Skip to main content
SpringerLink
Log in

The short- and long-term effects of nitrite on denitrifying anaerobic methane oxidation (DAMO) organisms

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The denitrifying anaerobic methane oxidation (DAMO) process can achieve methane oxidation and denitrification at the same time by using nitrate or nitrite as an electron acceptor. The short- and long-term effects of nitrite on DAMO organisms were studied from macro (such as denitrification) to micro (such as microbial structure and community) based on two types of DAMO microbial systems. The results showed that the inhibitory effects of nitrite on the two DAMO microbial systems increased with rising concentration and prolonged time. In the short-term inhibitory phase, nitrite with concentrations below 100 mg N L−1 did not inhibit the two distinct DAMO enrichments. When nitrite concentration was increased to 950 mg N L−1, the nitrogen removal performance was completely inhibited. However, in the long-term inhibition experiment, when nitrite concentration was increased to 650 mg N L−1, the nitrogen removal performance was completely inhibited. In addition, in acidic conditions, the real inhibitor of nitrite is FNA (free nitrous acid), while in alkaline conditions, the real inhibitor is the ionized form of nitrite. By using high-throughput sequencing technology, the species abundance and diversity of the two DAMO microbial systems showed an apparent decrease after long-term inhibition, and the community structure also changed significantly. For the enrichment culture dominated by DAMO bacteria, the substantial drop of Methylomonas may be the internal cause of the decreased nitrogen removal rate, and for the coexistence system that hosted both DAMO bacteria and archaea, the reduction of Nitrospirae may be an internal reason for the decline of the denitrification rate.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Allegue T, Arias A, Fernandez-Gonzalez N, Omil F, Garrido JM (2018) Enrichment of nitrite-dependent anaerobic methane oxidizing bacteria in a membrane bioreactor. Chem Eng J 347:721–730

    Article  CAS  Google Scholar 

  • Anthonisen A, Loehr R, Prakasam T, Srinath E (1976) Inhibition of nitrification by ammonia and nitrous-acid. J Wat Pollut Contm Fed 48:835–852

    CAS  Google Scholar 

  • Baker GC, Smith JJ, Cowan DA (2003) Review and re-analysis of domain-specific 16S primers. J Microbiol Methods 55:541–555

  • Chen SQ, Zhang D (2018) Study of corrosion behavior of copper in 3.5 wt.% NaCl solution containing extracellular polymeric substances of an aerotolerant sulphate-reducing bacteria. Corros Sci 136:275–284

    Article  CAS  Google Scholar 

  • Cho S, Yoshitaka T, Naoki F, Yohei Y, Hisashi S, Satoshi O (2010) Nitrogen removal performance and microbial community analysis of an anaerobic up-flow granular bed anammox reactor. Chemosphere 78(9):1129–1135

    Article  CAS  Google Scholar 

  • Chu ZR, Wang K, Li XK, Zhu MT, Yang L, Zhang J (2015) Microbial characterization of aggregates within a one-stage nitritation–anammox system using high-throughput amplicon sequencing. Chem Eng J 262:41–48

    Article  CAS  Google Scholar 

  • Coma M, Verawaty M, Pijuan M, Yuan Z, Bond PL (2012) Enhancing aerobic granulation for biological nutrient removal from domestic wastewater. Bioresour Technol 103(1):101–108

    Article  CAS  Google Scholar 

  • DeLong EF (2000) Microbiology—resolving a methane mystery. Nature 407(6804):577–579

    Article  CAS  Google Scholar 

  • Ding J, Fu L, Ding ZW, Lu YZ, Cheng SH, Zeng RJ (2015) Environmental evaluation of coexistence of denitrifying anaerobic methane-oxidizing archaea and bacteria in a paddy field. Appl Microbiol Biotechnol 100(1):1–8

    Google Scholar 

  • Dolinšek J, Lagkouvardos I, Wanek W, M Wagner M, Daims H (2013) Interactions of nitrifying bacteria and heterotrophs: identification of a Micavibrio-like putative predator of Nitrospira spp. Appl Environ Microb 79(6):2027–2037

    Article  CAS  Google Scholar 

  • Duan H, Wang QL, Erler DV, Ye L, Yuan ZG (2018) Effects of free nitrous acid treatment conditions on the nitrite pathway performance in mainstream wastewater treatment. Sci Total Environ 644:360–370

