Impact of protozoan grazing on bacterial community structure in soil microcosms

Applied and Environmental Microbiology

Volumn 68, Issue 12, 2002, Pages 6094-6105

  Rønn, Regin ^a,c   McCaig, Allison E ^a   Griffiths, Bryan S ^b   Prosser, James I ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOLOGY; ELECTROPHORESIS; PROTOZOA; RNA;

SOIL BACTERIA;

SOIL TESTING;

ORGANIC COMPOUND; RNA 16S;

BACTERIUM; COMMUNITY STRUCTURE; GRAZING; PROTOZOAN; SOIL MICROORGANISM;

ACANTHAMOEBA; ARTHROBACTER; ARTICLE; BACTERIAL FLORA; CERCOMONAS; COMMUNITY STRUCTURE; DENATURING GRADIENT GEL ELECTROPHORESIS; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; GRAZING; MICROBIAL DIVERSITY; MICROBIAL GROWTH; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT NUTRIENT; POLYMERASE CHAIN REACTION; PROTOZOON; SEQUENCE ANALYSIS; SOIL MICROFLORA; SPUMELLA; THAUMATOMONAS; WHEAT;

ANIMALS; BACTERIA; ECOSYSTEM; ELECTROPHORESIS, POLYACRYLAMIDE GEL; NITROGEN; PROTOZOA; SOIL; SOIL MICROBIOLOGY;

ACANTHAMOEBA; ACANTHAMOEBA SP.; ACTINOBACTERIA (CLASS); ARTHROBACTER; BACTERIA (MICROORGANISMS); CERCOMONAS; MASTIGOPHORA (FLAGELLATES); NEGIBACTERIA; POSIBACTERIA; PROTOZOA; SPUMELLA; THAUMATOMONAS; THAUMATOMONAS SP.; TRITICUM AESTIVUM;

EID: 0242417580     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.68.12.6094-6105.2002     Document Type: Article

References (64)

