Skip to main content

Advertisement

Log in

Role of Productivity and Protozoan Abundance for the Occurrence of Predation-resistant Bacteria in Aquatic Systems

  • Original Article
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Top–down control of lower trophic levels, e.g., bacteria, has been suggested to increase along aquatic productivity gradients. The response by the bacterial community may be to become more predation resistant in highly productive environments. To test this hypothesis, samples were taken from 20 aquatic systems along a productivity gradient (dissolved organic carbon from 7 to 71 mg/L), during late summer. The results showed that the biomass of bacteria, phytoplankton, and ciliates increased along the gradient (r 2 = 0.532, 0.426, and 0.758, P < 0.01, respectively). However, the organisms did not increase equally, and the ratio of protozoan to bacterial biomass showed a 100-fold increase along the gradient. Ciliates dominated the protozoan biomass in the more nutrient-rich waters. The edibility of colony-forming bacteria was tested using a ciliate predator, Tetrahymena pyriformis. Bacterial edibility was found to decrease with increases in nutrient richness and ciliate biomass in the aquatic systems (r 2 = 0.358, P < 0.01; r 2 = 0.242, P < 0.05, respectively). Quantile regression analysis indicated that the selection pressures on edible bacteria were increasing along the productivity gradient. Thus, inedible forms of bacteria were selected for in the transition from oligotrophic to eutrophic conditions. Isolated bacteria were distributed among the α-, β-, and γ- Proteobacteria and the Actinobacteria and Firmicutes taxa. We conclude that bacterial predation resistance increases in nutrient-rich waters with high protozoan predation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  1. Abd H, Johansson T, Golovliov I, Sandstrom G, Forsman M (2003) Survival and growth of Francisella tularensis in Acanthamoeba castellanii. Appl Environ Microbiol 69:600–606

    Article  PubMed  CAS  Google Scholar 

  2. Auer B, Elzer U, Arndt H (2004) Comparison of pelagic food webs in lakes along a trophicgradient and with seasonal aspects: influence of resource and predation. J Plankton Res 26:697–709

    Article  Google Scholar 

  3. Bandyopadhyay P, Xiao HF, Coleman HA, Price-Whelan A, Steinman HM (2004) Icm/dot-independent entry of Legionella pneumophila into amoeba and macrophage hosts. Infect Immun 72:4541–4551

    Article  PubMed  CAS  Google Scholar 

  4. Berglund J, Samuelsson K, Kull T, Muren U, Andersson A (2005) Relative strength of resource and predation limitation of heterotrophic nanoflagellates in a low-productive sea area. J Plankton Res 27:923–935

    Article  Google Scholar 

  5. Blackburn N, Hagstrom A, Wikner J, Cuadros-Hansson R, Bjornsen PK (1998) Rapid determination of bacterial abundance, biovolume, morphology, and growth by neural network-based image analysis. Appl Environ Microbiol 64:3246–3255

    PubMed  CAS  Google Scholar 

  6. Brooks T, Osicki RA, Springthorpe VS, Sattar SA, Filion L, Abrial D, Riffard S (2004) Detection and identification of Legionella species from groundwaters. J Toxicol Environ Health A Curr Issue 67:1845–1859

    Article  CAS  Google Scholar 

  7. Cade BS, Noon BR (2003) A gentle introduction to quantile regression for ecologists. Front Ecol Environ 1:412–420

    Google Scholar 

  8. Chen J, de Felipe KS, Clarke M, Lu H, Anderson OR, Segal G, Shuman HA (2004) Legionella . effectors that promote nonlytic release from protozoa. Science 303:1358–1361

    Article  PubMed  CAS  Google Scholar 

  9. Cole JJ, Findlay S, Pace ML (1988) Bacterial production in fresh and saltwater ecosystems-a cross-system overwiew. Mar Ecol Prog Ser 43:1–10

    Article  Google Scholar 

  10. Cole JR, Chai B, Marsh TL, Farris RJ, Wang Q, Kulam SA, Chandra S, McGarrell DM, Schmidt TM, Garrity GM et al (2003) The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res 31:442–443

    Article  PubMed  CAS  Google Scholar 

  11. Dorsch M, Stackebrandt E (1992) Some modifications in the procedure of direct sequencing of PCR amplified 16S rDNA. J Microbiol Methods 16:271–279

    Article  Google Scholar 

  12. Fenchel T (1987) Ecology of Protozoa: the biology of free-living phagotrophic protists. Brock/Springer series in contemporary bioscience. Science Tech, Wisconsin

