37: 101414

[6] Cheng C , He Q , Zhang J , Chai H , Yang Y , Pavlostathis S G , Wu H . (2022). New insight into ammonium oxidation processes and mechanisms mediated by manganese oxide in constructed wetlands. Water Research, 215: 118251

[7] Dai M , Zhang Y , Wu Y , Sun R , Zong W , Kong Q . (2021). Mechanism involved in the treatment of sulfamethoxazole in wastewater using a constructed wetland microbial fuel cell system. Journal of Environmental Chemical Engineering, 9(5): 106193

[8] Deng R , He Q , Yang D , Dong Q , Wu J , Yang X , Chen Y . (2021). Enhanced synergistic performance of nano-Fe⁰-CeO₂ composites for the degradation of diclofenac in DBD plasma. Chemical Engineering Journal, 406: 126884

[9] Guo F , Zhang J , Yang X , He Q , Ao L , Chen Y . (2020). Impact of biochar on greenhouse gas emissions from constructed wetlands under various influent chemical oxygen demand to nitrogen ratios. Bioresource Technology, 303: 122908

[10] Hu L , Cheng X , Qi G , Zheng M , Dang Y , Li J , Xu K . (2022). Achieving ammonium removal through anammox-derived Feammox with low demand of Fe(III). Frontiers in Microbiology, 13: 918634

[11] Hu Y , Zhao X , Zhao Y . (2014). Achieving high-rate autotrophic nitrogen removal via Canon process in a modified single bed tidal flow constructed wetland. Chemical Engineering Journal, 237: 329–335

[12] Hua D , Fan Q , Zhao Y , Xu H , Chen L , Li Y . (2020). Comparison of methanogenic potential of wood vinegar with gradient loads in batch and continuous anaerobic digestion and microbial community analysis. Science of the Total Environment, 739: 139943

[13] Jiao S , Xu L , Hu K , Li J , Gao S , Xu D . (2010). Morphological control of α-FeOOH nanostructures by electrodeposition. Journal of Physical Chemistry C, 114(1): 269–273

[14] Lezcano M A , Velazquez D , Quesada A , El-Shehawy R . (2017). Diversity and temporal shifts of the bacterial community associated with a toxic cyanobacterial bloom: an interplay between microcystin producers and degraders. Water Research, 125: 52–61

[15] Li R , Guan M , Wang W . (2021). Simultaneous arsenite and nitrate removal from simulated groundwater based on pyrrhotite autotrophic denitrification. Water Research, 189: 116662

[16] Liptzin D , Silver W L . (2009). Effects of carbon additions on iron reduction and phosphorus availability in a humid tropical forest soil. Soil Biology & Biochemistry, 41(8): 1696–1702

[17] Liu Y , Liu X H , Wang H C , Li Z L , Liang B , Sun Y L , Cheng H Y , Lu S Y , Wang A J . (2023). Pyrite coupled with steel slag to enhance simultaneous nitrogen and phosphorus removal in constructed wetlands. Chemical Engineering Journal, 470: 143944

[18] Logan B E , Hamelers B , Rozendal R , Schröder U , Keller J , Freguia S , Aelterman P , Verstraete W , Rabaey K . (2006). Microbial fuel cells: methodology and technology. Environmental Science & Technology, 40(17): 5181–5192

[19] Lu Q , Zhou J , Zhu G , Tan C , Chen S , Zhu X , Yan N , Zhang Y , Xu Q , Pan B , Rittmann B E . (2022). Anoxic/oxic treatment without biomass recycle. Science of the Total Environment, 834: 155166

[20] Pous N , Bañeras L , Corvini P F X , Liu S J , Puig S . (2023). Direct ammonium oxidation to nitrogen gas (Dirammox) in Alcaligenes strain HO-1: the electrode role. Environmental Science and Ecotechnology, 15: 100253

[21] Póvoa P , Oehmen A , Inocêncio P , Matos J S , Frazão A . (2017). Modelling energy costs for different operational strategies of a large water resource recovery facility. Water Science and Technology, 75(9): 2139–2148

[22] Prosser J I , Hink L , Gubry-Rangin C , Nicol G W . (2020). Nitrous oxide production by ammonia oxidizers: physiological diversity, niche differentiation and potential mitigation strategies. Global Change Biology, 26(1): 103–118

[23] Shi L , Dong H , Reguera G , Beyenal H , Lu A , Liu J , Yu H Q , Fredrickson J K . (2016). Extracellular electron transfer mechanisms between microorganisms and minerals. Nature Reviews. Microbiology, 14(10): 651–662

[24] Shuai W , Jaffe P R . (2019). Anaerobic ammonium oxidation coupled to iron reduction in constructed wetland mesocosms. Science of the Total Environment, 648: 984–992

[25] Tan X , Xie G J , Nie W B , Xing D F , Liu B F , Ding J , Ren N Q . (2022). Fe(III)-mediated anaerobic ammonium oxidation: a novel microbial nitrogen cycle pathway and potential applications. Critical Reviews in Environmental Science and Technology, 52(16): 2962–2994

[26] van Kessel M A , Speth D R , Albertsen M , Nielsen P H , Op Den Camp H J , Kartal B , Jetten M S , Lucker S . (2015). Complete nitrification by a single microorganism. Nature, 528(7583): 555–559

[27] Wan L , Liu H , Wang X . (2022). Anaerobic ammonium oxidation coupled to Fe(III) reduction: discovery, mechanism and application prospects in wastewater treatment. Science of the Total Environment, 818: 151687

[28] Wang Z , Le X , Cao X , Wang C , Chen F , Wang J , Feng Y , Yue L , Xing B . (2022). Triiron tetrairon phosphate (Fe₇(PO₄)₆) nanomaterials enhanced flavonoid accumulation in tomato fruits. Nanomaterials, 12(8): 1341

[29] Wu H , Zhang J , Ngo H H , Guo W , Hu Z , Liang S , Fan J , Liu H . (2015). A review on the sustainability of constructed wetlands for wastewater treatment: design and operation. Bioresource Technology, 175: 594–601

[30] Yang W H , Weber K A , Silver W L . (2012). Nitrogen loss from soil through anaerobic ammonium oxidation coupled to iron reduction. Nature Geoscience, 5(8): 538–541

[31] Yang Y , Xiao C , Lu J , Zhang Y . (2020). Fe(III)/Fe(II) forwarding a new anammox-like process to remove high-concentration ammonium using nitrate as terminal electron acceptor. Water Research, 172: 115528

[32] Yu C , Huang X , Chen H , Godfray H C J , Wright J S , Hall J W , Gong P , Ni S , Qiao S , Huang G . . (2019). Managing nitrogen to restore water quality in China. Nature, 567(7749): 516–520

[33] Zhang G , Hao Q , Ma R , Luo S , Chen K , Liang Z , Jiang C . (2023). Biochar and hematite amendments suppress emission of CH₄ and NO₂ in constructed wetlands. Science of the Total Environment, 874: 162451

[34] Zhou G W , Yang X R , Li H , Marshall C W , Zheng B X , Yan Y , Su J Q , Zhu Y G . (2016). Electron shuttles enhance anaerobic ammonium oxidation coupled to iron(III) reduction. Environmental Science & Technology, 50(17): 9298–9307

[35] Zhuang L L , Yang T , Zhang J , Li X . (2019). The configuration, purification effect and mechanism of intensified constructed wetland for wastewater treatment from the aspect of nitrogen removal: a review. Bioresource Technology, 293: 122086

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