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Enrichment of denitrifying methanotrophic bacteria from Taihu sediments by a membrane biofilm bioreactor at ambient temperature

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Abstract

Denitrification coupled to anaerobic methane oxidation is a recently discovered process performed by bacteria affiliated to the NC10 phylum. These microorganisms could play important roles in the energy-efficient way of anaerobic wastewater treatment where residual dissolved methane might be removed at the expense of nitrate or nitrite. The difficulty to enrich these microorganisms due to a slow growth rate, especially at low temperatures, limited its application in engineering field. In this study, an NC10 bacteria community was enriched from Taihu sediments by a membrane biofilm bioreactor at ambient temperature of 10–25 °C. After 13 months enrichment, the maximum denitrification rate of the enriched culture reached 0.54 mM day−1 for nitrate and 1.06 mM day−1 for nitrite. Anaerobic methane oxidation coupled denitrification was estimated from the 13C-labeled CO2 (13CO2) production during batch incubations with 13CH4. Furthermore, analysis of 16S rRNA genes clone library confirmed the presence of NC10 phylum bacteria and fluorescence in situ hybridization showed that NC10 bacteria dominated the reactor. All of the results indicated the NC10 bacteria community was competitive in terms of treating nitrate-contaminated water or wastewater under natural conditions.

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References

  • Bogner J, Pipatti R, Hashimoto S, Diaz C, Mareckova K, Diaz L, Kjeldsen P, Monni S, Faaij A, Gao Q, Zhang T, Ahmed MA, Sutamihardja RT, Gregory R (2008) Mitigation of global greenhouse gas emissions from waste: conclusions and strategies from the Intergovernmental Panel on Climate Change (IPCC) Fourth Assessment Report. Working Group III (Mitigation). Waste Manag Res 26:11–32

    Article  Google Scholar 

  • Chen XM, Guo JH, Shi Y, Hu SH, Yuan ZG, Ni BJ (2014) Modeling of simultaneous anaerobic methane and ammonium oxidation in a membrane biofilm reactor. Environ Sci Technol 48:9540–9547

    Article  CAS  Google Scholar 

  • Daims H, Bruhl A, Amann R, Schleifer KH, Wagner M (1999) The domain-specific probe EUB338 is insufficient for the detection of all bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22:434–444

    Article  CAS  Google Scholar 

  • Deutzmann JS, Schink B (2011) Anaerobic oxidation of methane in sediments of Lake Constance, an oligotrophic freshwater lake. Appl Environ Microbiol 77:4429–4436

    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 10:3164–3173

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hu SH, Zeng RJ, Burow LC, Lant P, Keller J, Yuan ZG (2009) Enrichment of denitrifying anaerobic methane oxidizing microorganisms. Environ Microbiol Rep 1:377–384

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Islas-Lima S, Thalasso F, Gomez-Hernandez J (2004) Evidence of anoxic methane oxidation coupled to denitrification. Water Res 38:13–16

    Article  CAS  Google Scholar 

  • Juretschko S, Timmermann G, Schmid M, Schleifer KH, Pommerening-Roser A, Koops HP, Wagner M (1998) Combined molecular and conventional analyses of nitrifying bacterium diversity in activated sludge: Nitrosococcus mobilis and Nitrospira-like bacteria as dominant populations. Appl Environ Microbiol 64:3042–3051

    CAS  Google Scholar 

  • Kampman C, Hendrickx TL, Luesken FA, van Alen TA, Op den Camp HJ, Jetten MS, Zeeman G, Buisman CJ, 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  Google Scholar 

  • Kojima H, Tsutsumi M, Ishikawa K, Iwata T, Mussmann M, Fukui M (2012) Distribution of putative denitrifying methane oxidizing bacteria in sediment of a freshwater lake, Lake Biwa. Syst Appl Microbiol 35:233–238

    Article  CAS  Google Scholar 

  • Luesken FA, Sanchez J, van Alen TA, Sanabria J, Op den Camp HJ, Jetten MS, Kartal B (2011a) Simultaneous nitrite-dependent anaerobic methane and ammonium oxidation processes. Appl Environ Microbiol 77:6802–6807

    Article  CAS  Google Scholar 

  • Luesken FA, van Alen TA, van der Biezen E, Frijters C, Toonen G, Kampman C, Hendrickx TL, Zeeman G, Temmink H, Strous M, Op den Camp HJ, Jetten MS (2011b) Diversity and enrichment of nitrite-dependent anaerobic methane oxidizing bacteria from wastewater sludge. Appl Microbiol Biotechnol 92:845–854

    Article  CAS  Google Scholar 

  • Meulepas RJ, Jagersma CG, Gieteling J, Buisman CJ, Stams AJ, Lens PN (2009) Enrichment of anaerobic methanotrophs in sulfate-reducing membrane bioreactors. Biotechnol Bioeng 104:458–470