    Google Scholar 

  13. Fokin SI (2004) Bacterial endocytobionts of ciliophora and their interactions with the host cell. Int Rev Cytol 236:181–249

    Article  PubMed  Google Scholar 

  14. Gao LY, Harb OS, Abu Kwaik Y (1997) Utilization of similar mechanisms by Legionella pneumophila to parasitize two evolutionarily distant host cells, mammalian macrophages and protozoa. Infect Immun 65:4738–4746

    PubMed  CAS  Google Scholar 

  15. Gasol JM, Pedros-Alio C, Vaque D (2002) Regulation of bacterial assemblages in oligotrophic plankton systems: results from experimental and empirical approaches. Antonie Van Leeuwenhoek 81:435–452

    Article  PubMed  CAS  Google Scholar 

  16. Grasshof KM, Ehrhardt M, Kremling K (1983) Methods of seawater analysis. Verlag Chemie, Weinheim

    Google Scholar 

  17. Greub G, Raoult D (2004) Microorganisms resistant to free-living amoebae. Clin Microbiol Rev 17:413–433

    Article  PubMed  Google Scholar 

  18. Hahn MW, Moore ER, Hofle MG (1999) Bacterial filament formation, a defense mechanism against flagellate grazing, is growth rate controlled in bacteria of different phyla. Appl Environ Microbiol 65:25–35

    PubMed  CAS  Google Scholar 

  19. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  20. Hansen AM (2000) Response of ciliates and Cryptomonas to the spring cohort of a cyclopoid copepod in a shallow hypereutrophic lake. J Plankton Res 22:185–203

    Article  Google Scholar 

  21. Harb OS, Gao LY, Abu Kwaik Y (2000) From protozoa to mammalian cells: a new paradigm in the life cycle of intracellular bacterial pathogens. Environ Microbiol 2:251–265

    Article  PubMed  CAS  Google Scholar 

  22. Hobbie JE, Daley RJ, Jasper S (1977) Use of nuclepore filters for counting bacteria by fluorescence microscopy. Appl Environ Microbiol 33:1225–1228

    PubMed  CAS  Google Scholar 

  23. Horner-Devine MC, Leibold MA, Smith VH, Bohannan BJM (2003) Bacterial diversity patterns along a gradient of primary productivity. Ecol Lett 6:613–622

    Article  Google Scholar 

  24. Jannasch HW, Jones GE (1959) Bacterial populations in sea water as determined by different methods of enumeration. Limnol Oceanogr 4:128–139

    Google Scholar 

  25. Jezbera J, Hornak K, Simek K (2005) Food selection by bacterivorous protists: insight from the analysis of the food vacuole content by means of fluorescence in situ hybridization. FEMS Microbiol Ecol 52:351–363

    Article  PubMed  CAS  Google Scholar 

  26. Jurgens K, Gude H (1994) The potential importance of grazing-resistant bacteria in planktonic systems. Mar Ecol Prog Ser 112:169–188

    Article  Google Scholar 

  27. Jurgens K, Matz C (2002) Predation as a shaping force for the phenotypic and genotypic composition of planktonic bacteria. Antonie Van Leeuwenhoek 81:413–434

    Article  PubMed  CAS  Google Scholar 

  28. Jurgens K, Skibbe O, Jeppesen E (1999) Impact of metazooplankton on the composition and population dynamics of planktonic ciliates in a shallow, hypertrophic lake. Aquat Microb Ecol 17:61–75

    Article  Google Scholar 

  29. Jurgens K, Pernthaler J, Schalla S, Amann R (1999) Morphological and compositional changes in a planktonic bacterial community in response to enhanced protozoan grazing. Appl Environ Microbiol 65:1241–1250

    PubMed  CAS  Google Scholar 

  30. Kisand V, Zingel P (2000) Dominance of ciliate grazing on bacteria during spring in a shallow eutrophic lake. Aquat Microb Ecol 22:135–142

    Article  Google Scholar 

  31. Klapper H (1991) Control of Eutrophication in inland waters. Ellis Horwood series in water and wastewater technology. Ellis Horwood, England

    Google Scholar 

  32. Koenker R (2005) Appendix A. In: Chesher A, Jackson M (eds) Quantile regression (Econometric Society Monographs). Cambridge University Press, Cambridge, pp 293–308