1. Anscombe, F. J., and B. N. Singh. 1948. Limitation of bacteria by micropredators in soil. Nature 161:140-141.
2. Boenigk, J., and H. Arndt. 2000. Comparative studies of the feeding behavior of two heterotrophic nanoflagellates: the filter-feeding choanoflagellate Monosiga ovata and the raptorial-feeding kinetoplastid Rhyncomonas nasuta. Aquat. Microb. Ecol. 22:243-249.
3. Boenigk, J., and H. Arndt. 2000. Particle handling during interception feeding by four species of heterotrophic nanoflagellates. J. Eukaryot. Microbiol. 47:350-358.
4. Boenigk, J., C. Matz, K. Jürgens, and R. Arndt. 2001. Confusing selective feeding with differential digestion in bacterivorous nanoflagellates. J. Eukaryot. Microbiol. 48:425-432.
5. Boenigk, J., C. Matz, K. Jürgens, and H. Arndt. 2001. The influence of preculture conditions and food quality on the ingestion and digestion process of three species of heterotrophic nanoflagellates. Microb. Ecol. 42:168-176.
6. Brock, T. D., M. T. Madigan, J. M. Martinko, and J. Parker. 1994. Biology of microorganisms, 7th ed. Prentice-Hall International, London, United Kingdom.
7. Caron, D. A. 1987. Grazing of attached bacteria by heterotrophic microflagellates. Microb. Ecol. 13:203-218.
8. Christensen, S., B. Griffiths, F. Ekelund, and R. Rønn. 1992. Huge increase in bacterivores on freshly killed barley roots. FEMS Microbiol. Ecol. 86:303-310.
9. Cordovilla, P., E. Valdiva, A. Gonzalea-Segura, A. Galvez, M. Martinez-Bueno, and M. Maqueda. 1993. Antagonistic action of the bacterium Bacillus licheniformis M-4 toward the amoeba Naegleria fowleri. J. Eukaryot. Microbiol. 40:323-328.
10. Darbyshire, J. F., R. E. Wheatley, M. P. Greaves, and R. H. E. Inkson. 1974. A rapid micromethod for estimating bacterial and protozoan populations in soil. Rev. Ecol. Biol. Sol 11:465-475.
11. Ekelund, F., H. B. Frederiksen, and R. Rønn. 2002. Population dynamics of active and total ciliate populations in arable soil amended with wheat. Appl. Environ. Microbiol. 68:1096-1101.
12. Ekelund, F., and D. J. Patterson. 1997. Some heterotrophic flagellates from a cultivated garden soil in Australia. Arch. Protistenkd. 148:461-478.
13. Ekelund, F., and R. Rønn. 1994. Notes on protozoa in agricultural soil, with emphasis on heterotrophic flagellates and naked amoebae and their ecology. FEMS Microbiol. Rev. 15:321-363.
14. Ekelund, F., R. Rønn, and B. S. Griffiths. 2001. Quantitative estimation of flagellate community structure and diversity in soil samples. Protist 152:301-314.
15. Farrelly, V., F. A. Rainey, and E. Stackebrandt. 1995. Effect of genome size and rrn gene copy number on PCR amplification of 16S rRNA genes from a mixture of bacterial species. Appl. Environ. Microbiol. 61:2798-2801.
16. Fenchel, T. 1987. Ecology of protozoa. The biology of free-living phagotrophic protists. Science Tech Publishers, Madison, Wis.
17. Gonzáles, J. M., J. Iriberri, L. Egea, and I. Barcina. 1990. Differential rates of digestion of bacteria by freshwater and marine phagotrophic protozoa. Appl. Environ. Microbiol. 56:1851-1857.
18. Griffiths, B. S., M. Bonkowski, G. Dobson, and S. Caul. 1999. Changes in soil microbial community structure in the presence of microbial-feeding nematodes and protozoa. Pedobiologia 43:297-304.
19. Griffiths, B. S., K. Ritz, N. Ebblewhite, and G. Dobson. 1999. Soil microbial community structure: effects of substrate loading rates. Soil Biol. Biochem. 31:145-153.
20. Groscop, J. A., and M. M. Brent. 1964. The effects of selected strains of pigmented microorganisms on small free-living amoebae. Can. J. Microbiol. 10:579-584.
21. Güde, H. 1979. Grazing by protozoa as selection factor for activated sludge bacteria. Microb. Ecol. 5:225-237.
22. Gurijala, K. R., and M. Alexander. 1987. Effect of growth rate and hydrophobicity on bacteria surviving protozoan grazing. Appl. Environ. Microbiol. 56:1631-1635.
