Detection of Ingested Bacteria in Benthic Ciliates Using Fluorescence In Situ Hybridization

Systematic and Applied Microbiology

Volumn 26, Issue 4, 2003, Pages 624-630

  Diederichs, Sandra ^a   Beardsley, Christine ^b   Cleven, Ernst Josef ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

Author keywords

16S rRNA; Bacteria ingestion; Benthic ciliates; DTAF; FLB; Fluorescence in situ hybridization; Oligonucleotide probes; Sediment; Tetrahymena pyriformis

Indexed keywords

ARTICLE; BACTERIUM DETECTION; BACTERIVORY; BENTHOS; CELL VACUOLE; CILIATE; CONTROLLED STUDY; EPIFLUORESCENCE MICROSCOPY; FLUORESCENCE IN SITU HYBRIDIZATION; INGESTION; INTERMETHOD COMPARISON; NONHUMAN; PARTICLE SIZE; PHYLOGENY; PRIORITY JOURNAL; RELIABILITY; SEDIMENT; TETRAHYMENA PYRIFORMIS;

BACTERIA (MICROORGANISMS); CILIOPHORA; PROTOZOA; TETRAHYMENA; TETRAHYMENA PYRIFORMIS;

EID: 0345293322     PISSN: 07232020     EISSN: None     Source Type: Journal    
DOI: 10.1078/072320203770865936     Document Type: Article

References (46)

