Skip to main content
SpringerLink
Log in

Simultaneous Feammox and anammox process facilitated by activated carbon as an electron shuttle for autotrophic biological nitrogen removal

  • Research Article
  • Published:
Frontiers of Environmental Science & Engineering Aims and scope Submit manuscript

Abstract

Ferric iron reduction coupled with anaerobic ammonium oxidation (Feammox) is a novel ferric-dependent autotrophic process for biological nitrogen removal (BNR) that has attracted increasing attention due to its low organic carbon requirement. However, extracellular electron transfer limits the nitrogen transformation rate. In this study, activated carbon (AC) was used as an electron shuttle and added into an integrated autotrophic BNR system consisting of Feammox and anammox processes. The nitrogen removal performance, nitrogen transformation pathways and microbial communities were investigated during 194 days of operation. During the stable operational period (days 126–194), the total nitrogen (TN) removal efficiency reached 82.9%±6.8% with a nitrogen removal rate of 0.46±0.04 kg-TN/m3/d. The contributions of the Feammox, anammox and heterotrophic denitrification pathways to TN loss accounted for 7.5%, 89.5% and 3.0%, respectively. Batch experiments showed that AC was more effective in accelerating the Feammox rate than the anammox rate. X-ray photoelectron spectroscopy (XPS) analyses showed the presence of ferric iron (Fe(III)) and ferrous iron (Fe(II)) in secondary minerals. X-ray diffraction (XRD) patterns indicated that secondary iron species were formed on the surface of iron-AC carrier (Fe/AC), and Fe(III) was primarily reduced by ammonium in the Feammox process. The phyla Anaerolineaceae (0.542%) and Candidatus Magasanikbacteria (0.147%) might contribute to the Feammox process, and Candidatus Jettenia (2.10%) and Candidatus Brocadia (1.18%) were the dominative anammox phyla in the bioreactor. Overall, the addition of AC provided an effective way to enhance the autotrophic BNR process by integrating Feammox and anammox.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aishvarya V, Barman S, Pradhan N, Ghosh M K (2019). Selective enhancement of Mn bioleaching from ferromanganese ores in presence of electron shuttles using dissimilatory Mn reducing consortia. Hydrometallurgy, 186: 269–274

    Article  CAS  Google Scholar 

  • APHA (1989). Standard Methods for the Examination of Water and Wastewater. Washington, DC: American Public Health Association

    Google Scholar 

  • Astals S, Peces M, Batstone D J, Jensen P D, Tait S (2018). Characterising and modelling free ammonia and ammonium inhibition in anaerobic systems. Water Research, 143: 127–135

    Article  CAS  Google Scholar 

  • Carver J C, Schweitzer G K, Carlson T A (1972). Use of X-ray photoelectron spectroscopy to study bonding in Cr, Mn, Fe, and Co compounds. Journal of Chemical Physics, 57(2): 973–982

    Article  CAS  Google Scholar 

  • Chai F, Li L, Xue S, Liu J (2020). Auxiliary voltage enhanced microbial methane oxidation co-driven by nitrite and sulfate reduction. Chemosphere, 250: 126259

    Article  CAS  Google Scholar 

  • Chen C, Sun F, Zhang H, Wang J, Shen Y, Liang X (2016). Evaluation of COD effect on anammox process and microbial communities in the anaerobic baffled reactor (ABR). Bioresource Technology, 216: 571–578

    Article  CAS  Google Scholar 

  • Chen H, Liu S, Yang F, Xue Y, Wang T (2009). The development of simultaneous partial nitrification, ANAMMOX and denitrification (SNAD) process in a single reactor for nitrogen removal. Bioresource Technology, 100(4): 1548–1554

    Article  CAS  Google Scholar 

  • Ding L J, An X L, Li S, Zhang G L, Zhu Y G (2014). Nitrogen loss through anaerobic ammonium oxidation coupled to iron reduction from paddy soils in a chronosequence. Environmental Science & Technology, 48(18): 10641–10647

    Article  CAS  Google Scholar 

  • Ding W, Stewart D I, Humphreys P N, Rout S P, Burke I T (2016). Role of an organic carbon-rich soil and Fe(III) reduction in reducing the toxicity and environmental mobility of chromium(VI) at a COPR disposal site. Science of the Total Environment, 541: 1191–1199