    Article  CAS  Google Scholar 

  • Modin O, Fukushi K, Nakajima F, Yamamoto K (2008) Performance of a membrane biofilm reactor for denitrification with methane. Bioresour Technol 99:8054–8060

    Article  CAS  Google Scholar 

  • Park JY, Yoo YJ (2009) Biological nitrate removal in industrial wastewater treatment: which electron donor we can choose. Appl Microbiol Biotechnol 82:415–429

    Article  CAS  Google Scholar 

  • Raghoebarsing AA, Pol A, van de Pas-Schoonen KT, Smolders AJ, Ettwig KF, Rijpstra WI, Schouten S, Damste JS, Op den Camp HJ, Jetten MS, Strous M (2006) A microbial consortium couples anaerobic methane oxidation to denitrification. Nature 440:918–921

    Article  CAS  Google Scholar 

  • Shen LD, Liu S, Zhu Q, Li XY, Cai C, Cheng DQ, Lou LP, Xu XY, Zheng P, Hu BL (2013) Distribution and diversity of nitrite-dependent anaerobic methane-oxidising bacteria in the sediments of the Qiantang River. Microb Ecol 67:341–349

    Article  Google Scholar 

  • Shen LD, Liu S, Huang Q, Lian X, He ZF, Geng S, Jin RC, He YF, Lou LP, Xu XY, Zheng P, Hu BL (2014) Evidence for the cooccurrence of nitrite-dependent anaerobic ammonium and methane oxidation processes in a flooded paddy field. Appl Environ Microbiol 80:7611–7619

    Article  Google Scholar 

  • Shi Y, Hu SH, Lou JQ, Lu PL, Keller J, Yuan ZG (2013) Nitrogen removal from wastewater by coupling anammox and methane-dependent denitrification in a membrane biofilm reactor. Environ Sci Technol 47:11577–11583

    Article  CAS  Google Scholar 

  • Syron E, Casey E (2008) Membrane-aerated biofilms for high rate biotreatment: performance appraisal, engineering principles, scale up, and development requirements. Environ Sci Technol 42:1833–1844

    Article  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  Google Scholar 

  • Thalasso F, Vallecillo A, Garchia-Encina P, Fdz-Polanco F (1997) The use of methane as a sole carbon source for waste water denitrification. Water Res 1:55–60

    Article  Google Scholar 

  • Thauer RK, Shima S (2008) Methane as fuel for anaerobic microorganisms. Ann N Y Acad Sci 1125:158–170

    Article  CAS  Google Scholar 

  • Wang Y, Zhu G, Harhangi HR, Zhu B, Jetten MS, Yin C, Op den Camp HJ (2012) Co-occurrence and distribution of nitrite-dependent anaerobic ammonium and methane-oxidizing bacteria in a paddy soil. FEMS Microbiol Lett 336:79–88

    Article  CAS  Google Scholar 

  • WEF AA (2005) Standard methods for the examination of water and wastewater, first ed. American Public Health Association, American Water Works Association, Water Environmental Federation, Washington DC

    Google Scholar 

  • Zhou LL, Wang Y, Long XE, Guo JH, Zhu GB (2014) High abundance and diversity of nitrite-dependent anaerobic methane-oxidizing bacteria in a paddy field profile. FEMS Microbiol Lett 360:33–41

    Article  CAS  Google Scholar 

  • Zhu B, van Dijk G, Fritz C, Smolders AJ, Pol A, Jetten MS, Ettwig KF (2012) Anaerobic oxidization of methane in a minerotrophic peatland: enrichment of nitrite-dependent methane-oxidizing bacteria. Appl Environ Microbiol 78:8657–8665

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by the Science Fund for Creative Research Groups (no. 21221004), China Postdoctoral Science Foundation (no. 2012M510462) Program for Changjiang Scholars, and Innovative Research Team in University and Research Fund (no. 318051417) for the Doctoral Program of Higher Education of Liaocheng University.

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Authors and Affiliations

  1. College of Life Science, Liaocheng University, Liaocheng, 252059, People’s Republic of China

    Shenghui Wang

  2. State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing, 100084, People’s Republic of China

    Shenghui Wang, Qing Wu, Ting Lei, Peng Liang & Xia Huang

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  1. Shenghui Wang
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  2. Qing Wu
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  3. Ting Lei
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  4. Peng Liang
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  5. Xia Huang
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Correspondence to Peng Liang or Xia Huang.

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Responsible editor: Gerald Thouand

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Wang, S., Wu, Q., Lei, T. et al. Enrichment of denitrifying methanotrophic bacteria from Taihu sediments by a membrane biofilm bioreactor at ambient temperature. Environ Sci Pollut Res 23, 5627–5634 (2016). https://doi.org/10.1007/s11356-015-5509-0

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  • DOI: https://doi.org/10.1007/s11356-015-5509-0

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