Skip to main content
SpringerLink
Log in

Ciliate grazing on Nitrosomonas europaea and Nitrospira moscoviensis: Is selectivity a factor for the nitrogen cycle in natural aquatic systems?

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Ciliated protists are important predators of bacteria in many aquatic habitats, including sediments. Since, many biochemical transformations within the nitrogen cycle are performed by bacteria, ciliates could have an indirect impact on the nitrogen cycle through selective grazing on nitrogen-transforming bacteria. As a case study, we examined ciliate grazing on nitrifying bacteria of the genera Nitrosomonas and Nitrospira. All experiments were designed as in vitro-experiments with cultures of different bacteria and ciliate species. The nitrifying bacteria used in our experiments were Nitrosomonas europaea [Winogradsky 1892] and Nitrospira moscoviensis [Ehrich 2001]. The ciliates comprised of four species that are known as efficient bacterivores and common members of the protist community in aquatic systems: Paramecium aurelia [Müller 1773], Euplotes octocarinatus [Carter 1972], Tetrahymena pyriformis [Ehrenberg 1830] and Cyclidium glaucoma [Müller 1786]. Our experimental approach, using a combination of DAPI and FISH staining, was successful in allowing the observation of ingestion of specific bacteria and their detection within ciliate food vacuoles. However, the ciliates in this study showed no significant selective grazing. No food preferences for a any bacterial taxon or any size class or morphotype were detected. Correlation with time between ciliate abundance and bacterial abundance or biovolume, using log transformed growth rates of ciliates and bacteria, showed no significant results. On the bacterial side, neither an active defence mechanism of the nitrifying bacteria against ciliate grazing, such as changes in morphology, nor competition for resources were observed. These results suggest that in our in vitro-experiments grazing by ciliates has no influence on abundance and growth of nitrifying bacteria and nitrification.

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

Similar content being viewed by others

References

  • Alphei, J., M. Bonkowski & S. Scheuch, 1996. Protozoa, Nematoda and Lumbricidae in the rhizosphere of Hordelymus europaeus (Poaceae): faunal interactions, response of microorganisms and effects on plant growth. Oecologia 106: 111–126.

    Google Scholar 

  • Altmann, D., P. Stief, R. Amann & D. De Beer, 2004. Distribution and activity of nitrifying bacteria in natural stream sediment versus laboratory sediment microcosms. Aquatic Microbial Ecology 36: 73–81.

    Article  Google Scholar 

  • Altmann, D., P. Stief, R. Amann, D. De Beer & A. Schramm, 2003. In situ distribution and activity of nitrifying bacteria in freshwater sediment. Environmental Microbiology 5: 798–803.

    Article  PubMed  CAS  Google Scholar 

  • Berninger, U.-G., B. J. Finlay & P. Kuuppo-Leinikki, 1991. Protozoan control of bacterial abundances in freshwater. Limnology and Oceanography 36: 139–147.

    Article  Google Scholar 

  • Cébron, A., T. Berthe & J. Garnier, 2003. Nitrification and nitrifying bacteria in the lower Seine river and estuary (France). Applied and Environmental Microbiology 69: 7091–7100.

    Article  PubMed  CAS  Google Scholar 

  • Chesson, J., 1983. The estimation and analysis of preference and its relationship to foraging models. Journal of Ecology 64: 1297–1304.

    Article  Google Scholar 

  • Cleven, E.-J., 2004. Seasonal and spatial distribution of ciliates in the sandy hyporheic zone of a lowland stream. European Journal of Protistology 40: 71–84.

    Article  Google Scholar 

  • Daims, H., J. L. Nielsen, P. H. Nielsen, K. H. Schleifer & M. Wagner, 2001. In situ characterization of Nitrospira-like nitrite-oxidizing bacteria active in wastewater treatment plants. Applied and Environmental Microbiology 67: 5273–5284.

    Article  PubMed  CAS  Google Scholar 

  • Diederichs, S., C. Beardsley & E.-J. Cleven, 2003. Detection of ingested bacteria in benthic ciliates using fluorescence in situ hybridization. Systematic and Applied Microbiology 26: 624–630.

