Abstract
Anaerobic bioreactors that can support simultaneous microbial processes of denitrification and methanogenesis are of interest to nutrient nitrogen removal. However, an important concern is the potential toxicity of nitrate (NO3 −) and nitrite (NO2 −) to methanogenesis. The methanogenic toxicity of the NO −x compounds to anaerobic granular biofilms and municipal anaerobic digested sludge with two types of substrates, acetate and hydrogen, was studied. The inhibition was the severest when the NO −x compounds were still present in the media (exposure period). During this period, 95% or greater inhibition of methanogenesis was evident at the lowest concentrations of added NO2 − tested (7.6–10.2 mg NO2 −-N l−1) or 8.3–121 mg NO3 −-N l−1 of added NO3 −, depending on substrate and inoculum source. The inhibition imparted by NO3 − was not due directly to NO3 − itself, but instead due to reduced intermediates (e.g., NO2 −) formed during the denitrification process. The toxicity of NO −x was found to be reversible after the exposure period. The recovery of activity was nearly complete at low added NO −x concentrations; whereas the recovery was only partial at high added NO −x concentrations. The recovery is attributed to the metabolism of the NO −x compounds. The assay substrate had a large impact on the rate of NO2 − metabolism. Hydrogen reduced NO2 − slowly such that NO2 − accumulated more and as a result, the toxicity was greater compared to acetate as a substrate. The final methane yield was inversely proportional to the amount of NO −x compounds added indicating that they were the preferred electron acceptors compared to methanogenesis.
Similar content being viewed by others
Abbreviations
- Anammox:
-
Anaerobic ammonium oxidation
- AOB:
-
Ammonia oxidizing bacteria
- AS:
-
Activated sludge
- BNNR:
-
Biological nutrient nitrogen removal
- DNRA:
-
Dissimilatory nitrate reduction to ammonium
- EGSB:
-
Expanded granular sludge bed reactor
- NPB:
-
Nitrite oxidizing bacteria
- VFA:
-
Volatile fatty acids
- UASB:
-
Upflow anaerobic sludge blanket reactor
- WWTPs:
-
Wastewater treatment plants
References
Akunna JC, Bizeau C, Moletta R (1992) Denitrification in anaerobic digesters—possibilities and influence of waste-water Cod/N-Nox ratio. Environ Technol 13:825–836. doi:10.1080/09593339209385217
An YY, Yang FL, Wong FS, Chua HC (2008) Simultaneous bioenergy (CH4) production and nitrogen removal in a combined upflow anaerobic sludge blanket and aerobic membrane bioreactor. Energy Fuels 22:103–107. doi:10.1021/ef7002816
APHA (2005) In: Eaton AD, Clesceri LS, Rice EW, Greenberg AE (eds) Standard Methods for the Examination of Water and Wastewater, 21st edn. American Public Health Association, Washington DC, pp 1368
Appels L, Baeyens J, Degreve J, Dewil R (2008) Principles and potential of the anaerobic digestion of waste-activated sludge. Prog Energy Combust Sci 34:755–781. doi:10.1016/j.pecs.2008.06.002
Balderston WL, Payne WJ (1976) Inhibition of methanogenesis in salt-marsh sediments and whole-cell suspensions of methanogenic bacteria by nitrogen-oxides. Appl Environ Microbiol 32(2):264–269
Baloch MI, Akunna JC, Collier PJ (2006) Carbon and nitrogen removal in a granular bed baffled reactor. Environ Technol 27:201–208. doi:10.1080/09593332708618634
Barker HA (1941) Biochemical activities of studies on the methane fermentation: V. Methanobacterium omdianskii. J Biol Chem 137:153–167
Clarens M, Bernet N, Delgenes JP, Moletta R (1998) Effects of nitrogen oxides and denitrification by Pseudomonas stutzeri on acetotrophic methanogenesis by Methanosarcina mazei. FEMS Microbiol Ecol 25:271–276. doi:10.1111/j.1574-6941.1998.tb00479.x
Ekama GA, Wentzel MC (2008) Nitrogen removal. In: Henze M, van Loosdrecht MCM, Ekema GA, Brdjanovic D (eds) Biological wastewater treatment: principles, modelling and design. IWA Publishing, London, pp 87–138
Frankin RJ (2001) Full-scale experiences with anaerobic treatment of industrial wastewater. Water Sci Technol 44:1–6
Hendriksen HV, Ahring BK (1996) Integrated removal of nitrate and carbon in an upflow anaerobic sludge blanket (UASB) reactor: operating performance. Water Res 30:1451–1458. doi:10.1016/0043-1354(96)00041-3
Henze M, Comeau Y (2008) Wastewater characterization. In: Henze M, van Loosdrecht MCM, Ekema GA, Brdjanovic D (eds) Biological wastewater treatment: principles, modelling and design. IWA Publishing, London, pp 33–52
Huang JS, Chou HH, Chen CM, Chiang CM (2007) Effect of recycle-to-influent ratio on activities of nitrifiers and denitrifiers in a combined UASB-activated sludge reactor system. Chemosphere 68:382–388. doi:10.1016/j.chemosphere.2007.01.037
Jetten M, Schmid M, van de Pas-Schoonen K, Damste JSS, Strous M (2005) Anammox organisms: enrichment, cultivation, and environmental analysis. Environ Microbiol 397:34–57
Kalyuzhnyi SV, Gladchenko MA, Kang H, Mulder A, Versprille A (2008) Development and optimisation of VFA driven DEAMOX process for treatment of strong nitrogenous anaerobic effluents. Water Sci Technol 57:323–328. doi:10.2166/wst.2008.044