    Article  CAS  Google Scholar 

  • Egli K, Fanger U, Alvarez PJ (2001) Enrichment and characterization of an anammox bacterium from a rotating biological contactor treating ammonium-rich leachate. Arch Microbiol 175(3):198–207

    Article  CAS  Google Scholar 

  • Ettwig KF, Shima S, van de Pas-Schoonen KT, Kahnt J, Medema MH, Op den Camp HJ, Jetten MS, Strous M (2008) Denitrifying bacteria anaerobically oxidize methane in the absence of archaea. Environ Microbiol 10(11):3164–3173

    Article  CAS  Google Scholar 

  • Ettwig KF, van Alen T, van de Pas-Schoonen KT, Jetten MSM, Strous M (2009) Enrichment and molecular detection of denitrifying methanotrophic bacteria of the NC10 phylum. Appl Environ Microbiol 75(11):3656–3662

    Article  CAS  Google Scholar 

  • Eugene WR, Baird RB, Eaton AD, Clesceri LS (1998) Standard Methods for the Examination of Water and Wastewater, 20th Edition. American N.A. Assoc., American Water Works Assoc., Water Pollution Control Fed Washington DC.

  • Francis CW, Mankin JB (1977) High nitrate denitrification in continuous flow-stirred reactors. Water Res 11(3):289–294

    Article  CAS  Google Scholar 

  • Furukawa K, Inatomi Y, Qiao S, Quan L, Yamamoto T, Isaka K, Sumino T (2009) Innovative treatment system for digester liquor using anammox process. Bioresour Technol 100(22):5437–5443

    Article  CAS  Google Scholar 

  • Fux C, Sierist H (2004) Nitrogen removal from sludge digester liquids by nitrification/denitrification or partial nitriation/anammox: environmental and economical considerations. Water Sci Technol 50(10):19–26

    Article  CAS  Google Scholar 

  • He ZF, Geng S, Pan YW, Cai CY, Wang JQ, Wang LQ, Liu S, Zheng P, Xu XH, Hu BL (2015a) Improvement of the trace metal composition of medium for nitrite-dependent anaerobic methane oxidation bacteria: iron (II) and copper (II) make a difference. Water Res 85:235–243

    Article  CAS  Google Scholar 

  • He ZF, Geng S, Shen LD, Lou LP, Zheng P, Xu X, Hu BL (2015b) The short- and long-term effects of environmental conditions on anaerobic methane oxidation coupled to nitrite reduction. Water Res 68:554–562

    Article  CAS  Google Scholar 

  • Ho A, Kerckhof FM, Luke C, Reim A, Krause S, Boon N, Bodelier PLE (2013) Conceptualizing functional traits and ecological characteristics of methane-oxidizing bacteria as life strategies. Environ Microbiol Rep 5:335–345

    Article  CAS  Google Scholar 

  • Hu S, Zeng RJ, Burow LC, Lant PA, Keller J, Yuan Z (2009) Enrichment of denitrifying anaerobic methane oxidizing microorgansims. Environ Microbiol Rep 1(5):377–384

    Article  CAS  Google Scholar 

  • Hu SH, Zeng RJ, Keller J, Lant PA, Yuan Z (2011) Effect of nitrate and nitrite on the selection of microorganisms in the denitrifying anaerobic methane oxidation process. Environ Microbiol Rep 3(3):315–319

    Article  CAS  Google Scholar 

  • Hu BL, He ZF, Geng S, Cai C, Lou LP, Zheng P, Xu X (2014a) Cultivation of nitrite-dependent anaerobic methane-oxidizing bacteria: impact of reactor configuration. Appl Microbiol Biotechnol 98:7983–7991

    Article  CAS  Google Scholar 

  • Hu BL, Shen LD, Lian X, Zhu Q, Liu H, He Z, Geng S, Cheng DQ, Lou LP, Xu X, Zheng P, He Y (2014b) Evidence for nitrite-dependent anaerobic methane oxidation as a previously overlooked microbial methane sink in wetlands. Proc N A Acad Sci U S A 111(12):4495–4500

    Article  CAS  Google Scholar 

  • Hu X, Xie L, Shim H, Zhang S, Yang D (2014c) Biological nutrient removal in a full scale anoxic/anaerobic/aerobic/pre-anoxic-MBR Plant for low C/N ratio municipal wastewater treatment. Chin J Chem Eng 22(4):447–454

