Interactions between bacteria, protozoa and nematodes in soil

Acta Protozoologica

Volumn 51, Issue 3, 2012, Pages 223-235

  Rønn, Regin ^a   Vestergård, Mette ^a   Ekelund, Flemming ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Amoebae; Bacteria; Colonisation; Competition; Feeding types; Flagellates; Interactions; Migration; Nematodes; Physico chemical environment; Plant growth; Population growth; Predation; Protozoa; Soil; Soil texture; Trophic interactions

Indexed keywords

BACTERIA (MICROORGANISMS); MASTIGOPHORA (FLAGELLATES); NEMATODA; PROTOZOA;

EID: 84873549794     PISSN: 00651583     EISSN: 16890027     Source Type: Journal    
DOI: 10.4467/16890027AP.12.018.0764     Document Type: Review

References (109)

1. Adl S. M. (2007) Motility and migration rate of protozoa in soil columns. Soil Biol. Biochem. 39: 700-703
2. Alphei J., Bonkowski M., Scheu S. (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
3. Altenburger A., Ekelund F., Jacobsen C. S. (2010) Protozoa and their bacterial prey colonize sterile soil fast. Soil Biol. Biochem. 42: 1636-1639
4. Anderson A. R. A., Young I. M., Sleeman B. D., Griffiths B. S., Robertson W. M. (1997) Nematode movement along a chemical gradient in a structurally heterogeneous environment. 1. Experiment. Fund. Appl. Nematol. 20: 157-163
5. Anderson T. R., Patrick Z. A. (1978) Mycophagous amoeboid organisms from soil that perforate spores of Thielaviopsis basicola and Cochliobolus sativus. Phytopathology 68: 1618-1626
6. Avery L., Shtonda B. B. (2003) Food transport in the C. elegans pharynx. J. Exp. Biol. 206: 2441-2457
7. Bjørnlund L., Rønn, R. (2008) 'David and Goliath' of the soil food web - flagellates that kill nematodes. Soil Biol. Biochem. 40: 2032-2039
8. Bjørnlund L., Liu M., Rønn R., Christensen S., Ekelund F. (2012) Nematodes and protozoa affect plants differently; depending on soil nutrient status. Eur. J. Soil Biol. 50: 28-31
9. Bjørnlund L., Mørk S., Vestergård M., Rønn R. (2006) Trophic interactions between rhizosphere bacteria and bacterial feeders influenced by phosphate and aphids in barley. Biol. Fert. Soils 43: 1-11
10. Bjørnlund L., Rønn R., Pechy-Tarr M., Maurhofer M., Keel C., Nybroe O. (2009) Functional GacS in Pseudomonas DSS73 prevents digestion by Caenorhabditis elegans and protects the nematode from killer flagellates. ISME J. 3: 770-779
11. Bonkowski M., Brandt F. (2002) Do soil protozoa enhance plant growth by hormonal effects? Soil Biol. Biochem. 34: 1709-1715
12. Boenigk J., Arndt H. (2000) Comparative studies on the feeding behavior of two heterotrophic nanoflagellates: the filterfeeding choanoflagellate Monosiga ovata and the raptorial-feeding ki-- netoplastid Rhynchomonas nasuta. Aquat. Microbial. Ecol. 22: 243-249
13. Boenigk J., Arndt H. (2002) Bacterivory by heterotrophic flagellates: community structure and feeding strategies. A. van Leeuw. 81: 465-480