1. Amann, R., Krummholz, L., Stahl, D. A.: Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J. Bact. 172, 762-770 (1990a).
2. Amann, R., Binder, B. J., Olson, R. J., Chisholm, S. W., Devereux, R., Stahl, D. A.: Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl. Environ. Microbiol. 56, 1919-1925 (1990b).
3. Amann, R., Springer, N., Ludwig, W., Görtz, H.-D., Schleifer, K.-H.: Identification in situ and phylogeny of uncultured bacterial endosymbionts. Nature 351, 161-164 (1991).
4. Amann, R.I., Ludwig, W., Schleifer, K.-H.: Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. Mar. 59, 143-169 (1995).
5. Azam, F., Fenchel, T., Field, J. G., Gray, J. S., Meyer-Reil, L. A., Thingstad, F.: The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser. 10, 257-263 (1983).
6. Boenigk, J., Arndt, H., Cleven, E.-J.: The problematic nature of fluorescently labelled bacteria (FLB) in Spumella feeding experiments - an explanation by using video microscopy. Arch. Hydrobiol. 152, 329-338 (2001).
7. Carlough, L.A., Meyer, J. L.: Rates of protozoan bacterivory in three habitats of a southeastern blackwater river. J. N. Am.Benthol. Soc. 9, 45-53 (1990).
8. Carrias, J.F., Amblard, C., Bourdier, G.: Protistan bacterivory in an oligomesotrophic lake: importance of attached ciliates and flagellates. Microb. Ecol. 31, 249-268 (1996).
9. Cleven, E.-J.: An improved method of taking cores in sandy sediments. Arch. Hydrobiol. 147, 65-72 (1999).
10. Cleven, E.-J., Weisse, T.: Seasonal succession and taxon-specific bacterial grazing rates of heterotrophic nanoflagellates in Lake Constance. Aquat. Microb. Ecol. 23, 147-161 (2001).
11. Cleven, E.-J., Meyer, E. I.: A sandy hyporheic zone limited vertically by a solid boundary. Arch. Hydrobiol. 157, 267-288 (2003).
12. Daims, H., Brühl, A., Amann, R., Schleifer, K.-H., Wagner, M.: The domain-specific probe EUB338 is insufficient for the detection of all bacteria: development and evaluation of a more comprehensive probe set. System. Appl. Microbiol. 22, 434-444 (1999).
13. Eisenmann, H., Harms, H., Meckenstock, R., Meyer, E. I., Zehnder, J. B.: Grazing of a Tetrahymena sp. On adhered bacteria in percolated columns monitored by in situ hybridization with fluorescent oligonucleotide probes. Appl. Environ. Microbiol. 64, 1264-1269 (1998).
14. Elliot, A.M., Clemmons, G. L.: An ultrastructural study of ingestion and digestion in Tetrahymena pyriformis. J. Protozool. 13, 311-323 (1966).
15. Epstein, S. S.: Simultaneous enumeration of protozoa and microfauna from marine sandy sediments. Aquat. Microb. Ecol. 9, 219-227 (1995).
16. Epstein, S. S.: Microbial food webs in marine sediments. I. Trophic interactions and grazing rates in two tidal flat communities. Microb. Ecol. 34, 188-198 (1997).
17. Epstein, S. S., Shiaris, M. P.: Rates of microbenthic and meiobenthic bacterivory in a temperate muddy tidal flat community. Appl. Environ. Microbiol. 58, 2426-2431 (1992).
18. Epstein, S. S., Burkovsky, I. V., Shiaris, M. P.: Ciliate grazing on bacteria, flagellates, and microalgae in a temperate zone sandy tidal flat: Ingestion rates and food niche partitioning. J. Exp. Mar. Biol. Ecol. 165, 103-123 (1992).
19. Foissner, W., Berger, H., Kohmann, F.: Taxonomie und ökologische Revision der Ciliaten des Saprobiensystems - Band III: Hymenostomata, Prostomatida, Nassulida. Informationsberichte des Bayer. Landesamtes für Wasserwirtschaft, Heft 1/94 (1994).
20. Fried J., Ludwig, W., Psenner, R., Schleifer, K.-H.: Improvement of ciliate identification and quantification: a new protocol for fluorescence in situ hybridization (FISH) in combination with silver stain techniques. Syst. Appl. Microbiol. 25, 555-571 (2002).
21. González, J.M.: Bacterivory rate estimates and fraction of active bacterivores in natural protist assemblages from aquatic systems. Appl. Environ. Microbiol. 65, 1463-1469 (1999).
22. González, J.M., Sherr, E. B., Sherr, B. F.: Size-selective grazing on bacteria by natural assemblages of estuarine flagellates and ciliates. Appl. Environ. Microbiol. 56, 583-589 (1990).
23. Gunderson, J.H., Goss, S. H.: Fluorescently-labeled oligonucleotide probes can be used to identify protistan food vacuole contents. J. Euk. Microbiol. 44, 300-304 (1997).
