Removal of ammonium and nitrate through Anammox and FeS-driven autotrophic denitrification

Highlights

● Simultaneous NH₄⁺/NO₃^– removal was achieved in the FeS denitrification system

● Anammox coupled FeS denitrification was responsible for NH₄⁺/NO₃^– removal

● Sulfammox, Feammox and Anammox occurred for NH₄⁺ removal

● Thiobacillus, Nitrospira , and Ca. Kuenenia were key functional microorganisms

Abstract

An autotrophic denitrifying bioreactor with iron sulfide (FeS) as the electron donor was operated to remove ammonium (NH₄⁺) and nitrate (NO₃⁻) synergistically from wastewater for more than 298 d. The concentration of FeS greatly affected the removal of NH₄⁺/NO₃⁻. Additionally, a low hydraulic retention time worsened the removal efficiency of NH₄⁺/NO₃⁻. When the hydraulic retention time was 12 h, the optimal removal was achieved with NH₄⁺ and NO₃⁻ removal percentages both above 88%, and the corresponding nitrogen removal loading rates of NH₄⁺ and NO₃⁻ were 49.1 and 44.0 mg/(L·d), respectively. The removal of NH₄⁺ mainly occurred in the bottom section of the bioreactor through sulfate/ferric reducing anaerobic ammonium oxidation (Sulfammox/Feammox), nitrification, and anaerobic ammonium oxidation (Anammox) by functional microbes such as Nitrospira, Nitrosomonas, and Candidatus Kuenenia. Meanwhile, NO₃⁻ was mainly removed in the middle and upper sections of the bioreactor through autotrophic denitrification by Ferritrophicum, Thiobacillus, Rhodanobacter, and Pseudomonas, which possessed complete denitrification-related genes with high relative abundances.

Graphical abstract

Keywords

Anammox / Denitrification / FeS / NH₄⁺/NO₃⁻ / Sulfammox

References

[1] APHA (2005). Standard Methods for the Examination for Water and Wastewater, 21st ed. APHA, AWWA and WEF. Washington, DC

[2] Cao X, Zheng H, Liao Y, Feng L, Jiang L, Liu C, Mao Y, Shen Q, Zhang Q, Ji F. (2022). Effects of iron-based substrate on coupling of nitrification, aerobic denitrification and Fe(II) autotrophic denitrification in tidal flow constructed wetlands. Bioresource Technology, 361: 127657

[3] Carboni M F, Mills S, Arriaga S, Collins G, Ijaz U Z, Lens P N L. (2022). Autotrophic denitrification of nitrate rich wastewater in fluidized bed reactors using pyrite and elemental sulfur as electron donors. Environmental Technology & Innovation, 28: 102878

[4] Cardenas E, Wu W M, Leigh M B, Carley J, Carroll S, Gentry T, Luo J, Watson D, Gu B, Ginder-Vogel M. . (2010). Significant association between sulfate-reducing bacteria and uranium-reducing microbial communities as revealed by a combined massively parallel sequencing-indicator species approach. Applied and Environmental Microbiology, 76(20): 6778–6786

[5] Chan-Pacheco C R, Valenzuela E I, Cervantes F J, Quijano G. (2021). Novel biotechnologies for nitrogen removal and their coupling with gas emissions abatement in wastewater treatment facilities. Science of the Total Environment, 797: 149228

[6] Chung J, Amin K, Kim S, Yoon S, Kwon K, Bae W. (2014). Autotrophic denitrification of nitrate and nitrite using thiosulfate as an electron donor. Water Research, 58: 169–178

[7] Dominika G, Joanna M, Jacek M. (2021). Sulfate reducing ammonium oxidation (SULFAMMOX) process under anaerobic conditions. Environmental Technology & Innovation, 28: 101416

[8] Du R, Cao S, Li B, Niu M, Wang S, Peng Y. (2017). Performance and microbial community analysis of a novel DEAMOX based on partial-denitrification and anammox treating ammonia and nitrate wastewaters. Water Research, 108: 46–56

[9] Du R, Peng Y, Ji J, Shi L, Gao R, Li X. (2019). Partial denitrification providing nitrite: opportunities of extending application for anammox. Environment International, 131: 105001

[10] Feng Y, Lu X, Al-Hazmi H, Mąkinia J. (2017). An overview of the strategies for the deammonification process start-up and recovery after accidental operational failures. Reviews in Environmental Science and Biotechnology, 16(3): 541–568

[11] Fortin D, Davis B, Beveridge T J. (1996). Role of Thiobacillus and sulfate-reducing bacteria in iron biocycling in oxic and acidic mine tailings. FEMS Microbiology Ecology, 21(1): 11–24

[12] Glass C, Silverstein J. (1998). Denitrification kinetics of high nitrate concentration water: pH effect on inhibition and nitrite accumulation. Water Research, 32(3): 831–839

[13] Hu Y, Li N, Jiang J, Xu Y, Luo X, Cao J. (2022). Simultaneous Feammox and anammox process facilitated by activated carbon as an electron shuttle for autotrophic biological nitrogen removal. Frontiers of Environmental Science & Engineering, 16(7): 90

[14] Hu Y, Wu G, Li R, Xiao L, Zhan X. (2020). Iron sulphides mediated autotrophic denitrification: an emerging bioprocess for nitrate pollution mitigation and sustainable wastewater treatment. Water Research, 179: 115914