14. Boenigk J., Matz C., Jürgens K., Arndt H. (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
15. Bouwman L. A., Zwart K. B. (1994) The ecology of bacterivorous protozoans and nematodes in arable soil. Agr. Ecosyst. Environ. 51: 145-160
16. Bouwman L. A., Bloem J., Van den Boogert P. H. J. F., Bremer F., Hoenderboom G. H. J., De Ruiter P. C. (1994) Short-term and long-term effects of bacterivorous nematodes and nematophagous fungi on carbon and nitrogen mineralization in microcosms. Biol. Fert. Soils 17: 249-256
17. Carson J. K., Gonzalez-Quinones V., Murphy D. V., Hinz C., Shaw J. A., Gleeson D. B. (2010) Low Pore Connectivity Increases Bacterial Diversity in Soil. Appl. Environ. Microbiol. 12: 3936-3942
18. Clarholm M. (1985) Interactions of bacteria, protozoa and plants leading to mineralization of soil nitrogen. Soil Biol. Biochem. 17: 181-187
19. Croll N. A. (1970) The Behaviour of Nematodes - their activities, senses and responses. Edward Arnold, London
20. De Mesel I., Derycke S., Moens T., Van der Gucht K., Vincx M., Swings J. (2004) Top-down impact of bacterivorous nematodes on the bacterial community structure: a microcosm study. Environ. Microbiol. 6: 733-744
21. Djigal D., Brauman A., Diop T. A., Chotte J. L., Villenave C. (2004) Influence of bacterial-feeding nematodes (Cephalobidae) on soil microbial communities during maize growth. Soil Biol. Biochem. 36: 323-331
22. Ekelund F. (1996) Growth kinetics of five common heterotrophic soil flagellates. Eur. J. Soil Biol. 32: 15-24.
23. Ekelund F. (1998) Enumeration and abundance of mycophagous protozoa in soil, with special emphasis on heterotrophic flagellates. Soil Biol. Biochem. 30: 1343-1347
24. Ekelund F. (2002) a study of the soil flagellate Phalansterium solitarium Sandon 1924 with preliminary data on its ultrastructure. Protistology 2: 152-158
25. Ekelund F., Patterson D. J. (1997) Some heterotrophic flagellates from a cultivated soil in Australia. Arch. Protistenkd. 148: 461- 478
26. Ekelund F., Rønn R. (1994) Notes on protozoa in agricultural soil with emphasis on heterotrophic flagellates and naked amoebae and their ecology. FEMS Microbiol. Rev. 15: 321-353
27. Ekelund F., Rønn R., Griffiths B. S. (2001) Quantitative estimation of flagellate community structure and diversity in soil samples. Protist 152: 301-314
28. Ekelund F., Frederiksen H. B., Rønn R. (2002) Population dynamics of active and total ciliate populations in arable soil amended with wheat. Appl. Environ. Microbiol. 68: 1096-1101
29. Ekelund F., Saj S., Vestergård M., Bertaux J., Mikola J. (2009) The "soil microbial loop" is not always needed to explain protozoan stimulation of plants. Soil Biol. Biochem. 41: 2336-2342
30. Elliott E. T., Anderson R. V., Coleman D. C., Cole C. V. (1980) Habitable pore space and microbial trophic interactions. Oikos 35: 327-335
31. Fenchel T. (1980) Relation between particle size selection and clearance in suspension-feeding ciliates. Limnol. Oceanogr. 25: 733-738.