Kassam ZA, Yerushalmi L, Guiot SR (2003) A market study on the anaerobic wastewater treatment systems. Water Air Soil Pollut 143:179–192. doi:10.1023/A:1022807416773
Kjeldsen P, Barlaz MA, Rooker AP, Baun A, Ledin A, Christensen TH (2002) Present and long-term composition of MSW landfill leachate: a review. Crit Rev Environ Sci Technol 32:297–336. doi:10.1080/10643380290813462
Kluber HD, Conrad R (1998) Inhibitory effects of nitrate, nitrite, NO and N2O on methanogenesis by Methanosarcina barkeri and Methanobacterium bryantii. FEMS Microbiol Ecol 25:331–339
Knight RL, Payne VWE, Borer RE, Clarke RA, Pries JH (2000) Constructed wetlands for livestock wastewater management. Ecol Eng 15:41–55. doi:10.1016/S0925-8574(99)00034-8
Kuenen JG (2008) Anammox bacteria: from discovery to application. Nat Rev Microbiol 6:320–326. doi:10.1038/nrmicro1857
Lee CY, Shin HS, Hwang SJ (2004) Characteristics of granular sludge in a single upflow sludge blanket reactor treating high levels of nitrate and simple organic compounds. Water Sci Technol 50:217–224
Mallin MA, Cahoon LB (2003) Industrialized animal production—a major source of nutrient and microbial pollution to aquatic ecosystems. Popul Environ 24:369–385. doi:10.1023/A:1023690824045
Mulder A, Vandegraaf AA, Robertson LA, Kuenen JG (1995) Anaerobic ammonium oxidation discovered in a denitrifying fluidized-bed reactor. FEMS Microbiol Ecol 16:177–183. doi:10.1111/j.1574-6941.1995.tb00281.x
O’Reilly C, Colleran E (2005) Toxicity of nitrite toward mesophilic and thermophilic sulphate-reducing, methanogenic and syntrophic populations in anaerobic sludge. J Ind Microbiol Biotechnol 32:46–52. doi:10.1007/s10295-004-0204-z
Peng YZ, Zhang SJ, Zeng W, Zheng SW, Mino T, Satoh H (2008) Organic removal by denitritation and methanogenesis and nitrogen removal by nitritation from landfill leachate. Water Res 42:883–892. doi:10.1016/j.watres.2007.08.041
Rittman BE, McCarty PL (2001) Environmental biotechnology: principles and applications. McGraw-Hill, New York, p 754
Strous M, Fuerst JA, Kramer EHM, Logemann S, Muyzer G, van de Pas-Schoonen KT, Webb R, Kuenen JG, Jetten MSM (1999) Missing lithotroph identified as new planctomycete. Nature 400(6743):446–449. doi:10.1038/22749
Sumino T, Isaka K, Ikuta H, Saiki Y, Yokota T (2006) Nitrogen removal from wastewater using simultaneous nitrate reduction and anaerobic ammonium oxidation in single reactor. J Biosci Bioeng 102:346–351. doi:10.1263/jbb.102.346
Tai CS, Singh KS, Grant SR (2006) Combined removal of carbon and nitrogen in an integrated UASB-jet loop reactor bioreactor system. J Environ Eng 132:624–637. doi:10.1061/(ASCE)0733-9372(2006)132:6(624)
Tchobanoglous G, Burtob FL, Stensel HD (2003) Wastewater engineering treatment and reuse: Metcalf & Eddy. McGraw-Hill, New York, p 1819
Tugtas AE, Pavlostathis SG (2007a) Inhibitory effects of nitrogen oxides on a mixed methanogenic culture. Biotechnol Bioeng 96:444–455. doi:10.1002/bit.21105
Tugtas AE, Pavlostathis SG (2007b) Effect of sulfide on nitrate reduction in mixed methanogenic cultures. Biotechnol Bioeng 97:1448–1459. doi:10.1002/bit.21338
Tugtas AE, Pavlostathis SG (2008) Inhibitory effects of nitrate reduction on methanogenesis in the presence of different electron donors. Water Sci Technol 57(5):693–698. doi:10.2166/wst.2008.069
van der Star WRL, Abma WR, Blommers D, Mulder JW, Tokutomi T, Strous M, Picioreanu 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. doi:10.1016/j.watres.2007.03.044
van Dongen U, Jetten MSM, van Loosdrecht MCM (2001) The SHARON®-Anammox® process for treatment of ammonium rich wastewater. Water Sci Technol 44(1):153–160
van Haandel A, Kato M, Cavalcanti P, Florencio L (2006) Anaerobic reactor design concepts for the treatment of domestic wastewater. Rev Environ Sci Biotechnol 5:21–38. doi:10.1007/s11157-005-4888-y
Vandegraaf AA, Mulder A, Debruijn P, Jetten MSM, Robertson LA, Kuenen JG (1995) Anaerobic oxidation of ammonium is a biologically mediated process. Appl Environ Microbiol 61:1246–1251
Vigneron V, Ponthieu M, Barina G, Audic JM, Duquennoi C, Mazeas L, Bernet N, Bouchez T (2007) Nitrate and nitrite injection during municipal solid waste anaerobic biodegradation. Waste Manag 27:778–791. doi:10.1016/j.wasman.2006.02.020
Zhang DJ (2003) The integration of methanogenesis with denitrification and anaerobic ammonium oxidation in an expanded granular sludge bed reactor. J Environ Sci (China) 15:423–432
Acknowledgments
This research was supported in part by grants of the University of Arizona Water Sustainability Program (TRIF-WSP) and from the International Arid Lands Consortium (IALC award # 06R-02).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Banihani, Q., Sierra-Alvarez, R. & Field, J.A. Nitrate and nitrite inhibition of methanogenesis during denitrification in granular biofilms and digested domestic sludges. Biodegradation 20, 801–812 (2009). https://doi.org/10.1007/s10532-009-9268-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10532-009-9268-9