    Article  CAS  Google Scholar 

  • Du R, Cao S, Li X, Wang J, Peng Y (2020). Efficient partial-denitrification/anammox (PD/A) process through gas-mixing strategy: System evaluation and microbial analysis. Bioresource Technology, 300: 122675

    Article  CAS  Google Scholar 

  • Egorova K S, Ananikov V P (2016). Which metals are green for catalysis? Comparison of the toxicities of Ni, Cu, Fe, Pd, Pt, Rh, and Au salts. Angewandte Chemie International Edition in English, 55(40): 12150–12162

    Article  CAS  Google Scholar 

  • Flemming H C, Wingender J (2010). The biofilm matrix. Nature Reviews. Microbiology, 8(9): 623–633

    Article  CAS  Google Scholar 

  • Francis Cheng R M (1997). Reduction of nitrate to ammonia by zero-valent iron. Chemosphere, 35(11): 2689–2695

    Article  Google Scholar 

  • Geoffrey C A, Michael T C, Alan J H, Philip M T (1974). X-Ray photoelectron spectroscopy of iron-oxygen systems. Journal of the Chemical Society, 14: 1525–1530

    Google Scholar 

  • Graaf A a V a N D E, Mulder A, Bruijn P D E, Jetten M S M, Robertson L A, Kuenen J G (1995). Anaerobic oxidation of ammonium is a biologically mediated process. Applied and Environmental Microbiology, 61: 1246–1251

    Article  Google Scholar 

  • Guo Y, Liu S, Tang X, Yang F (2017). Role of c-di-GMP in anammox aggregation and systematic analysis of its turnover protein in Candidatus Jettenia caeni. Water Research, 113: 181–190

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Jenni S, Vlaeminck S E, Morgenroth E, Udert K M (2014). Successful application of nitritation/anammox to wastewater with elevated organic carbon to ammonia ratios. Water Research, 49: 316–326

    Article  CAS  Google Scholar 

  • Jiang N, Juan Y, Tian L, Chen X, Sun W, Chen L (2018). Modification of the composition of dissolved nitrogen forms, nitrogen transformation processes, and diversity of bacterial communities by freeze-thaw events in temperate soils. Pedobiologia, 71: 41–49

    Article  Google Scholar 

  • Lackner S, Gilbert E M, Vlaeminck S E, Joss A, Horn H, van Loosdrecht M C (2014). Full-scale partial nitritation/anammox experiences-an application survey. Water Research, 55: 292–303

    Article  CAS  Google Scholar 

  • Li H, Zhong Y, Huang H, Tan Z, Sun Y, Liu H (2020). Simultaneous nitrogen and phosphorus removal by interactions between phosphate accumulating organisms (PAOs) and denitrifying phosphate accumulating organisms (DPAOs) in a sequencing batch reactor. Science of the Total Environment, 744: 140852

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Li X, Hou L, Liu M, Zheng Y, Yin G, Lin X, Cheng L, Li Y, Hu X (2015). Evidence of nitrogen loss from anaerobic ammonium oxidation coupled with ferric iron reduction in an intertidal wetland. Environmental Science & Technology, 49(19): 11560–11568

    Article  CAS  Google Scholar 

  • Li X, Yuan Y, Huang Y, Liu H W, Bi Z, Yuan Y, Yang P B (2018). A novel method of simultaneous NH4+ and NO3− removal using Fe cycling as a catalyst: Feammox coupled with NAFO. Science of the Total Environment, 631–632: 153–157

    Google Scholar 

  • Li Y, Ling J, Chen P, Chen J, Dai R, Liao J, Yu J, Xu Y (2021b). Pseudomonas mendocina LYX: A novel aerobic bacterium with advantage of removing nitrate high effectively by assimilation and dissimilation simultaneously. Frontiers of Environmental Science & Engineering, 15(4): 57

    Article  CAS  Google Scholar 

  • Lin Y, Li Y, Xu Z, Xiong J, Zhu T (2018). Transformation of functional groups in the reduction of NO with NH3 over nitrogen-enriched activated carbons. Fuel, 223: 312–323

    Article  CAS  Google Scholar 

  • Mandel A, Zekker I, Jaagura M, Tenno T (2019). Enhancement of anoxic phosphorus uptake of denitrifying phosphorus removal process by biomass adaption. International Journal of Environmental Science and Technology, 16(10): 5965–5978

