Abstract
How bacterial feeding fauna affects colonization and survival of bacteria in soil is not well understood, which constrains the applicability of bacterial inoculants in agriculture. This study aimed to unravel how food quality of bacteria and bacterial feeders with different feeding habits (the selective feeding flagellate Cercomonas longicauda versus the non-selective feeding nematode Caenorhabditis elegans) influence the abundance of two bacteria that compete for resources in simple model communities. Microcosms consisted of either one gfp-tagged bacterial strain (Pseudomonas fluorescens DSM50090 or one of two biocontrol strains P. fluorescens CHA0 or Pseudomonas sp. DSS73) or combinations of two bacterial strains. DSM50090 is a suitable food bacterium, DSS73 is of intermediate food quality, and CHA0 is inedible to the bacterial feeders. Bacterial and protozoan cell numbers were measured by flow cytometry. In the presence of flagellates, CHA0 increased its abundance as compared to the other biocontrol strain DSS73 or to DSM50090, which were both eaten by the flagellates. In contrast, the number of CHA0 declined as compared to DSS73 when the model community was subjected to nematode predation pressure. Hence, the results suggested that the outcome of competition among bacteria depended on their ability to cope with the prevailing bacterial predator.
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Andersen JB, Koch B, Nielsen TH, Sørensen D, Hansen M, Nybroe O, Christophersen C, Sørensen J, Molin S, Givskov M (2003) Surface motility in Pseudomonas sp. DSS73 is required for efficient biological containment of the root-pathogenic microfungi Rhizoctonia solani and Pythium ultimum. Microbiology 149:37–46
Andersen KS, Winding A (2004) Non-target effects of bacterial biological control agents on soil protozoa. Biol Fertil Soil 40:230–236
Begon M, Harper JL, Townsend CR (1996) Ecology: individuals, populations, and communities,, 3rd edn. Blackwell, Cambridge
Bennett AJ, Whipps JM (2008) Beneficial microorganism survival on seed, roots and in rhizosphere soil following application to seed during drum priming. Biol Control 44:349–361
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 Fertil Soil 43:1–11
Blanc C, Sy M, Djigal D, Brauman A, Normand P, Villenave C (2006) Nutrition on bacteria by bacterial-feeding nematodes and consequences on the structure of soil bacterial community. Europ J Soil Biol 42:70–78
Boenigk J, Arndt H (2000) Particle handling during interception feeding by four species of heterotrophic nanoflagellates. J Eukaryot Microbiol 47:350–358
Boenigk J, Matz C, Jürgens K, Arndt H (2001a) The influence of preculture conditions and food quality on the ingestion and digestion process of three species of heterotrophic nanoflagellates. Microb Ecol 42:68–176
Boenigk J, Matz C, Jürgens K, Arndt H (2001b) Confusing selective feeding with differential digestion in bacterivorous Nanoflagellates. J. Eukaryot Microbiol 48:425–432
Bonkowski M, Brandt F (2002) Do soil protozoa enhance plant growth by hormonal effects? Soil Biol Biochem 34:1709–1715
Brenner S (1974) The Genetics of Caenorhabditis elegans. Genetics 77:71–94
Cavalier-Smith T, Chao EE (2003) Phylogeny and classification of phylum Cercozoa (Protozoa). Protist 154:341–358
Choi KH, Kumar A, Schweizer HP (2006) A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: application for DNA fragment transfer between chromosomes and plasmid transformation. J Microbial Meth 64:391–397
Christensen S, Bjørnlund L, Vestergård M (2006) Decomposer biomass in the rhizosphere to asses rhizodeposition. Oikos 116:65–74
Christensen S, Bonde GJ (1985) Seasonal variation in number and activity of denitrifying bacteria in soil—taxonomy and physiological groups among isolates. Dan J Plant Soil Sci 89:367–372
Eccleston-Parry JD, Leadbeater BSC (1994) A comparison of the growth-kinetics of 6 marine heterotrophic nanoflagellates fed with one bacterial species. Mar Ecol-Prog Ser 105:167–177
Ekelund F (1996) Growth kinetics of five common heterotrophic soil flagellates. Eur J Soil Sci 32:15–24
Ekelund F, Daugbjerg N, Fredslund L (2004) Phylogeny of Heteromita, Cercomonas and Thaumatomonas based on SSU rDNA sequences, including the description of Neocercomonas jutlandica sp. nov., gen. nov. Eur J Protistol 40:119–135
Fu Y, O’Kelly C, Sieracki M, Distel DL (2003) Protistan grazing analysis by flow cytometry using prey labelled by in vivo expression of fluorescent proteins. Appl Environ Microbiol 69:6848–6855
Griffiths BS, Bonkowski M, Dobson G, Caul S (1999) Changes in soil microbial community structure in the presence of microbial feeding nematodes and protozoa. Pedobiologia 43:297–304
van Hannen EJ, Veninga M, Bloem J, Gons HJ, Laanbroek HJ (1999) Genetic changes in the bacterial community structure associated with protistan grazers. Arch Hydrobiol 145:25–38
Højberg O, Schnider U, Winteler HV, Sørensen J, Haas D (1999) Oxygen-sensing reporter strain of Pseudomonas fluorescens for monitoring the distribution of low-oxygen habitats in soil. Appl Environ Microbiol 65:4085–4093
Jousset A, Lara E, Wall LG, Valverde C (2006) Secondary metabolites help biocontrol strain Pseudomonas fluorescens CHA0 to escape protozoan grazing. Appl Environ Microbiol 72:7083–7090
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
Keel C, Schnider U, Maurhofer M, Voisard C, Laville J, Burger U, Wirthner P, Haas D, Défago G (1992) Suppression of root diseases by Pseudomonas fluorescens CHA0—importance of the bacterial secondary metabolite 2,4-diacetylphloroglucinol. Mol Plant-Microbe Interact 5:4–13
Koch B, Jensen LE, Nybroe O (2001) A panel of Tn7-based vectors for insertion of the gfp marker gene or for delivery of cloned DNA into Gram-negative bacteria at a neutral site. J Microbiol Meth 45:187–195
Koch TA, Ekelund F (2005) Strains of the heterotrophic flagellate Bodo designis from different environments vary considerably with respect to salinity preference and SSU rRNA gene composition. Protist 156:97–112
Laville J, Voisard C, Keel C, Maurhofer M, Defago G, