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Phylogenetic analysis of a microbial community involved in anaerobic oxidation of ammonium nitrogen

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Abstract

The phylogenetic diversity of a microbial community involved in anaerobic oxidation of ammonium nitrogen in the DEAMOX process was studied. Analysis of clone libraries containing 16S rRNA gene inserts of Bacteria, (including Planctomycetes) and Archaea revealed the presence of nucleotide sequences of the microorganisms involved in the main reactions of the carbon, nitrogen, and sulfur cycles, including nitrifying, denitrifying, and ANAMMOX bacteria. In the bacterial clone library, 16S rRNA gene sequences of representatives of the phyla Proteobacteria, Bacteroidetes, Chloroflexi, Firmicutes, Verrucomicrobia, Lentisphaerae, Spirochaetales, and Planctomycetes, as well as of some new groups, were detected. In the archaeal clone library, nucleotide sequences of methanogens belonging to the orders Methanomicrobiales, Methanobacteriales, and Methanosarcinales were found. It is possible that both ANAMMOX bacteria and bacteria of the genus Nitrosomonas are involved in anaerobic ammonium oxidation in the DEAMOX reactor. Many sequences were similar to those from the clone libraries obtained previously from the ANAMMOX community of marine sediments. It is also probable that the DEAMOX reactions occur in natural ecosystems (in marine and freshwater sediments and the oceanic water column), thereby providing for the coupling of the nitrogen and sulfur cycles.

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References

  1. Broda, E., Two Kinds of Lithotrophs Missing in Nature, Z. Allgem. Mikrobiol., 1977, vol. 17, pp. 491–493.

    Article  CAS  Google Scholar 

  2. Jetten, M., Schmid, M., van de Pas-Schoonen, K., Sinninghe-Damsté, J., and Strous, M., Anammox Organisms: Enrichment, Cultivation, and Environmental Analysis, Methods Enzymol., 2005, vol. 397, pp. 34–57.

    Article  CAS  PubMed  Google Scholar 

  3. Anyusheva, M.G. and Kalyuzhnyi, S.V., Anaerobic Oxidation of Ammonium: Microbiological, Biochemical, and Biotechnological Aspects, Usp. Sovrem. Biol., 2007, vol. 127, no. 1, pp. 34–43.

    CAS  Google Scholar 

  4. Kuypers, M.M.M., Sliekers, A.O., Lavik, G., Schmid, M., Jørgensen, B.B., Kuenen, J.G., Sinninghe, Damst’e, J.S., Strous, M., and Jetten, M.S.M., Anaerobic Ammonium Oxidation by Anammox Bacteria in the Black Sea, Nature, 2003, vol. 422, pp. 608–611.

    Article  CAS  PubMed  Google Scholar 

  5. Schmid, M., Twachtmann, U., Klein, M., Strous, M., Juretschko, S., Jetten, M., Metzger, J.W., Schleifer, K.H., and Wagner, M., Molecular Evidence for Genus Level Diversity of Bacteria Capable of Catalyzing Anaerobic Ammonium Oxidation, Syst. Appl. Microbiol., 2000, vol. 23, pp. 93–106.

    CAS  PubMed  Google Scholar 

  6. Schmid, M., Walsh, K., Webb, R.I., Rijpstra, W.I., van de Pas-Schoonen, K., Verbruggen, M.J., Hill, T., Moffett, B., Fuerst, J., Schouten, S., Damsté, J.S., Harris, J., Shaw, P., Jetten, M., and Strous, M. Candidatus “Scalindua brodae”, sp. nov., Candidatus “Scalindua wagneri”, sp. nov., Two New Species of Anaerobic Ammonium Oxidizing Bacteria, Syst. Appl. Microbiol., 2003, vol. 26, pp. 529–538.

    Article  CAS  PubMed  Google Scholar 

  7. Kartal, B., Rattray, J., van Niftrik, L., van de Vossenberg, J., Schmid, M.C., Webb, R.I., Schouten, S., Fuerst, J.A., Sinninghe Damsté, J., Jetten, M.S.M., and Strous, M., Candidatus “Anammoxoglobus propionicus”, a New Propionate Oxidizing Species of Anaerobic Ammonium Oxidizing Bacteria, Syst. Appl. Microbiol., 2007, vol. 30, pp. 39–49.

    Article  CAS  PubMed  Google Scholar 

  8. Schmid, M.C., Maas, B., Dapena, A., van de Pas-Schoonen, K., van de Vossenberg, J., Kartal, B., van Niftrik, L., Schmidt, I., Cirpus, I., Kuenen, J.G., Wagner, M., Sinninghe Damsté, J.S., Kuypers, M., Revsbech, N.P., Mendez, R., Jetten, M.S., and Strous, M., Biomarkers for in situ Detection of Anaerobic Ammonium-Oxidizing (Anammox) Bacteria, Appl. Environ. Microbiol., 2005, vol. 71, pp. 1677–1684.