    Article  CAS  Google Scholar 

  • Miao L, Zhang Q, Wang S, Li B, Wang Z, Zhang S, Zhang M, Peng Y (2018). Characterization of EPS compositions and microbial community in an anammox SBBR system treating landfill leachate. Bioresource Technology, 249: 108–116

    Article  CAS  Google Scholar 

  • Orsetti S, Laskov C, Haderlein S B (2013). Electron transfer between iron minerals and quinones: Estimating the reduction potential of the Fe(II)-goethite surface from AQDS speciation. Environmental Science & Technology, 47(24): 14161–14168

    Article  CAS  Google Scholar 

  • Oshiki M, Ishii S, Yoshida K, Fujii N, Ishiguro M, Satoh H, Okabe S (2013). Nitrate-dependent ferrous iron oxidation by anaerobic ammonium oxidation (anammox) bacteria. Applied and Environmental Microbiology, 79(13): 4087–4093

    Article  CAS  Google Scholar 

  • Qiao S, Tian T, Zhou J (2014). Effects of quinoid redox mediators on the activity of anammox biomass. Bioresource Technology, 152: 116–123

    Article  CAS  Google Scholar 

  • Qiu S, Liu J, Zhang L, Zhang Q, Peng Y (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, 2021, 15(2): 26

    Article  CAS  Google Scholar 

  • Rikmann E, Zekker I, Tenno T, Saluste A, Tenno T (2017). Inoculum-free start-up of biofilm- and sludge-based deammonification systems in pilot scale. International Journal of Environmental Science and Technology, 15(1): 133–148

    Article  Google Scholar 

  • Rubin S S, Marín I, Gómez M J, Morales E A, Zekker I, San Martín-Uriz P, Rodríguez N, Amils R (2017). Prokaryotic diversity and community composition in the Salar de Uyuni, a large scale, chaotropic salt flat. Environmental Microbiology, 19(9): 3745–3754

    Article  CAS  Google Scholar 

  • Shaw D R, Ali M, Katuri K P, Gralnick J A, Reimann J, Mesman R, van Niftrik L, Jetten M S M, Saikaly P E (2020). Extracellular electron transfer-dependent anaerobic oxidation of ammonium by anammox bacteria. Nature Communications, 11(1): 2058–2070

    Article  CAS  Google Scholar 

  • Sheng H, Weng R, Zhu J, He Y, Cao C, Huang M (2021). Calcium nitrate as a bio-stimulant for anaerobic ammonium oxidation process. Science of the Total Environment, 760: 143331

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Stern N, Mejia J, He S, Yang Y, Ginder-Vogel M, Roden E E (2018). Dual role of humic substances as electron donor and shuttle for dissimilatory iron reduction. Environmental Science & Technology, 52(10): 5691–5699

    Article  CAS  Google Scholar 

  • Sun J, Wei L, Yin R, Jiang F, Shang C (2020). Microbial iron reduction enhances in-situ control of biogenic hydrogen sulfide by FeOOH granules in sediments of polluted urban waters. Water Research, 171: 115453

    Article  CAS  Google Scholar 

  • Tenno T, Mashirin A, Zekker I, Uiga K, Rikmann E, Tenno T (2018). A novel proton transfer model of the closed equilibrium system H2O-CO2-CaCO3-NHx. Proceedings of the Estonian Academy of Sciences, 67(3): 260–270

    Article  Google Scholar 

  • Tenno T, Uiga K, Mashirin A, Zekker I, Rikmann E (2017). Modeling closed equilibrium systems of H2O-dissolved CO2-solid CaCO3. The Journal of Physical Chemistry A, 121(16): 3094–3100

    Article  CAS  Google Scholar 

  • Tian Z, Wang B, Li Y, Shen B, Li F, Wen X (2021). Enhancement on the ammonia oxidation capacity of ammonia-oxidizing archaeon originated from wastewater: Utilizing low-density static magnetic field. Frontiers of Environmental Science & Engineering, 2021, 15(5): 81

    Article  CAS  Google Scholar 

  • Wang G, Li Q, Gao X, Wang X C (2018). Synergetic promotion of syntrophic methane production from anaerobic digestion of complex organic wastes by biochar: Performance and associated mechanisms. Bioresource Technology, 250: 812–820

