Skip to main content
SpringerLink
Log in

Spatial and temporal distribution of nitrite-dependent anaerobic methane-oxidizing bacteria in an intertidal zone of the East China Sea

  • Environmental biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Nitrite-dependent anaerobic methane oxidation (N-DAMO), which couples anaerobic methane oxidation and nitrite reduction, is a recently discovered bioprocess coupling microbial nitrogen and carbon cycles. The discovery of this microbial process challenges the traditional knowledge of global methane sinks and nitrogen losses. In this study, the abundance and activity of N-DAMO bacteria were investigated and their contributions to methane sink and nitrogen loss were estimated in different seasons and different partitions of an intertidal zone of the East China Sea. The results showed that N-DAMO bacteria were extensively and continuously present in the intertidal zone, with the number of cells ranging from 5.5 × 104 to 2.8 × 105 copy g−1 soil and the potential activity ranging from 0.52 to 5.7 nmol CO2 g−1 soil day−1, contributing 5.0–36.6% of nitrite- and sulfate-dependent anaerobic methane oxidation in the intertidal zone. The N-DAMO activity and its contribution to the methane consumption were highest in the spring and in the low intertidal zone. These findings showed that the N-DAMO process is an important methane and nitrogen sink in the intertidal zone and varies with the seasons and the partitions of the intertidal zone.

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

Similar content being viewed by others

References

  • Arshad A, Speth DR, De Graaf RM, Op den Camp HJM, Jetten MSM, Welte CU (2015) A metagenomics-based metabolic model of nitrate-dependent anaerobic oxidation of methane by Methanoperedens-like archaea. Front Microbiol 6:1423

    Article  PubMed  PubMed Central  Google Scholar 

  • Beal EJ, House CH, Orphan VJ (2009) Manganese- and iron-dependent marine methane oxidation. Science 325:184–187

    Article  CAS  PubMed  Google Scholar 

  • Borrel G, Jézéquel D, Biderre-Petit C, Morel-Desrosiers N, Morel JP, Peyret P, Fonty G, Lehours AC (2011) Production and consumption of methane in freshwater lake ecosystems. Res Microbiol 162(9):832–847

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Zhou Z, Gu JD (2015) Complex community of nitrite-dependent anaerobic methane oxidation bacteria in coastal sediments of the Mai Po wetland by PCR amplification of both 16S rRNA and pmoA genes. Appl Microbiol Biotechnol 99(3):1463–1473

    Article  CAS  PubMed  Google Scholar 

  • Deutzmann JS, Schink B (2011) Anaerobic oxidation of methane in sediments of Lake Constance, an oligotrophic freshwater lake. Appl Environ Microbiol 77(13):4429–4436

    Article  CAS  PubMed  PubMed Central  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 oxidise methane in the absence of Archaea. Environ Microbiol 10:3164–3173

    Article  CAS  PubMed  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(11):3656–3662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ettwig KF, Butler MK, Le Paslier D, Pelletier E, Mangenot S, Kuypers MM, Schreiber F, Dutilh BE, Zedelius J, de Beer D, Gloerich J, Wessels HJ, van Alen T, Luesken F, Wu ML, van de Pas-Schoonen KT, Op den Camp HJ, Janssen-Megens EM, Francoijs KJ, Stunnenberg H, Weissenbach J, Jetten MSM, Strous M (2010) Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464:543–548

    Article  CAS  PubMed  Google Scholar 

  • Ettwig KF, Zhu BL, Speth DR, Keltjens JT, Jetten MSM, Kartal B (2016) Archaea catalyze iron-dependent anaerobic oxidation of methane. Proc Natl Acad Sci U S A 113(45):12792–12796

    Article  CAS  PubMed Central  Google Scholar 

  • Han P, Gu JD (2013) A newly designed degenerate PCR primer based on pmoA gene for detection of nitrite-dependent anaerobic methane-oxidizing bacteria from different ecological niches. Appl Microbiol Biotechnol 97(23):10155–10162

    Article  CAS  PubMed  Google Scholar 

  • Haroon MF, Hu S, Shi Y, Imelfort M, Keller J, Hugenholtz P, Yuan ZG, Tyson GW (2013) Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature 500:567–570