32. Fenchel T. (1987). Ecology of protozoa. The biology of free-living phagotrophic protists. Springer-Verlag, Berlin
33. Foissner W. (1987) Soil protozoa: Fundamental problems, ecological significance, adaptations in ciliates and testaceans, bioindicators and guide to the literature. Progr. Protistol. 2: 69-212
34. Freckman D. W., Whitford W. G., Steinberger Y. (1987) Effect of irrigation on nematode population dynamics and activity in desert soils. Biol. Fert. Soils 3: 3-10
35. Georgieva S., Christensen S., Petersen H., Gjelstrup P., Thorup-Kristensen K. (2005) Early decomposer assemblages of soil organisms in litterbags with vetch and rye roots. Soil Biol. Biochem. 37: 1145-1155
36. Giller P. S. (1991) The diversity of soil communities, the 'poor man's tropical rainforest'. Biodivers. Conserv. 5: 135-168
37. Grewal P. S., Wright D. J. (1992) Migration of Caenorhabditis elegans (Nematoda: Rhabditidae) larvae towards bacteria and the nature of the bacterial stimulus. Fund. Appl. Nematol. 15: 159-166
38. Griffiths B. S. (1986) Mineralization of nitrogen and phosphorus by mixed cultures of the ciliate protozoan Colpoda steinii, the nematode Rhabditis sp. and the bacterium Pseudomonas fluorescens. Soil Biol. Biochem. 18: 637-641
39. Griffiths B. S. (1989) Enhanced nitrification in the presence of bacteriophagous protozoa. Soil Biol. Biochem. 21: 1045-1051
40. Griffiths B. S. (1994) Soil Nutrient Flow. In: Soil Protozoa, (Ed. J. F. Darbyshire). CAB International, Wallingford, 65-91
41. Griffiths B. S., Caul S. (1993) Migration of bacterial-feeding nematodes, but not protozoa, to decomposing grass residues. Biol. Fert. Soils 15: 201-207
42. Griffiths B. S., Young I. M., Caul S. (1995) Nematode and protozoan population-dynamics on decomposing barley leaves incubated at different soil matric potentials. Pedobiologia 39: 454-461
43. Griffiths B. S., Bonkowski M., Dobson G., Caul S. (1999) Changes in soil microbial community structure in the presence of microbialfeeding nematodes and protozoa. Pedobiologia 43: 297-304
44. Griffiths B. S., Ritz K., Bardgett R. D., Cook R., Christensen S., Ekelund F., Sørensen S. J., Bååth E., Bloem J., de Ruiter P. C., Dolfing J., Nicolardot B. (2000) Ecosystem response of pasture soil communities to fumigation-induced microbial diversity reductions: an examination of the biodiversity-ecosystem function relationship. Oikos 90: 279-294
45. Hahn M. W., Höfle M. G. (2001) Grazing of protozoa and its effect on populations of aquatic bacteria. FEMS Microbiol. Ecol. 35: 113-127
46. Hausman K., Hülsman N., Radek R. (2003) Protistology. E. Schweizerbart'sche Verlagsbuchhandlung, Berlin, Stuttgart
47. Hess S., Sausen N., Melkonian M. (2012) Shedding light on vampires: The phylogeny of vampyrellid amoebae revisited. Plos One 7: e31165
48. Holtkamp R., Kardol P., van der Wal A., Dekker S. C., van der Putten W., de Ruiter P. C. (2008) Soil food web structure during ecosystem development after land abandonment. Appl. Soil Ecol. 39: 23-34
49. Hunt H. W., Coleman D. C., Ingham E. R., Elliott E. T., Moore J. C., Rose S. L., Reid C. P. P., Morley C. R. (1987) The detrital food web in a shortgrass prairie. Biol. Fert. Soils 3: 57-68
50. Ingham R. E., Trofymow J. A., Ingham E. R., Coleman D. C. (1985) Interactions of bacteria, fungi, and their nematode grazers: effects on nutrient cycling and plant growth. Ecol. Monogr. 55: 119-140
51. Jentschke G., Bonkowski M., Godbold D. L., Scheu S. (1995) Soil protozoa and forest tree growth: non-nutritional effects and interactions with mycorrhizae. Biol. Fert. Soils 20: 263-269
