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International Journal of Environmental Research

, Volume 12, Issue 5, pp 749–753 | Cite as

Effects of Copper and PQQ on the Denitrification Activities of Microorganisms Facilitating Nitrite- and Nitrate-Dependent DAMO Reaction

  • Masashi Hatamoto
  • Sho Nemoto
  • Takashi Yamaguchi
Technical note

Abstract

The growth rate of microorganisms that facilitate the denitrifying anaerobic methane oxidation (DAMO) reaction is slow; thus, establishment of appropriate cultivation conditions for these microorganisms is necessary. In this study, the effect of copper (Cu) and pyrroloquinoline quinone (PQQ) concentrations on the nitrite- and nitrate-dependent DAMO activities of these microorganisms were evaluated using an upflow-type continuous cultivation system. The study confirmed that 6 µM Cu and 2 nM PQQ had a positive effect on nitrite-dependent DAMO, but had little effect on nitrate-dependent DAMO. Conventional basal medium does not contain PQQ; therefore, supplementation of basal medium with PQQ could be an effective method for the cultivation of bacteria that facilitate nitrite-dependent DAMO.

Keywords

M. oxyfera M. nitroreducens NC10 Anaerobic methanotroph 

Notes

Acknowledgements

This research was financially supported by JSPS KAKENHI Grant Numbers 25701010, 15K12225, and 16H02975.

Supplementary material

41742_2018_118_MOESM1_ESM.docx (368 kb)
Supplementary material 1 (DOCX 367 kb)