    Article  CAS  PubMed  Google Scholar 

  • He ZF, Cai C, Shen LD, Lou LP, Zheng P, Xu XH, Hu BL (2015a) Effect of inoculum sources on the enrichment of nitrite-dependent anaerobic methane-oxidizing bacteria. Appl Microbiol Biotechnol 99(2):939–946

    Article  CAS  PubMed  Google Scholar 

  • He ZF, Geng S, Cai CY, Liu S, Liu Y, Pan YW, Lou LP, Zheng P, Xu XH, Hu BL (2015b) Anaerobic oxidation of methane coupled to nitrite reduction by halophilic marine NC10 bacteria. Appl Environ Microbiol 81(16):5538–5545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • He ZF, Cai CY, Wang JQ, Xu XH, Zheng P, Jetten MSM, Hu BL (2016) A novel denitrifying methanotroph of the nc10 phylum and its microcolony. Sci Rep 6:32241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herbert RA (1999) Nitrogen cycling in coastal marine ecosystems. FEMS Microbiol Rev 23(5):563–590

    Article  CAS  PubMed  Google Scholar 

  • Hu BL, Shen LD, Du P, Zheng P, Xu XY, Zeng JN (2012) The influence of intense chemical pollution on the community composition, diversity and abundance of anammox bacteria in the jiaojiang estuary (china). PLoS One 7(3):181–190

    Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Intergovernmental Panel on Climate Change (2001) Climate change 2001: the scientific basis. Contribution of Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge

    Google Scholar 

  • Intergovernmental Panel on Climate Change (2014) Climate Change 2014: Synthesis Report. In: Core Writing Team, Pachauri RK, Meyer LA (eds) Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva 151 pp

    Google Scholar 

  • Juretschko S, Timmermann G, Schmid MC, Schleifer KH, Pommerening-Röser 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  PubMed  PubMed Central  Google Scholar 

  • Knittel K, Boetius A (2009) Anaerobic oxidation of methane: progress with an unknown process. Annu Rev Microbiol 63:311–334

    Article  CAS  PubMed  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(4):233–238

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Metaxas A, Scheibling RE (1993) Community structure and organization of tidepools. Mar Ecol Prog 98(1):187–198

    Article  Google Scholar 

  • Olsson L, Ye S, Yu X, Wei M, Krauss KW, Brix H (2015) Factors influencing CO2 and CH4 emissions from coastal wetlands in the Liaohe Delta, Northeast China. Biogeosciences 12:4965–4977

    Article  Google Scholar 

  • Padilla CC, Bristow LA, Sarode N, Garciarobledo E, Gómez RE, Benson CR, Bourbonnais A, Altabet MA, Girguis PR, Thamdrup B (2016) NC10 bacteria in marine oxygen minimum zones. ISME J 10(8):2067–2071

    Article  CAS  PubMed  PubMed Central  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(7086):918–921

    Article  CAS  PubMed  Google Scholar 

  • Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71(3):1501–1506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen LD, Liu S, Lou LP, Liu WP, Xu XY, Zheng P, Hu BL (2013) Broad distribution of diverse anaerobic ammonium-oxidising bacteria in Chinese agricultural soils. Appl Environ Microbiol 79:6167–6172

    Article  CAS  PubMed  PubMed Central  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 (2014a) Evidence for the cooccurrence of nitrite-dependent anaerobic ammonium and methane oxidation processes in a flooded paddy field. Appl Environ Microbiol 80(24):7611–7619

    Article  PubMed  PubMed Central  Google Scholar 

  • Shen LD, Liu S, ZhuQ LXY, Cai C, Cheng DQ, Lou LP, XuXY ZP, Hu BL (2014b) Distribution and diversity of nitrite-dependent anaerobic methane-oxidising bacteria in the sediments of the Qiantang River. Microb Ecol 67(2):341–349

    Article  CAS  PubMed  Google Scholar 

  • Shen LD, Zhu Q, Liu S, Du P, Zeng JN, Cheng DQ, Xu XY, Zheng P, Hu BL (2014c) Molecular evidence for nitrite-dependent anaerobic methane-oxidising bacteria in the Jiaojiang Estuary of the East Sea (China). Appl Microbiol Biotechnol 98(11):5029–5038

