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. 1997 Feb;63(2):596–601. doi: 10.1128/aem.63.2.596-601.1997

Contrasting Bacterial Strategies To Coexist with a Flagellate Predator in an Experimental Microbial Assemblage

J Pernthaler, T Posch, K Simek, J Vrba, R Amann, R Psenner
PMCID: PMC1389522  PMID: 16535516

Abstract

We studied predator-induced changes within a slowly growing mixed microbial assemblage that was sustained by algal exudates in a continuous cultivation system. In situ hybridization with fluorescent monolabeled oligonucleotide probes was used for a tentative community analysis. This method also allowed us to quantify the proportions of predators with ingested bacteria of different taxonomic groups. In addition, we determined grazing rates on bacteria with fluorescently labelled prey. Bacteria belonging to the alpha and beta subdivisions of the phylum Proteobacteria ((alpha)- and (beta)-Proteobacteria, respectively) showed very different responses to the addition of a bacterivorous flagellate, Bodo saltans. Within one day, filamentous protist-inedible bacteria developed; these belonged to the (beta)-Proteobacteria and constituted between 8.7 and 34% of bacteria from this subgroup. Total abundance of (beta)-Proteobacteria decreased from 3.05 x 10(sup6) to 0.23 x 10(sup6) cells ml(sup-1), and estimated cell division rates were low. Other morphologically inconspicuous protist-edible bacteria belonging to the (alpha)-Proteobacteria were found to respond to predation by an increase in growth rate. Although these bacteria were heavily grazed upon, as on average >85% of flagellate cells had ingested (alpha)-Proteobacteria, they numerically dominated after the addition of B. saltans (mean, 1.35 x 10(sup6) cells ml(sup-1)). It was thus mainly those fast-dividing strains of (alpha)-Proteobacteria that supported the growth of the flagellate population. We conclude that bacteria in mixed assemblages can adopt at least two distinct strategies as a reaction to intense flagellate predation: to outgrow predation pressure or to develop inedible, inactive filaments. Since these strategies occurred within 24 h after the addition of the flagellate, we hypothesize that chemical stimuli released by the predator may have triggered bacterial responses.

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Selected References

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  1. Alfreider A., Pernthaler J., Amann R., Sattler B., Glockner F., Wille A., Psenner R. Community analysis of the bacterial assemblages in the winter cover and pelagic layers of a high mountain lake by in situ hybridization. Appl Environ Microbiol. 1996 Jun;62(6):2138–2144. doi: 10.1128/aem.62.6.2138-2144.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Amann R. I., Krumholz L., Stahl D. A. Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J Bacteriol. 1990 Feb;172(2):762–770. doi: 10.1128/jb.172.2.762-770.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Amann R. I., Ludwig W., Schleifer K. H. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev. 1995 Mar;59(1):143–169. doi: 10.1128/mr.59.1.143-169.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Amann R., Springer N., Ludwig W., Görtz H. D., Schleifer K. H. Identification in situ and phylogeny of uncultured bacterial endosymbionts. Nature. 1991 May 9;351(6322):161–164. doi: 10.1038/351161a0. [DOI] [PubMed] [Google Scholar]
  5. Bloem J., Starink M., Bär-Gilissen M. J., Cappenberg T. E. Protozoan grazing, bacterial activity, and mineralization in two-stage continuous cultures. Appl Environ Microbiol. 1988 Dec;54(12):3113–3121. doi: 10.1128/aem.54.12.3113-3121.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Fuhrman J. A., Azam F. Bacterioplankton secondary production estimates for coastal waters of british columbia, antarctica, and california. Appl Environ Microbiol. 1980 Jun;39(6):1085–1095. doi: 10.1128/aem.39.6.1085-1095.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Giovannoni S. J., Britschgi T. B., Moyer C. L., Field K. G. Genetic diversity in Sargasso Sea bacterioplankton. Nature. 1990 May 3;345(6270):60–63. doi: 10.1038/345060a0. [DOI] [PubMed] [Google Scholar]
  8. González J. M., Iriberri J., Egea L., Barcina I. Differential rates of digestion of bacteria by freshwater and marine phagotrophic protozoa. Appl Environ Microbiol. 1990 Jun;56(6):1851–1857. doi: 10.1128/aem.56.6.1851-1857.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gurijala K. R., Alexander M. Effect of growth rate and hydrophobicity on bacteria surviving protozoan grazing. Appl Environ Microbiol. 1990 Jun;56(6):1631–1635. doi: 10.1128/aem.56.6.1631-1635.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kuhlmann H. W., Heckmann K. Interspecific morphogens regulating prey-predator relationships in protozoa. Science. 1985 Mar 15;227(4692):1347–1349. doi: 10.1126/science.227.4692.1347. [DOI] [PubMed] [Google Scholar]
  11. Sherr B. F., Sherr E. B., McDaniel J. Effect of protistan grazing on the frequency of dividing cells in bacterioplankton assemblages. Appl Environ Microbiol. 1992 Aug;58(8):2381–2385. doi: 10.1128/aem.58.8.2381-2385.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Sherr B. F., Sherr E. B., Rassoulzadegan F. Rates of digestion of bacteria by marine phagotrophic protozoa: temperature dependence. Appl Environ Microbiol. 1988 May;54(5):1091–1095. doi: 10.1128/aem.54.5.1091-1095.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Simek K., Chrzanowski T. H. Direct and indirect evidence of size-selective grazing on pelagic bacteria by freshwater nanoflagellates. Appl Environ Microbiol. 1992 Nov;58(11):3715–3720. doi: 10.1128/aem.58.11.3715-3720.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Simek K., Vrba J., Pernthaler J., Posch T., Hartman P., Nedoma J., Psenner R. Morphological and compositional shifts in an experimental bacterial community influenced by protists with contrasting feeding modes. Appl Environ Microbiol. 1997 Feb;63(2):587–595. doi: 10.1128/aem.63.2.587-595.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Verhagen F. J., Laanbroek H. J. Effects of Grazing by Flagellates on Competition for Ammonium between Nitrifying and Heterotrophic Bacteria in Chemostats. Appl Environ Microbiol. 1992 Jun;58(6):1962–1969. doi: 10.1128/aem.58.6.1962-1969.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Vrba J, Simek K, Pernthaler J, Psenner R. Evaluation of Extracellular, High-affinity beta-N-acetylglucosaminidase Measurements from Freshwater Lakes: An Enzyme Assay to Estimate Protistan Grazing on Bacteria and Picocyanobacteria. Microb Ecol. 1996 Jul;32(1):81–99. [PubMed] [Google Scholar]

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