52. Jones F. G. W., Thomasson A. J. (1976) Bulk density as an indicator of pore space in soils usable by nematodes. Nematologica 22: 133-137
53. Jousset A., Lara E., Wall L. G., Valverde C. (2006) Secondary metabolites help biocontrol strain Pseudomonas fluorescens CHA0 to escape protozoan grazing. Appl. Environ. Microbiol. 72: 7083-7090
54. Jousset A., Scheu S., Bonkowski M. (2008) Secondary metabolite production facilitates establishment of rhizobacteria by reducing both protozoan predation and the competitive effects of indigenous bacteria. Funct. Ecol. 22: 714-719
55. Jürgens K., DeMott W. R. (1995) Behavioral flexibility in prey selection by bacterivorous nanoflagellates. Limnol. Oceanogr. 40: 1503-1507
56. Jürgens K., Güde H. (1994) The potential importance of grazing-- -resistant bacteria in planktonic systems. Mar. Ecol. Prog. Ser. 112: 169-188
57. Jürgens K., Matz C. (2002) Predation as a shaping force for the phenotypic and genotypic composition of planktonic bacteria. A. van Leeuw. 81: 413-434
58. Klinge K. (1958) Pseudomonas-fluorescens-Polysaccharide als Schutz gegen Phagozytose durch Amöben. Naturwissenschaften 22: 550-551
59. Kreuzer K., Adanczyk J., Iijima M., Wagner M., Scheu S., Bonkowski M. (2006) Grazing of a common species of soil protozoa (Acanthamoeba castellani) affects rhizosphere bacterial community composition and root architecture of rice (Oryza sativa L.). Soil Biol. Biochem. 38: 1665-1672
60. Krome K., Rosenberg K., Dickler C., Kreuzer K., Ludwig-Müller J., Ullrich-Eberius C., Scheu S., Bonkowski M. (2010) Soil bacteria and protozoa affect root branching via effects on the auxin and cytokinin balance in plants. Plant Soil 328: 191-201
61. Kühn S., Medlin L., Eller G. (2004) Phylogenetic position of the parasitoid nanoflagellate Pirsonia inferred from nuclear-encoded small subunit ribosomal DNA and a description of Pseudopirsonia n. gen. and Pseudopirsonia mucosa (Drebes) comb. nov. Protist 155: 143-156
62. Kuikman P. J., Van Elsas J. D., Jansen A. G., Burgers S. L. G. E., Van Veen J. A. (1990) Population dynamics and activity of bacteria and protozoa in relation to their spatial distribution in soil. Soil Biol. Biochem. 22: 1063-1073
63. 15N-Nitrogen mineralization from bacteria by protozoan grazing at different soil moisture regimes. Soil Biol. Biochem. 23: 193-200
64. Lekfeldt J. D. S., Rønn R. (2008) A common soil flagellate (Cercomonas sp.) grows slowly when feeding on the bacterium Rhodococcus fascians in isolation, but does not discriminate against it in a mixed culture with Sphingopyxis witflariensis. FEMS Microbiol. Ecol. 65: 113-124
65. Matz C., Jürgens K. (2003) Interaction of nutrient limitation and protozoan grazing determines the phenotypic structure of a bacterial community. Microb. Ecol. 45: 384-398
66. Matz C., Kjelleberg S. (2005) Off the hook - how bacteria survive protozoan grazing. Trends Microbiol. 13: 302-307
67. Matz C., Boenigk J., Arndt H., Jürgens K. (2002) Role of bacterial phenotypic traits in selective feeding of the heterotrophic nanoflagellate Spumella sp. Aquat. Microb. Ecol. 27: 137-148
68. Matz C., Bergfeld T., Rice S. A., Kjelleberg S. (2004) Microcolonies, quorum sensing and cytotoxicity determine the survival of Pseudomonas aeruginosa biofilms exposed to protozoan grazing. Environ. Microbiol. 6: 218-226.
69. Moens T., Verbeeck L., De Maeyer A., Swings J., Vincx M. (1999) Selective attraction of marine bacterivorous nematodes to their bacterial food. Mar. Ecol. Prog-Ser. 176: 165-178.