24. Hadas, O., Malinsky-Rushansky, N., Pinkas, R., Cappenberg, T. E.: Grazing on autotrophic and heterotrophic picoplankton by ciliates isolated from Lake Kinneret, Israel. J. Plankton Res. 20, 1435-1448 (1998).
25. Hammer, A., Gruttner, C., Schuhmann, R.: The effect of electrostatic charge of food particles on capture efficiency by Oxyrrhis marina Dujardin (dinoflagellate). Protist 150, 375-382 (1999).
26. Hartung, J., Elpelt, B., Klösener, K.-H.: Statistik: Lehr- und Handbuch der angewandten Statistik, München, Oldenbourg-Verlag 1995.
27. Iriberri, J., Ayo, B., Santamaria, E., Barcina, I., Egea, L.: Influence of bacterial density and water temperature on the grazing activity of two freshwater ciliates. Freshw. Biol. 33, 223-231 (1995).
28. Kemp, P.F.: Bacterivory by benthic ciliates: Significance as a carbon source and impact on sediment bacteria. Mar. Ecol. Prog. Ser. 49, 163-169 (1988).
29. Landry, M. R., Lehner-Fournier, J. M., Sundstrom, J. A., Fagerness, V. L., Selph, K. E.: Discrimination between living und heat-killed prey by a marine zooflagellate, Paraphysomonas vestita (Stokes). J. Exp. Mar. Biol. Ecol. 146, 139-151 (1991).
30. Llobet-Brossa, E., Rossello-Mora, R., Amann, R.: Microbial community composition of Wadden Sea sediments as revealed by fluorescence in situ hybridization. Appl. Environ. Microbiol. 64, 2691-2696 (1998).
31. Lloyd, D., Williams, A. G., Amann, R., Hayes, A. J., Durrant, L., Ralphs, J. R.: Intracellular prokaryotes in rumen ciliate protozoa: Detection by confocal laser scanning microscopy after in situ hybridization with fluorescent 16S rRNA probes. Europ. J. Protistol. 32, 523-531 (1996).
32. Pernthaler, J., Posch, T., Šimek, K., Vrba, J., Amann, R., Psenner, R.: Contrasting bacterial strategies in an experimental microbial assemblage. Appl. Environm. Microbiol. 63, 596-601 (1997).
33. Pernthaler, J., Glöckner, F.-O., Schönhuber, W., Amann, R.: Fluorescence in situ hybridization (FISH) with rRNA-targeted oligonucleotide probes. Method Microbiol. 30, 207-226 (2001).
34. Peters, F.: Prediction of planktonic protistan grazing rates, Limnol. Oceanogr. 39, 195-206 (1994).
35. Porter, K.G., Feig, Y. S.: The use of DAPI for identifying and counting aquatic microflora. Limnol. Oceanogr. 25, 943-948 (1980).
36. Posch, T., Arndt, H.: Uptake of sub-micrometre- and micrometre-sized detrital particles by bacterivorous and omnivorous ciliates. Aquat. Microb. Ecol. 10, 45-53 (1996).
37. Posch, T., Jezbera, J., Vrba, J., Šimek, K., Pernthaler, J., Andreatta, S., Sonntag, B.: Size selective feeding in Cyclidium glaucoma (Ciliophora, Scuticociliatida) and its effects on bacterial community structure: a study from a continuous cultivation system. Microb. Ecol. 42, 217-227 (2001).
38. Ravenschlag, K., Sahm, K., Amann, R.: Quantitative molecular analysis of the microbial community in marine arctic sediments (Svalbard). Appl. Environ. Microbiol. 67, 387-395 (2001).
39. Sachs, L.: Angewandte Statistik. Anwendung statistischer Methoden. Berlin, Springer-Verlag 1991.
40. Sherr, B.F., Sherr, E. B., Fallon, R. D.: Use of monodispersed, fluorescently labeled bacteria to estimate in situ protozoan bacterivory. Appl. Environ. Microbiol. 53, 958-965 (1987).
41. Sibbald, M. J., Albright, L. J., Sibbald, P. R.: Chemosensory responses of a heterotrophic microflagellate to bacteria and several nitrogen compounds. Mar. Ecol. Prog. Ser. 36, 201-204 (1987).
42. Starink, M., Krylova, I. N., Bär-Gilissen, M.-J., Bak, R. P., Cappenberg, T. E.: Rates of benthic protozoan grazing on free and attached sediment bacteria measured with fluorescently stained sediment. Appl. Environ. Microbiol. 60, 2259-2264 (1994).
43. Starink, M., Bär-Gilissen, M.-J., Bak, R. P. M., Cappenberg, T. E.: Quantitative centrifugation to extract benthic protozoa from freshwater sediments. Appl. Environ. Microbiol. 60, 167-173 (1994).
44. Stockner, J.G., Porter, K. G.: Microbial Food Webs in Freshwater Planktonic Ecosystems, pp. 69-83. In: Complex Interactions in Lake Communities (S.R. Carpenter, ed.), Berlin, Springer Verlag 1988.
45. Wallner, G., Amann, R., Beisker, W.: Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms. Cytometry 14, 136-143 (1993).
46. Wilks, S. A., Sleigh, M. A.: Grazing rates in Euplotes mutabilis: relationships between particle size and concentration. Microb. Ecol. 36, 165-174 (1998).