Abstract
Electric field was applied to enhance the activity of anaerobic ammonium oxidation (anammox) bacteria for nitrogen removal in this study. The effect of different distributive modes with the total electric field time of 6 h/24 h (R2) and 18 h/24 h (R3) at 2 V/cm was determined through long-term tests. With the continuous application time increasing from 3 to 9 h in R3 (1 to 3 h in R2), the total nitrogen removal rate (NRR) showed an acceleration trend. When the electric field was applied continuously for 9 h (R3, mode 3, application-rest time: 9 h–3 h), the NRR dramatically increased 38.7 % over that of control on day 160. Besides, it was demonstrated that the increase of crude enzyme activities and the cell quantities were the main reasons for the enhancement of nitrogen removal performance of the anammox process. Additionally, transmission electron microscope observation proved the morphological change of anammox biomass under electric field application.
Similar content being viewed by others
References
APHA (1995) Standard methods for the examination of water and wastewater, 19th edn. American Public Health Association, New York
Bradford MM (1976) A rapid and sensitive for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Duan XM, Zhou JT, Qiao S, Wei HF (2011) Application of low intensity ultrasound to enhance the activity of anammox microbial consortium for nitrogen removal. Bioresour Technol 102:4290–4293
Hira D, Toh H, Migita C, Okubo H, Nishiyama T, Hattori M, Furukawa K, Fujii T (2012) Anammox organism KSU-1 expresses a NirK-type copper-containing nitrite reductase instead of a NirS-type with cytochrome cd 1. FEBS Lett 586:1658–1663
Jetten MSM, Wagner M, Fuerst J, van Loosdrecht M, Kuenen G, Strous M (2001) Microbiology and application of the anaerobic ammonium oxidation (anammox) process. Curr Opin Biotechnol 12:283–288
Jetten MSM, van Niftrik L, Strous M, Kartal B, Keltjens JT, Huub JM, den Camp O (2009) Biochemistry and molecular biology of anammox bacteria. Crit Rev Biochem Mol Biol 44:65–84
Kartal B, Maalcke WJ, de Almeida NM, Cirpus I, Gloerich J, Geerts W, Op den Camp HJM, Harhangi HR, Janssen-Megens EM, Francoijs KJ, Stunnenberg HG, Keltjens JT, Jetten MSM, Strous M (2011) Molecular mechanism of anaerobic ammonium oxidation. Nature 479:127–130
Liu ST, Yang FL, Meng FG, Chen HH, Gong Z (2008) Enhanced anammox consortium activity for nitrogen removal: impacts of static magnetic field. J Biotechnol 138:96–102
Matsumoto N, Yoshignaga H, Ohmura N, Ando A, Saiki H (2002) Numerical stimulation for electrochemical cultivation of iron oxidizing bacteria. Biotechnol Bioeng 78:17–23
Meincke M, Bock E, Kastrau D, Kroneck PMH (1992) Nitrite oxidoreductase from Nitrobacter hamburgensis: redox centers and their catalytic role. Arch Microbiol 158:127–131
Meller RB, Campbell WH (1992) Reduction of nitrate and nitrite in water by immobilized enzymes. Nature 355:717–719
Mulder A, Vandegraaf AA, Robertson LA, Kuenen JG (1995) Anaerobic ammonium oxidation discovered in a denitrifying fluidized bed reactor. FEMS Microbiol Ecol 16:177–184
Mulder JW, van Loosdrecht MCM, Hellinga C, van Kempen R (2001) Full-scale application of the sharon process for treatment of rejection water of digested sludge dewatering. Water Sci Technol 43:127–134
Neumann S, Jetten MSM, van Niftrik L (2011) The ultrastructure of the compartmentalized anaerobic ammonium-oxidizing bacteria is linked to their energy metabolism. Biochem Soc Trans 39:1805–1810
Ohmura N, Matsumoto N, Sasaki K, Saiki H (2002) Electrochemical regeneration of Fe(III) to support growth on anaerobic iron respiration. Appl Environ Microbiol 68:405–407
Op den Camp HJM, Kartal B, Guven D, van Niftrik LA, Haaijer SCM, van der Star WR, van de Pas-Schoonen KT, Cabezas A, Ying Z, Schmid MC, Kuypers MMM, van de Vossenberg J, Harhangi HR, Picioreanu C, van Loosdrecht MCM, Kuene JG, Strous M, Jetten MSM (2006) Global impact and application of the anaerobic ammonium-oxidizing (anammox) bacteria. Biochem Soc Trans 34:174–178
Qiao S, Yin X, Zhou JT, Furukawa KJ (2013) Inhibition and recovery of continuous electric field application on the activity of anammox biomass. Biodegradation 25:505–513
Shimamura M, Nishiyama T, Shigetomo H, Toyomoto T, Kawahara Y, Furukawa K, Fujii T (2007) Isolation of a multiheme protein with features of a hydrazine-oxidizing enzyme from an anaerobic ammonium-oxidizing enrichment culture. Appl Environ Microbiol 73:1065–1072
Sinninghe Damste JS, Strous M, Rijpstra WIC, Hopmans EC, Geenevasen JAJ, van Duin ACT, van Niftrik LA, Jetten MSM (2002) Linearly concatenated cyclobutane lipids form a dense bacterial membrane. Nature 419:708–712
Strous M, Fuerst JA, Kramer EHM, Logemann S, Muzyer G, van de Pas-Schoonen KT, Webb R, Kuene JG, Jetten MSM (1999) Missing lithotroph identified as new planctomycete. Nature 400:446–449
Thrash JC, Van Trump JI, Weber KA, Miller E, Achenbach LA, Coates JD (2007) Electrochemical stimulation of microbial perchlorate reduction. Environ Sci Technol 41:1740–1746
Van der Graaf AA, de Bruijn P, Robertson LA, Jetten MSM, Kuenen JG (1996) Autotrophic growth of anaerobic ammonium-oxidizing micro-organisms in a fluidized bed reactor. Microbiology 142:2187–2196
Van der Star WRL, Abma WR, Blommers D, Mulder JW, Tokutomi T, Picioreanu M, Strous C, Van Loosdrecht MCM (2007) Startup of reactors for anoxic ammonium oxidation: experiences from the first full-scale anammox reactor in Rotterdam. Water Res 41:4149–4163
Van Niftrik L, Geerts W, Van Donselaar E, Humbel B, Webb R, Fuerst J, Verkleij A, Jetten M, Strous M (2008) Linking ultrastructure and function in four genera of anaerobic ammonium-oxidizing bacteria: cell plan, glycogen storage, and localization of cytochrome c proteins. J Bacteriol 2:708–717
Zhao W, Yang R, Zhang H, Zhang W, Hua X, Tang Y (2011) Quantitative and real time detection of pulsed electric field induced damage on Escherichia coli cells and sublethally injured microbial cells using flow cytometry in combination with fluorescent techniques. Food Control 22:566–573
Acknowledgments
This work was supported by the Natural Science Foundation of China (No. 21377014), Science and Technology Research Projects of Liaoning Provincial Department of Education (No. L2013026), and Dalian Municipal Science and Technology Projects (No. 2012E11SF067).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Yin, X., Qiao, S. & Zhou, J. Using electric field to enhance the activity of anammox bacteria. Appl Microbiol Biotechnol 99, 6921–6930 (2015). https://doi.org/10.1007/s00253-015-6631-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-015-6631-0