    Google Scholar 

  33. Kogure K, Simidu U, Taga N (1979) A tentative direct microscopic method for counting living marine bacteria. Can J Microbiol 25:415–420

    Article  PubMed  CAS  Google Scholar 

  34. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  35. Massana R, Murray AE, Preston CM, DeLong EF (1997) Vertical distribution and phylogenetic characterization of marine planktonic Archaea in the Santa Barbara Channel. Appl Environ Microbiol 63:50–56

    PubMed  CAS  Google Scholar 

  36. Matz C, Kjelleberg S (2005) Off the hook-how bacteria survive protozoan grazing. Trends Microbiol 13:302–307

    Article  PubMed  CAS  Google Scholar 

  37. Matz C, Jurgens K (2003) Interaction of nutrient limitation and protozoan grazing determines the phenotypic structure of a bacterial community. Microb Ecol 45:384–398

    Article  PubMed  CAS  Google Scholar 

  38. Muren U, Berglund J, Samuelsson K, Andersson A (2005) Potential effects of elevated sea-water temperature on pelagic food webs. Hydrobiologia 545:153–166

    Article  Google Scholar 

  39. Muyzer G, Brinkhoff T, Nubel U, Santegoeds C, Schäfer H, Wawer C (1997) Denaturing gradient gel electrophoresis (DGGE) in microbial ecology. In: Kowalchuk GA (ed) Molecular microbial ecology manual. Kluwer, The Netherlands, pp 1–27

    Google Scholar 

  40. Neild AL, Roy CR (2004) Immunity to vacuolar pathogens: what can we learn from Legionella? Cell Microbiol 6:1011–1018

    Article  PubMed  CAS  Google Scholar 

  41. Nixon SW (1995) Coastal marine eutrophication—a definition, social causes, and future concerns. Ophelia 41:199–219

    Google Scholar 

  42. Norland S (1993) The relationship between biomass and volume of bacteria. In: Kemp PF, Sherr BF, Sherr EB, Cole JJ (eds) Handbook of methods in aquatic microbial ecology. Lewis, London, pp 303–307

    Google Scholar 

  43. Posch T, Arndt H (1996) Uptake of sub-micrometre- and micrometre-sized detrital particles by bacterivorous and omnivorous ciliates. Aquat Microb Ecol 10:45–53

    Article  Google Scholar 

  44. R Development Core Team (2005) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN:3-900051-07-0, http://www.R-project.org

    Google Scholar 

  45. Sanders RW, Caron DA, Berninger UG (1992) Relationships between bacteria and heterotrophic nanoplancton in marine and fresh waters: an inter-ecosystem comparison. Mar Ecol Prog Ser 86:1–14

    Article  Google Scholar 

  46. Sherr EB, Caron DA, Sherr BF (1993) Staining of heterotrophic protists for visualization via epiflourecens microscopy. In: Kemp PF, Sherr BF, Sherr EB (eds) Current methods in aquatic microbial ecology. Lewis, New York, pp 213–228

    Google Scholar 

  47. Torsvik V, Daae FL, Sandaa RA, Ovreas L (1998) Novel techniques for analysing microbial diversity in natural and perturbed environments. J Biotechnol 64:53–62

    Article  PubMed  CAS  Google Scholar 

  48. Zwart G, Crump BC, Agterveld MPKV, Hagen F, Han SK (2002) Typical freshwater bacteria: an analysis of available 16S rRNA gene sequences from plankton of lakes and rivers. Aquat Microb Ecol 28:141–155

    Article  Google Scholar 

Download references

Acknowledgments

This study was supported by grants from the Centre for Environmental Research in Umeå (CMF, no. 0322248), Stiftelsen JC Kempes Minnes Stipendiefond, the Swedish Ministry of Defence (no. A4854), and the Swedish Research Council (No. 60276201). We thank Dr. Erik Lundberg for chemical analyses and Daniel Johansson and Pär Larsson for support with phylogenetic analysis. Peter Mathisen is acknowledged for laboratory work. We thank Prof. Mats Jansson and Prof. Lars Ericson for reviewing drafts of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Johanna Thelaus.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Thelaus, J., Forsman, M. & Andersson, A. Role of Productivity and Protozoan Abundance for the Occurrence of Predation-resistant Bacteria in Aquatic Systems. Microb Ecol 56, 18–28 (2008). https://doi.org/10.1007/s00248-007-9320-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-007-9320-4

Keywords

Navigation