23. Hackett, C. A., and B. S. Griffiths. 1997. Statistical analysis of the time-course of Biolog substrate utilisation. J. Microbiol. Methods 30:63-69.
24. Hahn, M. W., and M. G. Höfle. 1998. Grazing pressure by a bacterivorous flagellate reverses the relative abundance of Comomonas acidovorans PX54 and Vibrio strain CB5 in chemostat cocultures. Appl. Environ. Microbiol. 64:1910-1918.
25. Hahn, M. W., E. R. B. Moore, and M. G. Höfle. 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.
26. Hahn, M. W., and M. G. Höfle. 2001. Grazing of protozoa and its effect on populations of aquatic bacteria. FEMS Microbiol. Ecol. 35:113-121.
27. Heidmann, T. 1989. Startkarakterisering af arealer til systemforskning. II. Resultater fra arealet ved Foulum. Tidsskr. Planteavls Specialserie S2007:1-186.
28. Iriberri, J., I. Azúa, A. Labirua-Iturburu, I. Artolozaga, and I. Barcina. 1994. Differential elimination of enteric bacteria by protists in a freshwater system. J. Appl. Bacteriol. 77:476-483.
29. Jongman, R. H. G., C. J. F. ter Braak, and O. F. R. van Tongeren. 1987. Data analysis in community and landscape ecology. Centre for Agricultural Publishing and Documentation (Pudoc), Wageningen, The Netherlands.
30. Jürgens, K., and W. R. DeMott. 1995. Behavioral flexibility in prey selection by bacterivorous nanoflagellates. Limnol. Oceanogr. 40:1503-1507.
31. Jürgens, K., and H. Güde. 1994. The potential importance of grazing-resistant bacteria in planktonic systems. Mar. Ecol. Prog. Ser. 112:169-188.
32. Jürgens, K., J. Pernthaler, S. Schalla, and R. Amann. 1999. Morphological and compositional changes in a planktonic bacterial community in response to enhanced protozoan grazing. Appl. Environ. Microbiol. 65:1241-1250.
33. Kennedy, A. C., and V. L. Gewin. 1997. Soil microbial diversity: present and future considerations. Soil Science 162:607-617.
34. Kinner, N. E., R. W. Harvey. K. Blakeslee, G. Novarino, and L. D. Meeker. 1998. Size-selective predation on groundwater bacteria by nanoflagellates in an organic-contaminated aquifer. Appl. Environ. Microbiol. 64:618-625.
35. Magurran, A. E. 1988. Ecological diversity and its measurement. Chapman & Hall, London, United Kingdom.
36. May, K. R. 1965. A new graticule for particle counting and sizing. J. Scientific Instrum. 42:500-501.
37. McCaig, A. E., L. A. Glover, and J. I. Prosser. 2001. Numerical analysis of grassland bacterial community structure under different land management regimens by using 16S ribosomal DNA sequence data and denaturing gradient gel electrophoresis banding patterns. Appl. Environ. Microbiol. 67:4554-4559.
38. Monger, B. C., M. R. Landry, and S. L. Brown. 1999. Feeding selection of heterotrophic marine nanoflagellates based on the surface hydrophobicity of their picoplankton prey. Limnol. Oceanogr. 44:1917-1927.
39. Muyzer, G., E. C. de Waal, and A. G. Uitterlinden. 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 59:695-700.
40. Page, F. C. 1988. A new key to freshwater and soil gymnamoebae. Freshwater Biological Association, Ambleside, United Kingdom.
41. Payne, R. W., P. W. Lane, P. G. N. Digny, S. A. Harding, P. K. Leech, G. W. Morgan, A. D. Todd, R. Thompson, G. T. Wilson, S. J. Welham, and R. P. White. 1993. Genstat 5 release 3 reference manual. Oxford University Press, Oxford, United Kingdom.
42. Pernthaler, J., B. Sattler, K. Šimek, A. Schwarzenbacher, and R. Psenner. 1996. Top-down effects on the size-biomass distribution of a freshwater bacterioplankton community. Aquat. Microb. Ecol. 10:255-263.
43. Pernthaler, J., T. Posch, K. Šimek, J. Vrba, A. Pernthaler, F. O. Glöckner, U. Nübel, R. Psenner, and R. Amann. 2001. Predator-specific enrichment of actinobacteria from a cosmopolitan freshwater clade in mixed continuous culture. Appl. Environ. Microbiol. 67:2145-2155.
44. Polz, M. F., and C. M. Cavanaugh. 1998. Bias in template-to-product ratios in multitemplate PCR. Appl. Environ. Microbiol. 64:3724-3730.