    Article  CAS  Google Scholar 

  • Jaroszynski LW, Cicek N, Sparling R, Oleszkiewicz JA (2011) Importance of the operating pH in maintaining the stability of anoxic ammonium oxidation (anammox) activity in moving bed biofilm reactors. Bioresour Technol 102(14):7051–7056

    Article  CAS  Google Scholar 

  • Jung JY, Kang SH, Chung YC, Ahn DH (2007) Factors affecting the activity of anammox bacteria during start up in the continuous culture reactor. Water Sci Technol 55(1/2):459–468

    Article  CAS  Google Scholar 

  • Kampman C, Hendrickx TLG, Luesken FA, Alen TA, Camp HJM, Jetten MSM, Zeeman G, Buisman CJN, Temmink H (2012) Enrichment of denitrifying methanotrophic bacteria for application after direct low-temperature anaerobic sewage treatment. J Hazard Mater 227-228:164–171

    Article  CAS  Google Scholar 

  • Kumaraswamy S, Ramakrishnan B, Sethunathan N (2001) Methane production and oxidation in an anoxic rice soil as influenced by inorganic redox species. J Environ Qual 30(6):2195–2201

    Article  CAS  Google Scholar 

  • Li WW, Lu PL, Chai FG, Zhang LL, Han XK, Zhang DJ (2018) Long-term nitrate removal through methane-dependent denitrification microorganisms in sequencing batch reactors fed with only nitrate and methane. AMB Express 8(1):108

    Article  CAS  Google Scholar 

  • Lotti F, Imlach WL, Saieva L, Beck ES, Le HT, Li DK, Jiao W, Mentis GZ, Beattie CE (2012) An SMN-dependent U12 splicing event essential for motor circuit function. Cell 151:440–454

    Article  CAS  Google Scholar 

  • Lou JQ, Wang XL, Yang DY, Sun PD (2016) Effects of electron acceptor and inoculum on denitrifying anaerobic methane oxidation (DAMO) organisms. Acta Sci Circumst 36(11):4087–4095 (in Chinese)

    CAS  Google Scholar 

  • Luciene ABS, Laura RL, Guilherme O, Carlos ALC, CAr J (2017) Illumina sequencing-based analysis of a microbial community enriched under anaerobic methane oxidation condition coupled to denitrification revealed coexistence of aerobic and anaerobic methanotrophs. Environ Sci Pollut Res 24(20):1–14

    Google Scholar 

  • Luesken FA, Wu ML, Op den Camp HJ, Keltjens JT, Stunnenberg H, Francoijs KJ, Strous M, Jetten MS (2012) Effect of oxygen on the anaerobic methanotroph ‘Candidatus Methylomirabilis oxyfera’: kinetic and transcriptional analysis. Environ Microbiol 14(4):1024–1034

    Article  CAS  Google Scholar 

  • Luo JH, Chen H, Yuan Z, Guo J (2018) Methane-supported nitrate removal from groundwater in a membrane biofilm reactor. Water Res 132:71–78

    Article  CAS  Google Scholar 

  • Ma B, Yang L, Wang QL, Yuan ZG, Wang YY, Peng YZ (2017) Inactivation and adaptation of ammonia-oxidizing bacteria and nitrite-oxidizing bacteria when exposed to free nitrous acid. Bioresour Technol 245:1266–1270

    Article  CAS  Google Scholar 

  • Moradi M, Song Z, Xiao T (2018) Exopolysaccharide produced by Vibrio neocaledonicus sp. as a green corrosion inhibitor: production and structural characterization. J Mater Sci Technol 34(12):2447–2457

    Article  Google Scholar 

  • Murrell JC (1992) Genetics and molecular biology of methanotrophs. FEMS Microbiol Rev 8(3–4):233–248

    Article  CAS  Google Scholar 

  • Oberoi AS, Philip L, Bhallamudi SM (2015) Biodegradation of various aromatic compounds by enriched bacterial cultures: Part A-monocyclic and polycyclic aromatic hydrocarbons. Appl Biochem Biotechnol 176:1870–1888

  • Pallach M, Marchetti R, Di Lorenzo F, Fabozzi A, Giraud E, Gully D, Paduano L, Molinaro A, Errico GD, Silipo A (2018) Zymomonas mobilis exopolysaccharide structure and role in high ethanol tolerance. Carbohyd Polym 201:293–299