    Article  PubMed  CAS  Google Scholar 

  • Ehrich, S., D. Behrens, E. Lebedeva, W. Ludwig & E. Bock, 1995. A new obligately chemolithoautotrophic, nitrite-oxidizing bacterium, Nitrospira moscoviensis sp. nov. and its phylogenetic relationship. Archiv für Mikrobiologie 164: 16–23.

    CAS  Google Scholar 

  • Eisenmann, H., H. Harms, R. Meckenstock, E. I. Meyer & A. J. B. Zehnder, 1998. Grazing of a Tetrahymena sp. on adhered bacteria in percolated columns monitored by in situ hybridization with fluorescent oligonucleotide probes. Applied and Environmental Microbiology 64: 1264–1269.

    PubMed  CAS  Google Scholar 

  • Fenchel, T., 1980. Suspension feeding in ciliated protozoa: feeding rates and their ecological significance. Microbial Ecology 6: 13–25.

    Article  Google Scholar 

  • Fenchel, T., 1986. Protozoan filter feeding. European Journal of Protistology 1: 65–113.

    Google Scholar 

  • Hausmann, K., N. Hülsmann & R. Radek, 2001. Ingestion, Digestion, and Defecation. In Protistology. Schweizerbart’sche Verlags Verlagsbuchhandlung, Germany.

    Google Scholar 

  • Hendricks, S. P., 1996. Bacterial biomass, activity, and production within the hyporheic zone of a north-temperate stream. Archiv für Hydrobiologie 136: 467–487.

    Google Scholar 

  • Jezbera, J., K. Horňák & K. Šimek, 2004. Food selection by bacterivorous protists: insight from the analysis of the food vacuole content by means of fluorescence in situ hybridization. FEMS Microbiology Ecology 52: 351–363.

    Article  CAS  Google Scholar 

  • Jürgens, K. & W. R. DeMott, 1995. Behavioral flexibility in prey selection by bacterivorous nanoflagellates. Limnology and Oceanography 40: 1503–1507.

    Article  Google Scholar 

  • Kemp, P. F., 1988. Bacterivory by benthic ciliates: significance as a carbon source and impact on sediment bacteria. Marine Ecology-Progress Sereries 49: 63–169.

    Google Scholar 

  • Köhler, W., G. Schachtel, P. Voleske, 2002. Biostatistik: Einführung in die Biometrie für Biologen und Agrarwissenschaftler. Springer Verlag, Berlin.

    Google Scholar 

  • Könneke, M., A. E. Bernhard, J. R. de la Torre, C. B. Walker, J. B. Waterbury & D. A. Stahl, 2005. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437: 543–546.

    Article  PubMed  CAS  Google Scholar 

  • Lavrentyev, P. J., W. S. Gardner & J. R. Johnson, 1997. Cascading trophic effects on aquatic nitrification: experimental evidence and potential implications. Aquatic Microbial Ecology 13: 161–175.

    Article  Google Scholar 

  • Loy, A., M. Horn & M. Wagner, 2003. probeBase: an online resource for rRNA-targeted oligonucleotide probes. Nucleic Acids Research 31: 514–516.

    Article  PubMed  CAS  Google Scholar 

  • Mallory, L. M., C. S. Yuk, I. N. Liang & M. Alexander, 1983. Alternative prey: a mechanism for elimination of bacterial species by protozoa. Applied and Environmental Microbiology 46: 1073–1079.

    PubMed  CAS  Google Scholar 

  • Miyake, A., 1981. Physiology and biochemistry of conjugation in ciliates. In Levandowsky, M. & S. H. Hunter (eds), Biochemistry and Physiology of Protozoa. Academic Press, New York: 125–198. .

    Google Scholar 

  • Mobarry, B. K., M. Wagner, V. Urbain, B. E. Rittmann & D. A. Stahl, 1996. Phylogenetic probes for analyzing abundance and spatial organization of nitrifying bacteria. Applied and Environmental Microbiology 62: 2156–2162.

    PubMed  CAS  Google Scholar 

  • Pernthaler, J., F. O. Glöckner, W. Schönhuber & R. Amann, 2001. Fluorescence in situ hybridization (FISH) with rRNA-targeted oligonucleotide probes. Methods Microbiology 30: 207–226.