    Article  CAS  PubMed  Google Scholar 

  9. Kalyuzhnyi, S., Gladchenko, M., Mulder, A., and Versprille, B., DEAMOX-New Biological Nitrogen Removal Process Based on Anaerobic Ammonia Oxidation Coupled to Sulphide Driven Conversion of Nitrate Into Nitrite, Water Res., 2006, vol. 40, pp. 3637–3645.

    Article  CAS  PubMed  Google Scholar 

  10. Weisburg, W., Barns, S.M., Pelletier, D.A., and Lane, D.J., 16S Ribosomal DNA Amplification for Phylogenetic Study, J. Bacteriol., 1991, vol. 173, pp. 697–703.

    CAS  PubMed  Google Scholar 

  11. Kirkpatrick, J., Oakley, B., Fuchsman, C., Srinivasan, S.T., Staley, J.T., and Murray, J.W., Diversity and Distribution of Planctomycetes and Related Bacteria in the Suboxic Zone of the Black Sea, Appl. Environ. Microbiol., 2006, vol. 72, pp. 3079–3083.

    Article  CAS  PubMed  Google Scholar 

  12. Kolganova, T.V., Kuznetsov, B.B., and Tourova, T.P., Designing and Testing Oligonucleotide Primers for Amplification and Sequencing of Archaeal 16S rRNA Genes, Mikrobiologiya, 2002, vol. 71, pp. 283–285 [Microbiology (Engl. Transl.), vol. 71, no. 2, pp. 243–246].

    CAS  Google Scholar 

  13. Thompson, J.D., Higgins, D.G., and Gibson, T.J., CLUSTAL W: Improving the Sensitivity of Progressive Multiple Sequence Alignment through Sequence Weighting, Positions-Specific Gap Penalties and Weight Matrix Choice, Nucleic Acids Res., 1994, vol. 9, pp. 3251–3270.

    Google Scholar 

  14. Saitou, N. and Nei, M., The Neighbour-Joining Method: A New Method for Reconstructing Phylogenetic Trees, Mol. Biol. Evol., 1987, vol. 4, pp. 406–425.

    CAS  PubMed  Google Scholar 

  15. Van de Peer, Y. and De Wachter, R., TREECON for Windows: A Software Package for the Construction and Drawing of Evolutionary Trees for the Microsoft Windows Environment, Comput. Appl. Biosci., 1994, vol. 10, pp. 569–570.

    PubMed  Google Scholar 

  16. Juretschko, S., Loy, A., Lehner, A., and Wagner, M., The Microbial Community Composition of a Nitrifying-Denitrifying Activated Sludge from an Industrial Sewage Treatment Plant Analyzed by the Full-Cycle rRNA Approach, Syst. Appl. Microbiol., 2002, vol. 25, pp. 84–99.

    Article  CAS  PubMed  Google Scholar 

  17. Liu, B., Zhang, F., Feng, X., Liu, Y., Yan, X., Zhang, X., Wang, L., and Zhao, L., Thauera and Azoarcus as Functionally Important Genera in a Denitrifying Quinoline-Removal Bioreactors Revealed by Microbial Community Structure Comparison, FEMS Microbiol. Ecol., 2006, vol. 55, pp. 274–286.

    Article  CAS  PubMed  Google Scholar 

  18. Cytryn, E.D., van Rijn, J., Schramm, A., Gieseke, A., de Beer, D., and Minz, D., Identification of Bacteria Potentially Responsible for Oxic and Anoxic Sulfide Oxidation in Biofilters of a Recirculating Mariculture System, Appl. Environ. Microbiol., 2005, vol. 71, pp. 6134–6141.

    Article  CAS  PubMed  Google Scholar 

  19. Bock, E., Schmidt, I., Stuven, R., and Zart, D., Nitrogen Loss Caused by Denitrifying Nitrosomonas Cells Using Ammonium or Hydrogen as Electron Donors and Nitrite as Electron Acceptor, Arch. Microbiol., 1995, vol. 163, pp. 16–20.

    Article  CAS  Google Scholar 

  20. Hoshino, T., Terahara, T., Tsuneda, S., Hirata, A., and Inamori, Y., Molecular Analysis of Microbial Population Transition Associated with the Start of Denitrification in a Wastewater Treatment Process, J. Appl. Microbiol., 2005, vol. 99, pp. 1165–1175.