    Article  CAS  Google Scholar 

  • Pijuan M, Ye L, Yuan Z (2010) Free nitrous acid inhibition on the aerobic metabolism of poly-phosphate accumulating organisms. Water Res 44(20):6063–6072

    Article  CAS  Google Scholar 

  • Podosokorskaya OA, Kadnikov VV, Gavrilov SN, Mardanov AV, Merkel AY, Karnachuk OV (2013) Characterization of Melioribacter roseus gen. nov., sp nov., a novel facultatively anaerobic thermophilic cellulolytic bacterium from the class Ignavibacteria, and a proposal of a novel bacterial phylum Ignavibacteriae. Environ Microbiol 15:1759–1771

    Article  CAS  Google Scholar 

  • Puyol JM, Carvajal-Arroyo R, Sierra-Alvarez JA (2014) Nitrite (not free nitrous acid) is the main inhibitor of the anammox process at common pH conditions. Biotechnol Lett 36:547–551

    Article  CAS  Google Scholar 

  • Raghoebarsing AA, Pol A, van de Pas-Schoonen KT, Smolders AJP, Ettwig KF, Rijpstra WIC, Schouten S, Damsté JSS, Op den Camp HJM, Jetten MSM, Strous M (2006) A microbial consortium couples anaerobic methane oxidation to denitrification. Nature 440(7086):918–921

    Article  CAS  Google Scholar 

  • Saito T, Brdjanovic D, van Loosdrecht MCM (2004) Effect of nitrite on phosphate uptake by phosphate accumulating organisms. Water Res 38(17):3760–3768

    Article  CAS  Google Scholar 

  • Schramm A, De Beer D, Gieseke A, Amann R (2000) Microenvironments and distribution of nitrifying bacteria in a membrane-bound biofilm. Environ Microbiol 2:680–686

    Article  CAS  Google Scholar 

  • Sheng GP, Yu HQ, Li XY (2010) Extracellular polymeric substances (EPS) of microbial aggregates in biological wastewater treatment systems: a review. Biotechnol Adv 28:882–894

    Article  CAS  Google Scholar 

  • Strous M, Kuenen JG, Jetten MSM (1999) Key physiology of anaerobic ammonium oxidation. Appl Eviron Microbiol 65(7):3248–3250

    CAS  Google Scholar 

  • Sun SP, Nàcher CPI, Merkey B, Zhou Q, Xia SQ, Yang DH, Sun JH, Smets BF (2010) Effective biological nitrogen removal treatment processes for domestic wastewaters with low C/N ratios: a review. Environ Eng Sci 27(2):111–126

    Article  CAS  Google Scholar 

  • Tan LC, Nancharaiah YV, Lu SP, van Hullebusch ED, Gerlach R, Lens PNL (2018) Biological treatment of selenium-laden wastewater containing nitrate and sulfate in an upflow anaerobic sludge bed reactor at pH 5.0. Chemosphere 211:684–693

    Article  CAS  Google Scholar 

  • Vadivelu VM, Yuan ZG, Fux C, Keller J (2006) The inhibitory effects of free nitrous acid on the energy generation and growth processes of an enriched Nitrobacter culture. Environ Sci Technol 40(14):4442–4448

    Article  CAS  Google Scholar 

  • Wang DB, Wang YL, Liu YW, Ngo HH, Lian Y, Zhao JW, Chen F, Yang Q, Zeng GM, Li XM (2017a) Is denitrifying anaerobic methane oxidation-centered technologies a solution for the sustainable operation of wastewater treatment plants? Bioresour Technol 234:456–465

    Article  CAS  Google Scholar 

  • Wang R, Yang C, Zhang M, Xu SY, Dai CL, Liang LY, Zhao HP, Zheng P (2017b) Chemoautotrophic denitrification based on ferrous iron oxidation: reactor performance and sludge characteristics. Chem Eng J 313:693–701

    Article  CAS  Google Scholar 

  • Wang YL, Wang D, Yang Q, Zeng G, Li X (2017c) Wastewater opportunities for denitrifying anaerobic methane oxidation. Trends Biotechnol 35(09):799–802