70. Moore J. C., McCann K., de Ruiter P. C. (2005) Modeling trophic pathways, nutrient cycling, and dynamic stability in soils. Pedobiologia 49: 499-510
71. Munn E. A., Munn P. D. (2002) Feeding and digestion. In: The biology of nematodes, (Ed. D. L. Lee). Taylor & Francis, Singapore, 211-232
72. Neidig N., Jousset A., Nunes F., Bonkowski M., Paul R. J., Scheu S. (2010) Interference between bacterial feeding nematodes and amoebae relies on innate and inducible mutual toxicity. Funct. Ecol. 24: 1133-1138
73. Old K. M., Darbyshire J. F. (1978) Soil fungi as food for giant amoebae. Soil Biol. Biochem. 111: 93-100
74. Old K. M., Darbyshire J. F. (1980) Arachnula impatiens Cienk., a mycophagous giant amoeba from soil. Protistologica 16: 277-287
75. Pedersen A. L., Nybroe O., Winding A., Ekelund F., Bjørnlund L. (2009) Bacterial feeders, the nematode Caenorhabditis elegans and the flagellate Cercomonas longicauda, have different effects on outcome of competition among the Pseudomonas biocontrol strains CHA0 and DSS73. Microb. Ecol. 57: 501-509
76. Pedersen A. L., Ekelund F., Johansen A., Winding A. (2010) Interaction of bacterial feeding flagellates and Pseudomonas spp. Biol. Fert. Soils 46: 151-158
77. Pedersen A. L., Winding A., Altenburger A., Ekelund F. (2011) Protozoan growth rates on secondary-metabolite-producing Pseudomonas spp. correlate with high-level protozoan taxonomy. FEMS Microbiol. Lett. 316: 16-22
78. Rosenberg K., Bertaux J., Krome K., Hartmann A., Scheu S., Bonkowski M. (2009) Soil amoebae rapidly change bacterial community composition in the rhizosphere of Arabidopsis thaliana. ISME J. 3: 675-684
79. Rutherford P. M., Juma N. G. (1992) Influence of texture on habitable pore space and bacterial-protozoan populations in soil. Biol. Fert. Soils 12: 221-227
80. Rønn R., Thomsen I. K., Jensen B. (1995) Naked amoebae, flagellates and nematodes in soil of different texture. Eur. J. Soil Biol. 31: 135-141
81. Rønn R., Ekelund F., Grunert J. (2001a). Protozoan response to addition of the bacteria Mycobacterium chlorophenolicus and Pseudomonas chlororaphis to soil microcosms. Biol. Fert. Soils. 33: 126-131
82. Rønn R. M., Griffiths B. S., Young I. M. (2001b) Protozoa, nematodes and N-mineralization across a prescribed soil textural gradient. Pedobiologia 45: 481-495
83. Rønn R., McCaig A. E., Griffiths B. S., Prosser J. I. (2002) Impact of protozoan grazing on bacterial community structure in soil microcosms. Appl. Environ. Microbiol. 68: 6094-6105
84. Salinas K. A., Edenborn S. L., Sexstone A. J., Kotcon J. B. (2007) Bacterial preferences of the bacterivorous soil nematode Cephalobus brevicauda (Cephalobidae): Effect of bacterial type and size. Pedobiologia 51: 55-64
85. Sandon H. (1927) The composition and distribution of the protozoan fauna of the soil. Oliver and Boyd, Edinburgh and London
86. Sayre R. M. (1973) Theratromyxa weberi, an amoeba predatory on plant-parasitic nematodes. J. Nematol. 5: 258-264
87. Sayre R. M., Wergin W. P. (1989) Morphology and fine structure of the trophozoites of Theratromyxa weberi (Protozoa: Vampyrellidae) predacious on soil nematodes. Can. J. Microbiol. 35: 589-602
88. Schnepf E., Kühn S. F. (2000) Food uptake and fine structure of Cryothecomonas longipes sp. nov., a marine nanoflagellate incertae sedis feeding phagotrophically on large diatoms. Helgoland Marine Research 54: 18-32
89. Shtonda B. B., Avery L. (2006) Dietary choice behavior in Caenorhabditis elegans. J. Exp. Biol. 209: 89-102
90. Small R. W. (1987) a review of the prey of predatory soil nematodes. Pedobiologia 30: 179-206
91. Steiner G., Albin F. M. (1946) Resuscitation of the nematode Tylenchus polyhypnus, n. sp. after almost 39 years dormancy. Journal of the Washington Academy of Science 36: 97-99