    Article  CAS  Google Scholar 

  • Wang Q, Rogers M J, Ng S S, He J (2021). Fixed nitrogen removal mechanisms associated with sulfur cycling in tropical wetlands. Water Research, 189: 116619

    Article  CAS  Google Scholar 

  • Wang Q, Ye L, Jiang G, Hu S, Yuan Z (2014). Side-stream sludge treatment using free nitrous acid selectively eliminates nitrite oxidizing bacteria and achieves the nitrite pathway. Water Research, 55: 245–255

    Article  CAS  Google Scholar 

  • Wang W, Yan Y, Zhao Y, Shi Q, Wang Y (2020). Characterization of stratified EPS and their role in the initial adhesion of anammox consortia. Water Research, 169: 115223

    Article  CAS  Google Scholar 

  • Warneke S, Schipper L A, Bruesewitz D A, Baisden W T (2011). A comparison of different approaches for measuring denitrification rates in a nitrate removing bioreactor. Water Research, 45(14): 4141–4151

    Article  CAS  Google Scholar 

  • Xiao R, Ni B J, Liu S, Lu H (2021). Impacts of organics on the microbial ecology of wastewater anammox processes: Recent advances and meta-analysis. Water Research, 191: 116817

    Article  CAS  Google Scholar 

  • Xie F, Zhao B, Cui Y, Ma X, Zhang X, Yue X (2021). Reutilize tire in microbial fuel cell for enhancing the nitrogen removal of the anammox process coupled with iron-carbon micro-electrolysis. Frontiers of Environmental Science & Engineering, 2021, 15(6): 121

    Article  CAS  Google Scholar 

  • Xu S, Wu X, Liu H (2021a). Overlooked nitrogen-cycling microorganisms in biological wastewater treatment. Frontiers of Environmental Science & Engineering, 2021, 15(6): 133

    Article  CAS  Google Scholar 

  • Xu J, Li C, Zhu N, Shen Y, Yuan H (2021b). Particle size-dependent behavior of redox-active biochar to promote anaerobic ammonium oxidation (anammox). Chemical Engineering Journal, 410: 127925

    Article  CAS  Google Scholar 

  • Yang D, Wang L, Li Z, Tang X, He M, Yang S, Liu X, Xu J (2020). Simultaneous adsorption of Cd(II) and As(III) by a novel biochar-supported nanoscale zero-valent iron in aqueous systems. Science of the Total Environment, 708: 134823

    Article  CAS  Google Scholar 

  • Yang S, Guo B, Shao Y, Mohammed A, Vincent S, Ashbolt N J, Liu Y (2019). The value of floc and biofilm bacteria for anammox stability when treating ammonia-rich digester sludge thickening lagoon supernatant. Chemosphere, 233: 472–481

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Yang Y, Xiao C, Yu Q, Zhao Z, Zhang Y (2021). Using Fe(II)/Fe(III) as catalyst to drive a novel anammox process with no need of anammox bacteria. Water Research, 189: 116626–117732

    Article  CAS  Google Scholar 

  • Zekker I, Artemchuk O, Rikmann E, Ohimai K, Dhar Bhowmick G, Madhao Ghangrekar M, Burlakovs J, Tenno T (2021a). Start-up of Anammox SBR from non-specific inoculum and process acceleration methods by hydrazine. Water (Basel), 13(3): 350–365

    CAS  Google Scholar 

  • Zekker I, Kivirüüt A, Rikmann E, Mandel A, Jaagura M, Tenno T, Artemchuk O, Rubin S D, Tenno T (2018). Enhanced efficiency of nitritating-anammox sequencing batch reactor achieved at low decrease rates of oxidation-reduction potential. Environmental Engineering Science, 36(3): 350–360

    Article  Google Scholar 

  • Zekker I, Raudkivi M, Artemchuk O, Rikmann E, Priks H, Jaagura M, Tenno T (2021b). Mainstream-sidestream wastewater switching promotes anammox nitrogen removal rate in organic-rich, low-temperature streams. Environmental Technology, 42(19): 3073–3082

    Article  CAS  Google Scholar 

  • Zekker I, Rikmann E, Tenno T, Vabamäe P, Tomingas M, Menert A, Loorits L, Tenno T (2012). Anammox bacteria enrichment and phylogenic analysis in moving bed biofilm reactors. Environmental Engineering Science, 29(10): 946–950