    Article  CAS  Google Scholar 

  • Wang XL, Yan YG, Gao DW (2018) The threshold of influent ammonium concentration for nitrate over-accumulation in a one-stage deammonification system with granular sludge without aeration. Sci Total Environ 634:843–852

    Article  CAS  Google Scholar 

  • Wett (2007) Development and implementation of a robust deammonification process. Water Sci Technol 56(7):81–88

    Article  CAS  Google Scholar 

  • Wu ML, de Vries S, van Alen TA, Butler MK, Op den Camp HJ, Keltjens JT, Jetten MS, Strous M (2011a) Physiological role of the respiratory quinol oxidase in the anaerobic nitrite-reducing methanotroph ‘Candidatus Methylomirabilis oxyfera. Microbiology 157(3):890–898

    Article  CAS  Google Scholar 

  • Wu ML, Ettwig KF, Jetten MS, Strous M, Keltjens JT, van Niftrik L (2011b) A new intra-aerobic metabolism in the nitrite-dependent anaerobic methane-oxidizing bacterium ‘Candidatus Methylomirabilis oxyfera’. Biochem Soc Trans 39(1):243–248

    Article  CAS  Google Scholar 

  • Yu H, Kashima H, Regan JM, Hussain A, Elbeshbishy E, Lee HS (2017) Kinetic study on anaerobic oxidation of methane coupled to denitrification. Enzyme Micro Tech 11(104):47–55

    Article  CAS  Google Scholar 

  • Zeng XY, Takahiro H, Hiroto O (2016) Comparison of microbial communities inside and outside of a denitrification hotspot in confined groundwater. Int Biodeterior Biodegrad 114:104–109

    Article  CAS  Google Scholar 

  • Zhang F, Hou J, Miao L, Chen J, Xu Y, You G, Liu S, Ma J (2018) Chlorpyrifos and 3,5,6-trichloro-2-pyridinol degradation in zero valent iron coupled anaerobic system: performances and mechanisms. Chem Eng J 353:254–263

    Article  CAS  Google Scholar 

  • Zhou Y, Pijuan M, Zeng RJ, Yuan Z (2008) Free nitrous acid inhibition on nitrous oxide reduction by a denitrifying-enhanced biological phosphorus removal sludge. Environ Sci Technol 42(22):8260–8265

    Article  CAS  Google Scholar 

  • Zhou Y, Ganda L, Lim M, Yuan ZG, Staffan K, Jern WN (2010) Free nitrous acid (FNA) inhibition on denitrifying poly-phosphate accumulating organisms (DPAOs). Appl Microbiol Biotechnol 88(1):359–369

    Article  CAS  Google Scholar 

  • Zhou Y, Oehmen A, Lim M, Vadivelu V, Ng WJ (2011) The role of nitrite and free nitrous acid (FNA) in wastewater treatment plants. Water Res 45(15):4672–4682

    Article  CAS  Google Scholar 

  • Zhu N, Tang J, Tang C, Duan P, Yao L, Wu Y, Dionysiou DD (2018) Combined CdS nanoparticles-assisted photocatalysis and periphytic biological processes for nitrate removal. Chem Eng J 353:237–245

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was financially supported by the Key Project of Science and Technology of Zhejiang Province, China (no. 2014C03002) and the central government’s specially supported funding for the development of local colleges and universities (no. S1701).

Author information

Authors and Affiliations

  1. School of Environmental Science and Engineering, Zhejiang Gongshang University, No. 149, Jiaogong Road, Hangzhou, 310012, China

    Juqing Lou, Xilei Wang, Jiaping Li & Jingyi Han

Authors
  1. Juqing Lou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xilei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jiaping Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jingyi Han
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Juqing Lou.

Ethics declarations

Conflict of interest

J.L. declares that she has no conflict of interest.

X.W. declares that she has no conflict of interest.

J.L. declares that she has no conflict of interest.

J.H. declares that he has no conflict of interest.

Ethical approval

This article does not contain any studies with human participants performed by any of the authors.

Additional information

Responsible editor: Gerald Thouand

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lou, J., Wang, X., Li, J. et al. The short- and long-term effects of nitrite on denitrifying anaerobic methane oxidation (DAMO) organisms. Environ Sci Pollut Res 26, 4777–4790 (2019). https://doi.org/10.1007/s11356-018-3936-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-018-3936-4

Keywords

Search

Navigation