92. Thirup L., Ekelund F., Johnsen K., Jacobsen C. S. (2000) Population dynamics of the fast-growing sub-populations of Pseudomonas and total bacteria, and their protozoan grazers, revealed by fenpropimorph treatment. Soil Biol. Biochem. 32: 1615-1623
93. Thurman J., Parry J. D., Hill P. J., Laybourn-Parry J. (2010). The filter-feeding ciliates Colpidium striatum and Tetrahymena pyriformis display selective feeding behaviours in the presence of mixed, equally-sized, bacterial prey. Protist 161: 577-588
94. Verhagen F. J. M., Duyts, H., Laanbroek H. J. (1993) Effects of grazing by flagellates on the competition for ammonium between nitrifying and heterotrophic bacteria in soil columns. Appl. Environ. Microbiol. 59: 2099-2106
95. Vestergaard P., Rønn R., Christensen S. (2001) Reduced particle size of plant material does not stimulate decomposition, but affects the microbivorous microfauna. Soil Biol. Biochem. 33: 1805-1810
96. Vestergård M., Bjørnlund L., Henry F., Rønn R. (2007) Decreasing prevalence of rhizosphere IAA producing and seedling root growth promoting bacteria with barley development irrespective of protozoan grazing regime. Plant Soil 295: 115-125
97. Weber A. P., Zwillenberg L. O., Van der Laan P. A. (1952) a predacious amoeboid organism destroying larvae of the potato root eelworm and other nematodes. Nature 169: 834-835
98. Weekers P. H. H., Bodelier P. L. E., Wijen J. P. H., Vogels G. D. (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
99. Wildschutte H., Wolfe D. M., Tamewitz A., Lawrence J. G. (2004) Protozoan predation, diversifying selection, and the evolution of antigenic diversity in Salmonella. Proc. Nat. Acad. Sci. 101: 10644-10649
100. Winslow R. D., Williams T. D. (1957) Amoeboid organisms attacking larvae of the potato root eelworm (Heterodera rostochiensis Woll.) in England and the beet eelworm (H. schachtii Schm.) in Canada. Eur. J. Plant Pathol. 63: 242-243
101. Woombs M., Laybourn-Parry J. (1984) Feeding biology of Diplogasteritus nudicapitatus and Rhabditis curvivcaudata (Nematoda) related to food concentration and temperature, in sewage treatment plants. Oecologia 64: 163-167
102. Wootton E. C., Zubkov M. V., Jones D. H., Jones R. H., Martel C. M., Thornton C. A., Robert E. C. (2007) Biochemical prey recognition by planktonic protozoa. Environ. Microbiol. 9: 216-222
103. Xiao H., Griffiths B., Chen X., Liu M., Jiao J., Hu F., Li H. (2010) Influence of bacterial-feeding nematodes on nitrification and the ammonia-oxidizing bacteria (AOB) community composition. Appl. Soil Ecol. 45: 131-137
104. Yeates G. W. (1987) Nematode feeding and activity: the importance of development stages. Biol. Fertil. Soils 3: 143-146
105. Yeates G. W., Bongers T., De Goede R. G. M., Freckman D., Georgieva S. S. (1993) Feeding habits in soil nematode families and genera - an outline for soil ecologists. J. Nematol. 25: 315-331
106. Yeates G. W., Foissner W. (1995) Testate amoebae as predators of nematodes. Biol. Fert. Soils 20: 1-7
107. Yeates G. W., Dando J. L., Shepherd T. G. (2002) Pressure plate studies to determine how soil moisture affects access of bacterial-feeding nematodes to food in soil. Eur. J. Soil Sci. 53: 355-365
108. Young I. M., Griffiths B. S., Robertson W. M., McNicol J. W. (1998) Nematode (Caenorhabditis elegans) movement in sand as affected by particle size, moisture and the presence of bacteria (Escherichia coli). Eur. J. Soil Sci. 49: 237-241
109. Zwart K. B., Kuikman P. J., Van Veen J. A. (1994) Rhizosphere Protozoa: Their significance in nutrient dynamics. In: Soil Protozoa, (Ed. J. F. Darbyshire). CAB International, Wallingford, 93-121