[15] Huang S, Jaffé P R. (2015). Characterization of incubation experiments and development of an enrichment culture capable of ammonium oxidation under iron-reducing conditions. Biogeosciences, 12(3): 769–779

[16] Jin R C, Yang G F, Yu J J, Zheng P. (2012). The inhibition of the Anammox process: a review. Chemical Engineering Journal, 197: 67–79

[17] Kraft B, Jehmlich N, Larsen M, Bristow L A, Konneke M, Thamdrup B, Canfield D E. (2022). Oxygen and nitrogen production by an ammonia-oxidizing archaeon. Science, 375(6576): 97–100

[18] Li H, Su J Q, Yang X R, Zhou G W, Lassen S B, Zhu Y G. (2019). RNA stable isotope probing of potential feammox population in paddy soil. Environmental Science & Technology, 53(9): 4841–4849

[19] Li R, Morrison L, Collins G, Li A, Zhan X. (2016). Simultaneous nitrate and phosphate removal from wastewater lacking organic matter through microbial oxidation of pyrrhotite coupled to nitrate reduction. Water Research, 96: 32–41

[20] Li S H, Zhou X, Cao X W, Chen J B. (2021). Insights into simultaneous anammox and denitrification system with short-term pyridine exposure: process capability, inhibition kinetics and metabolic pathways. Frontiers of Environmental Science & Engineering, 15(6): 139

[21] Lichtenberg M, Line L, Schrameyer V, Jakobsen T H, Rybtke M L, Toyofuku M, Nomura N, Kolpen M, Tolker-Nielsen T, Kuhl M, Bjarnsholt T, Jensen P O. (2021). Nitric-oxide-driven oxygen release in anoxic Pseudomonas aeruginosa. iScience, 24(12): 103404

[22] Liu L Y, Xie G J, Xing D F, Liu B F, Ding J, Cao G L, Ren N Q. (2021). Sulfate dependent ammonium oxidation: a microbial process linked nitrogen with sulfur cycle and potential application. Environmental Research, 192: 110282

[23] Ma J, Wei J, Kong Q, Li Z, Pan J, Chen B, Qiu G, Wu H, Zhu S, Wei C. (2021). Synergy between autotrophic denitrification and Anammox driven by FeS in a fluidized bed bioreactor for advanced nitrogen removal. Chemosphere, 280: 130726

[24] MaJ DPan J XLiZ MWangY XWuH Z WeiC H (2019). Performance and mechanisms of advanced nitrogen removal via FeS-driven autotrophic denitrification coupled with Anammox. Environmental Sciences, 40(8): 3683-3690 (in Chinese)

[25] Mohamed N M, Saito K, Tal Y, Hill R T. (2010). Diversity of aerobic and anaerobic ammonia-oxidizing bacteria in marine sponges. ISME Journal, 4(1): 38–48

[26] Mulder A, van de Graaf A A, Robertson L A, Kuenen J G. (1995). Anaerobic ammonium oxidation discovered in a denitrifying fluidized bed reactor. FEMS Microbiology Ecology, 16(3): 177–183

[27] Wan D, Li Q, Liu Y, Xiao S, Wang H. (2019). Simultaneous reduction of perchlorate and nitrate in a combined heterotrophic-sulfur-autotrophic system: secondary pollution control, pH balance and microbial community analysis. Water Research, 165: 115004

[28] 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

[29] Wang Y, Wu G, Zheng X, Mao W, Guan Y. (2022). Synergistic ammonia and nitrate removal in a novel pyrite-driven autotrophic denitrification biofilter. Bioresource Technology, 355: 127223

[30] Xin Y, Liu L, Wei L, Huang X, Liu C. (2021). Recycling of rural abandoned constructed wetlands: mariculture wastewater treatment. Journal of Water Reuse and Desalination, 11(2): 279–288

[31] Yang Y, Chen T, Morrison L, Gerrity S, Collins G, Porca E, Li R, Zhan X. (2017). Nanostructured pyrrhotite supports autotrophic denitrification for simultaneous nitrogen and phosphorus removal from secondary effluents. Chemical Engineering Journal, 328: 511–518

[32] Zhang T, Feng Z, Shi Y, Yin Q, Wu G. (2022). Ammonium removal and potential microbial interactions under oxygen-Limited conditions. Journal of Environmental Engineering, 148(4): 04022008

[33] Zhu B, Wang J, Bradford L M, Ettwig K, Hu B, Lueders T. (2019a). Nitric oxide dismutase (nod) genes as a functional marker for the diversity and phylogeny of methane-driven oxygenic denitrifiers. Frontiers in Microbiology, 10: 1577

[34] Zhu T, Cheng H, Yang L, Su S, Wang H, Wang S, Wang A. (2019b). Coupled sulfur and iron(II) carbonate-driven autotrophic denitrification for significantly enhanced nitrate removal. Environmental Science & Technology, 53(3): 1545–1554

Acknowledgements

This study was supported by the Guangxi Key R & D Program (No. 2021AB25056), and the Shenzhen Key Scientific and Technological Project (No. JSGG20191129094410446).

Electronic Supplementary Material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s11783-023-1674-4 and is accessible for authorized users.

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