45. Postma, J., and J. A. van Veen. 1990. Habitable pore space and survival of Rhizobium leguminosarum biovar trifolii introduced into soil. Microb. Ecol. 19:149-161.
46. Priemé, A., J. I. B. Sitaula, Å. K. Klemedtsson, and L. R. Bakken. 1996. Extraction of methane-oxidizing bacteria from soil particles. FEMS Microbiol. Ecol. 21:59-68.
47. Rønn, R., F. Ekelund, and S. Christensen. 1995. Optimizing soil extract and broth media for MPN-enumeration of naked amoebae and heterotrophic flagellates in soil. Pedobiologia 39:10-19.
48. Rønn, R., I. K. Thomsen, and B. Jensen. 1995. Naked amoebae, flagellates, and nematodes in soils of different texture. Eur. J. Soil Biol. 31:135-141.
49. Rønn, R., B. S. Griffiths, F. Ekelund, and S. Christensen. 1996. Spatial distribution and successional pattern of microbial activity and micro-faunal populations on decomposing barley roots. J. Appl. Ecol. 33:662-672.
50. Rønn, R., J. Grunert, and F. Ekelund. 2001. Protozoan response to addition of the bacteria Mycobacterium chlorophenolicum and Pseudomonas chlororaphis to soil microcosms. Biol. Fertil. Soils 33:126-131.
51. Rønn, R. M., B. S. Griffiths, and I. M. Young. 2001. Protozoa, nematodes and N-mineralization across a prescribed soil textural gradient. Pedobiologia 45:481-495.
52. Schmalenberger, A., F. Schweiger, and C. C. Tebbe. 2001. Effect of primers hybridising to different evolutionarily conserved regions of the small-subunit rRNA gene in PCR-based microbial community analyses and genetic profiling. Appl. Environ. Microbiol. 67:3557-3563.
53. Sherr, B. F., E. B. Sherr, and J. McDaniel. 1992. Effect of protistan grazing on the frequency of dviding cells in bacterioplankton assemblages. Appl. Environ. Microbiol. 58:2381-2385.
54. Sibbald, M. J., and L. J. Albright. 1988. Aggregated and free bacteria as food sources for heterotrophic microflagellates. Appl. Environ. Microbiol. 54:613-616.
55. Šimek, K., J. Vrba, J. Pernthaler, T. Posch, P. Hartman, J. Nedoma, and R. Psenner. 1997. Morphological and compositional shifts in an experimental bacterial community influenced by protists with contrasting feeding modes. Appl. Environ. Microbiol. 63:587-595.
56. Šimek. K., J. Pernthaler, M. G. Weinbauer, K. Hornák, J. R. Dolan, J. Nedoma, M. Mašín, and R. Amann. 2001. Changes in bacterial community composition and dynamics and viral mortality rates associated with enhanced flagellate grazing in a mesoeutrophic reservoir. Appl. Environ. Microbiol. 67:2723-2733.
57. Sinclair, J. L., and M. Alexander. 1989. Effect of protozoan predation on relative abundance of fast- and slow-growing bacteria. Can. J. Microbiol. 35:578-582.
58. Singh, B. N. 1941. Selectivity in bacterial food by soil amoebae in pure mixed culture and in sterilized soil. Ann. Appl. Biol. 28:52-64.
59. Verity, P. G. 1991. Feeding in planktonic protozoans: evidence for nonrandom acquisition of prey. J. Protozool. 38:69-76.
60. Vestergaard, P., R. Rønn, and S. Christensen. 2001. Reduced particle size of plant material does not stimulate decomposition, but affects the microbivorous microfauna. Soil Biol. Biochem. 33:1805-1810.
61. Webster, G., T. M. Embley, and J. I. Prosser. 2002. Grassland management regimens reduce small-scale heterogeneity and species diversity of β-proteobacterial ammonia oxidizer populations. Appl. Environ. Microbiol. 68:20-30.
62. Weekers, P. H. H., P. L. E. Bodelier, J. P. H. Wijen, and G. D. Vogels. 1993. Effects of grazing by the free-living soil amoebae Acanthamoeba castellanii, Acanthamoeba polyphaga, and Hartmannella vermiformis on various bacteria. Appl. Environ. Microbiol. 59:2317-2319.
63. Wratten, S. D., and G. L. A. Fry. 1980. Field and laboratory exercises in ecology. Edward Arnold, London, United Kingdom.
64. Wright, D., K. Killham, L. A., Glover, and J. I. Prosser. 1993. The effects of location on protozoan grazing of a genetically modified bacterial inoculum in soil. Geoderma 56:633-640.