    Article  CAS  Google Scholar 

  • Zhang H, Du R, Cao S, Wang S, Peng Y (2019a). Mechanisms and characteristics of biofilm formation via novel DEAMOX system based on sequencing biofilm batch reactor. Journal of Bioscience and Bioengineering, 127(2): 206–212

    Article  CAS  Google Scholar 

  • Zhang J, Zhang Y C, Wang X J, Li J, Zhou R X, Wei J, Liang D B, Zhang K (2019b). Effects of substrate shock on release of AHL signals in ANAMMOX granules and properties of granules. Environmental Science. Water Research & Technology, 5(4): 756–768

    Article  CAS  Google Scholar 

  • Zhang X, Zhang N, Chen Z, Ma Y, Wang L, Zhang H, Jia J (2019c). Long-term impact of sulfate on an autotrophic nitrogen removal system integrated partial nitrification, anammox and endogenous denitrification (PAED). Chemosphere, 235: 336–343

    Article  CAS  Google Scholar 

  • Zhang Y, Wang S, Gu S, Zhang L, Dong Y, Jiang L, Fan W, Peng Y (2021a). The combined effects of biomass and temperature on maximum specific ammonia oxidation rate in domestic wastewater treatment. Frontiers of Environmental Science & Engineering, 2021, 15(6): 123 https://doi.org/10.1007/s11783-021-1411-9

    Article  CAS  Google Scholar 

  • Zhang Y, Wang M, Gao X, Qian J, Pan B (2021b). Structural evolution of lanthanum hydroxides during long-term phosphate mitigation: Effect of nanoconfinement. Environmental Science & Technology, 55(1): 665–676

    Article  CAS  Google Scholar 

  • Zheng S, Liu F, Wang B, Zhang Y, Lovley D R (2020). Methanobacterium capable of direct interspecies electron transfer. Environmental Science & Technology, 54(23): 15347–15354

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Key Research and Development Program of Guangdong Province (China) (No. 2019B110205004), the Program for Guangdong Introducing Innovative and Entrepreneurial Teams (China) (No. 2019ZT08L213), the Key Special Project for Introduced Talents Team of Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou, China) (No. GML2019ZD0403) and the National Natural Science Foundation of China (Grant No. 52000039).

Author information

Authors and Affiliations

  1. Key Laboratory for City Cluster Environmental Safety and Green Development of the Ministry of Education, Institute of Environmental and Ecological Engineering, Guangdong University of Technology, Guangzhou, 510006, China

    Yingbin Hu, Ning Li, Jin Jiang, Xiaonan Luo & Jie Cao

  2. Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, 511458, China

    Yingbin Hu, Ning Li, Jin Jiang, Xiaonan Luo & Jie Cao

  3. School of Environmental Science and Engineering, Guangdong University of Technology, Guangzhou, 510006, China

    Yanbin Xu

Authors
  1. Yingbin Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ning Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jin Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yanbin Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiaonan Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jie Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Yingbin Hu: Conceptualization, Writing- Original Draft, Investigation. Ning Li: Investigation, Validation, Writing- Review & Editing. Jin Jiang: Project administration, Funding acquisition, Writing- Review & Editing, Supervision. Yanbin Xu: Validation, Writing- Review & Editing, Funding acquisition. Xiaonan Luo: Investigation, Data Curation. Jie Cao: Investigation, Data Curation.

Corresponding author

Correspondence to Ning Li.

Ethics declarations

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.

Additional information

Highlights

• The autotrophic nitrogen removal combining Feammox and anammox was achieved.

• Activated carbon can be used as an electron shuttle to enhance Feammox activity.

• Fe(III) was reduced to Fe(II) and the secondary Fe(II) mineral (FeOOH) was obtained.

• The iron-reducing bacteria and Anammox consortium was enriched simultaneously.

Supporting Materials

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hu, Y., Li, N., Jiang, J. et al. Simultaneous Feammox and anammox process facilitated by activated carbon as an electron shuttle for autotrophic biological nitrogen removal. Front. Environ. Sci. Eng. 16, 90 (2022). https://doi.org/10.1007/s11783-021-1498-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11783-021-1498-z

Keywords

Search

Navigation