References

  1. Ameyama M, Shinagawa E, Matsushita K, Adachi O (1985) Growth stimulating activity for microorganisms in naturally occurring substances and partial characterization of the substance for the activity as pyrroloquinoline quinone. Agric Biol Chem 49:699–709Google Scholar
  2. Anthony C (2004) The quinoprotein dehydrogenases for methanol and glucose. Arch Biochem Biophys 428:2–9CrossRefGoogle Scholar
  3. Anthony C, Ghosh M (1998) The structure and function of the PQQ-containing quinoprotein dehydrogenases. Prog Biophys Mol Biol 69:1–21CrossRefGoogle Scholar
  4. 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 75:3656–3662CrossRefGoogle Scholar
  5. Ettwig KF, Butler MK, Le Paslier D, Pelletier E, Mangenot S, Kuypers MMM, Schreiber F, Dutilh BE, Zedelius J, De Beer D, Gloerich J, Wessels HJCT, Van Alen T, Luesken F, Wu ML, Van De Pas-Schoonen KT, Op Den Camp HJM, Janssen-Megens EM, Francoijs KJ, Stunnenberg H, Weissenbach J, Jetten MSM, Strous M (2010) Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464:543–548CrossRefGoogle Scholar
  6. Forster P, Ramaswamy V, Artaxo P, Berntsen T, Betts R, Fahey DW, Haywood J, Lean J, Lowe DC, Myhre G, Nganga J, Prinn R, Raga G, Schulz M, Van Dorland R (2007) Changes in atmospheric constituents and in radiative forcing. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, New YorkGoogle Scholar
  7. Fu L, Ding J, Lu YZ, Ding ZW, Zeng RJ (2017) Nitrogen source effects on the denitrifying anaerobic methane oxidation culture and anaerobic ammonium oxidation bacteria enrichment process. Appl Microbiol Biotechnol 101:3895–3906CrossRefGoogle Scholar
  8. Glass JB, Orphan VJ (2012) Trace metal requirements for microbial enzymes involved in the production and consumption of methane and nitrous oxide. Front Microbiol 3:61Google Scholar
  9. Haroon MF, Hu S, Shi Y, Imelfort M, Keller J, Hugenholtz P, Yuan Z, Tyson GW (2013) Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature 500:567–570CrossRefGoogle Scholar
  10. Hatamoto M, Kimura M, Sato T, Koizumi M, Takahashi M, Kawakami S, Araki N, Yamaguchi T (2014) Enrichment of denitrifying methane-oxidizing microorganisms using up-flow continuous reactors and batch cultures. PLoS One 9:e115823.  https://doi.org/10.1371/journal.pone.0115823 CrossRefGoogle Scholar
  11. Hatamoto M, Sato T, Nemoto S, Yamaguchi T (2017) Cultivation of denitrifying anaerobic methane-oxidizing microorganisms in a continuous-flow sponge bioreactor. Appl Microbiol Biotechnol 101:5881–5888CrossRefGoogle Scholar
  12. He Z, Cai C, Geng S, Lou L, Xu X, Zheng P, Hu B (2013) Mdodeling a nitrite-dependent anaerobic methane oxidation process: parameters identification and model evaluation. Bioresour Technol 147:315–320CrossRefGoogle Scholar
  13. He Z, Geng S, Pan Y, Cai C, Wang J, Wang L, Liu S, Zheng P, Xu X, Hu B (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 85:235–243CrossRefGoogle Scholar
  14. He Z, Geng S, Shen L, Lou L, Zheng P, Xu X, Hu B (2015b) The short- and long-term effects of environmental conditions on anaerobic methane oxidation coupled to nitrite reduction. Water Res 68:554–562CrossRefGoogle Scholar
  15. He Z, Wang J, Zhang X, Cai C, Geng S, Zheng P, Xu X, Hu B (2015c) Nitrogen removal from wastewater by anaerobic methane-driven denitrification in a lab-scale reactor: heterotrophic denitrifiers associated with denitrifying methanotrophs. Appl Microbiol Biotechnol 99:10853–10860CrossRefGoogle Scholar
  16. He Z, Geng S, Wang L, Cai C, Wang J, Liu J, Zheng P, Xu X, Hu B (2016) Improvement of mineral nutrient concentrations and pH control for the nitrite-dependent anaerobic methane oxidation process. Sep Purif Technol 162:148–153CrossRefGoogle Scholar
  17. Hu S, Zeng RJ, Burow LC, Lant P, Keller J, Yuan Z (2009) Enrichment of denitrifying anaerobic methane oxidizing microorganisms. Environ Microbiol Rep 1:377–384CrossRefGoogle Scholar
  18. Kampman C, Temmink H, Hendrickx TLG, Zeeman G, Buisman CJN (2014) Enrichment of denitrifying methanotrophic bacteria from municipal wastewater sludge in a membrane bioreactor at 20 °C. J Hazard Mater 274:428–435CrossRefGoogle Scholar
  19. 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 92:845–854CrossRefGoogle Scholar
  20. Luesken FA, Wu ML, Op den Camp HJM, Keltjens JT, Stunnenberg H, Francoijs KJ, Strous M, Jetten MSM (2012) Effect of oxygen on the anaerobic methanotroph ‘Candidatus Methylomirabilis oxyfera’: kinetic and transcriptional analysis. Environ Microbiol 14:1024–1034CrossRefGoogle Scholar
  21. Raghoebarsing AA, Pol A, van de Pas-Schoonen KT, Smolders AJP, Ettwig KF, Rijpstra WIC, Schouten S, Damste JSS, Op den Camp HJM, Jetten MSM, Strous M (2006) A microbial consortium couples anaerobic methane oxidation to denitrification. Nature 440:918–921CrossRefGoogle Scholar
  22. Wu ML, Ettwig KF, Jetten MSM, Strous M, Keltjens JT, Van Niftrik L (2011) A new intra-aerobic metabolism in the nitrite-dependent anaerobic methane-oxidizing bacterium Candidatus ‘Methylomirabilis oxyfera’. Biochem Soc Trans 39:243–248CrossRefGoogle Scholar
  23. Wu ML, Wessels HJCT, Pol A, Op den Camp HJM, Jetten MSM, van Niftrik L, Keltjens JT (2015) XoxF-type methanol dehydrogenase from the anaerobic methanotroph “Candidatus Methylomirabilis oxyfera”. Appl Environ Microbiol 81:1442–1451CrossRefGoogle Scholar
  24. Zhu B, van Dijk G, Fritz C, Smolders AJP, Pol A, Jetten MSM, Ettwiga KF (2012) Anaerobic oxidization of methane in a minerotrophic peatland: enrichment of nitrite-dependent methane-oxidizing bacteria. Appl Environ Microbiol 78:8657–8665CrossRefGoogle Scholar

Copyright information

© University of Tehran 2018

Authors and Affiliations

  1. 1.Department of Civil and Environmental Systems EngineeringNagaoka University of TechnologyNagaokaJapan
  2. 2.Top Runner Incubation Center for Academia-Industry FusionNagaoka University of TechnologyNagaokaJapan
  3. 3.Department of Science of Technology InnovationNagaoka University of TechnologyNagaokaJapan

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