    Article  CAS  Google Scholar 

  • Shen LD, Huang Q, He ZF, Lian X, Liu S, He YF, Lou LP, Xu XY, Zheng P, Hu BL (2015a) Vertical distribution of nitrite-dependent anaerobic methane-oxidising bacteria in natural freshwater wetland soils. Appl Microbiol Biotechnol 99(1):349–357

    Article  CAS  PubMed  Google Scholar 

  • Shen LD, Liu S, He ZF, Lian X, Huang Q, He YF, Lou LP, Xu XY, Zheng P, Hu BL (2015b) Depth-specific distribution and importance of nitrite-dependent anaerobic ammonium and methane-oxidising bacteria in an urban wetland. Soil Biol Biochem 83:43–51

    Article  CAS  Google Scholar 

  • Shen LD, Hu BL, Liu S, Chai XP, He ZF, Ren HX, Liu Y, Geng S, Wang W, Tang JL, Wang YM, Lou LP, Xu XY, Zheng P (2016) Anaerobic methane oxidation coupled to nitrite reduction can be a potential methane sink in coastal environments. Appl Microbiol Biotechnol 100(16):7171–7180

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • ter Braak CJF, Šmilauer P (2002) CANOCO reference manual and CanoDraw for Windows user’s guide: software for canonical community ordination (version 4.5). Microcomputer Power, Ithaca

    Google Scholar 

  • Wang Y, Zhu GB, Harhangi HR, Zhu BL, Jetten MSM, Yin CQ, Op den Camp HJM (2012) Co-occurrence and distribution of nitrite-dependent anaerobic ammonium and methane oxidizing bacteria in a paddy soil. FEMS Microbiol Lett 336(2):79–88

    Article  CAS  PubMed  Google Scholar 

  • Welte CU, Rasigraf O, Vaksmaa A, Versantvoort W, Arshad A, Op den Camp HJ, Jetten MS, Lüke C, Reimann J (2016) Nitrate- and nitrite-dependent anaerobic oxidation of methane. Environ Microbiol Rep 8(6):941

    Article  CAS  PubMed  Google Scholar 

  • Xu X, Zou X, Cao L, Zhamangulova N, Zhao Y, Tang D, Liu D (2014) Seasonal and spatial dynamics of greenhouse gas emissions under various vegetation covers in a coastal saline wetland in southeast China. Ecol Eng 73:469–477

    Article  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  PubMed  Google Scholar 

  • Zhu BL, van Dijk G, Fritz C, Smolders AJP, Pol A, Jetten MSM, 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  PubMed  PubMed Central  Google Scholar 

  • Zhu GB, Zhou LL, Wang Y, Wang SY, Guo JH, Long XE, Sun XB, Jiang B, Hou QY, Jetten MSM, Yin CQ (2015) Biogeographical distribution of denitrifying anaerobic methane oxidizing bacteria in Chinese wetland ecosystems. Environ Microbiol Rep 7:128–138

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was funded by the National Natural Science Foundation of China (No. 41641031 and No. 51478415).

Author information

Authors and Affiliations

  1. Department of Environmental Engineering, Zhejiang University, Hangzhou, 310058, China

    Jiaqi Wang, Lidong Shen, Zhanfei He, Jiajie Hu, Zhaoyang Cai, Ping Zheng & Baolan Hu

  2. Zhejiang Province Key Laboratory for Water Pollution Control and Environmental Safety, Hangzhou, China

    Baolan Hu

Authors
  1. Jiaqi Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lidong Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhanfei He
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jiajie Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhaoyang Cai
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ping Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Baolan Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Baolan Hu.

Ethics declarations

This article does not contain any experiments involving human participants or animals performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

ESM 1

(PDF 732 kb).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, J., Shen, L., He, Z. et al. Spatial and temporal distribution of nitrite-dependent anaerobic methane-oxidizing bacteria in an intertidal zone of the East China Sea. Appl Microbiol Biotechnol 101, 8007–8014 (2017). https://doi.org/10.1007/s00253-017-8521-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-017-8521-0

Keywords

Search

Navigation