    Article  CAS  Google Scholar 

  • Posch, T., J. Jezbera, J. Vrba, K. Šimek, J. Pernthaler, S. Andreatta & B. Sonntag, 2001. Size selective feeding in Cyclidium glaucoma (Ciliophora, Scuticociliatida) and its effects on bacterial community structure: a study from a continuous cultivation system. Microbial Ecology 42: 217–227.

    Article  PubMed  Google Scholar 

  • Prast, M., A. A. Bischoff, U. Waller, R. Amann & U.-G. Berninger, 2007. Impact of ciliates on nitrification and nitrifying bacteria in Baltic Sea sediments. Marine Ecology Progress Series (in press).

  • Rautenstrauss, B. W. & T. Liehr, 2002. FISH Technology. Springer Verlag, Berlin, Germany.

    Google Scholar 

  • Ribblett, S. G., M. A. Palmer & D. W. Coats, 2005. The importance of bacterivorous protists in the decomposition of stream leaf litter. Freshwater Biology 50: 516–526. .

    Article  Google Scholar 

  • Sachs, L., 2000. Angewandte Statistik: Anwendung statistischer Methoden. Springer Verlag, Berlin.

    Google Scholar 

  • Sherr, E. B. & B. F. Sherr, 2002. Significance of predation by protists in aquatic microbial food webs. Antonie van Leeuwenhoek Journal of Microbiology 81: 293–308. .

    Article  CAS  Google Scholar 

  • Šimek, K., J. Vrba & P. Hartman, 1994. Size-selective feeding by Cyclidium sp. on bacterioplankton and various sizes of cultured bacteria. FEMS Microbiology Ecology 14: 157–168.

    Article  Google Scholar 

  • Spieck, E. & E. Bock, 1998. Taxonomische, physiologische und ökologische Vielfalt nitrifizierender Bakterien. Biospektrum 4: 25–31.

    Google Scholar 

  • Stoecker, D. K., D. J. Gifford & M. Putt, 1994. Preservation of marine planktonic ciliates: losses and cell shrinkage during fixation. Marine Ecology Progress Series 110: 293–299.

    Article  Google Scholar 

  • Strauss, E. A. & E. K. Dodds, 1997. Influence of protozoa and nutrient availability on nitrification rates in subsurface sediments. Microbial Ecology 34: 155–165.

    Article  PubMed  CAS  Google Scholar 

  • Wilks, S. A. & M. A. Sleigh, 1998. Grazing Rates in Euplotes mutabilis: relationship between particle size and concentration. Microbial Ecology 36: 165–174.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank M.W. Hahn, Institute for Limnology, Mondsee, Austria, for support in FISH-technology and supply of bacterial cultures. Further thanks are due to H.-D. Görtz, University of Stuttgart, Germany, for the supply of ciliate cultures and E. Spieck, Biocenter Klein Flottbek, Hamburg, Germany, for providing bacterial cultures. We particularly thank S.A. Wickham for helpful comments on statistical analyses, A. Pitt for help with the laboratory experiments and S. Agatha for constructive suggestions. Two anonymous reviewers provided valuable comments on an earlier version of this manuscript.

Author information

Authors and Affiliations

  1. Department of Organismic Biology, University of Salzburg, Hellbrunnerstrasse 34, 5020, Salzburg, Austria

    Elke Neubacher, Mario Prast & Ulrike-Gabriele Berninger

  2. Department of Limnology, University of Münster, Munster, Germany

    Ernst-Josef Cleven

Authors
  1. Elke Neubacher
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mario Prast
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ernst-Josef Cleven
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ulrike-Gabriele Berninger
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Elke Neubacher.

Additional information

Handling editor: L. Naselli-Flores

Rights and permissions

Reprints and permissions

About this article

Cite this article

Neubacher, E., Prast, M., Cleven, EJ. et al. Ciliate grazing on Nitrosomonas europaea and Nitrospira moscoviensis: Is selectivity a factor for the nitrogen cycle in natural aquatic systems?. Hydrobiologia 596, 241–250 (2008). https://doi.org/10.1007/s10750-007-9100-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-007-9100-7

Keywords

Search

Navigation