    Article  CAS  PubMed  Google Scholar 

  21. Sass, H., Overmann, J., Rutters, H., Babenzien, H.-D., and Cypionka, H., Desulfosporomusa polytropa gen. nov., sp. nov., a Novel Sulfate-Reducing Bacterium from Sediments of an Oligotrophic Lake, Arch. Microbiol., 2004, vol. 182, pp. 204–211.

    Article  CAS  PubMed  Google Scholar 

  22. Delbes, C., Moletta, R., and Godon, J.J., Monitoring of Activity Dynamics of an Anaerobic Digester Bacterial Community Using 16S rRNA Polymerase Chain Reaction-Single-Strand Conformation Polymorphism Analysis, J. Environ. Microbiol., 2000, vol. 2, pp. 506–515.

    Article  CAS  Google Scholar 

  23. Grotenhuis, J.T.C., Smit, M., Plugge, C.M., Yuansheng, X.U., van Lammeren, A.A.M., Stams, A.J.M., and Zehnder, A.J.B., Bacteriological Composition and Structure of Granular Sludge Adapted to Different Substrates, Appl. Environ. Microbiol., 1991, vol. 57, pp. 1942–1949.

    CAS  PubMed  Google Scholar 

  24. Neef, A., Amann, R.I., Schlesner, H., and Schleifer, K.-H., Monitoring a Widespread Bacterial Group: In situ Detection of Planctomycetes with 16S rRNA-Targeted Probes, Microbiology (UK), 1998, vol. 144, pp. 3257–3266.

    Article  CAS  Google Scholar 

  25. Freitag, T.E. and Prosser, J.I., Community Structure of Ammonia-Oxidizing Bacteria within Anoxic Marine Sediments, Appl. Environ. Microbiol., 2003, vol. 69, pp. 1359–1371.

    Article  CAS  PubMed  Google Scholar 

  26. Strous, M., Pelletier, E., Mangenot, S., Rattei, T., Lehner, A., Taylor, M.W., Horn, M., Daims, H., Bartol-Mavel, D., Wincker, P., Barbe, V., Fonknechten, N., Vallenet, D., Segurens, B., Schenowitz-Truong, C., Médigue, C., Collingro, A., Snel, B., and Dutilh, B.E., Op den Camp, H.J., van der Drift, C., Cirpus, I., van de Pas-Schoonen, K.T., Harhangi, H.R., van Niftrik, L., Schmid, M., Keltjens, J., van de Vossenberg, J., Kartal, B., Meier, H., Frishman, D., Huynen, M.A., Mewes, H.W., Weissenbach, J., Jetten, M.S., Wagner, M., and Le Paslier, D., Deciphering the Evolution and Metabolism of an Anammox Bacterium from a Community Genome, Nature, 2006, vol. 440, pp. 790–794.

    Article  PubMed  Google Scholar 

  27. Prokopenko, M.G., Hammond, D.E., Berelson, W.M., Bernhard, J.M., Stott, L., and Douglas, R., Nitrogen Isotopes, Diagenesis and Possible Chemosymbiosis between Two Lithotrophs (Thioploca and Anammox)-“Riding on a Glider”, Earth Planet Sci. Lett, 2006, vol. 242, pp. 186–204.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Chemical Enzymology, Faculty of Chemistry, Moscow State University, Moscow, 119991, Russia

    S. V. Kalyuzhnyi, M. A. Gladchenko & A. I. Trukhina

  2. Winogradsky Institute of Microbiology, Russian Academy of Sciences, pr. 60-letiya Oktyabrya 7, k. 2, Moscow, 117312, Russia

    N. M. Shestakova, T. P. Tourova & T. N. Nazina

  3. Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, ul. Vavilova 32, Moscow, 119991, Russia

    A. B. Poltaraus

Authors
  1. S. V. Kalyuzhnyi
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  2. N. M. Shestakova
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  3. T. P. Tourova
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  4. A. B. Poltaraus
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  5. M. A. Gladchenko
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  6. A. I. Trukhina
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  7. T. N. Nazina
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Correspondence to T. N. Nazina.

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Original Russian Text © S.V. Kalyuzhnyi, N.M. Shestakova, T.P. Tourova, A.B. Poltaraus, M.A. Gladchenko, A.I. Trukhina, T.N. Nazina, 2010, published in Mikrobiologiya, 2010, Vol. 79, No. 2, pp. 260–269.

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Kalyuzhnyi, S.V., Shestakova, N.M., Tourova, T.P. et al. Phylogenetic analysis of a microbial community involved in anaerobic oxidation of ammonium nitrogen. Microbiology 79, 237–246 (2010). https://doi.org/10.1134/S0026261710020165

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  • DOI: https://doi.org/10.1134/S0026261710020165

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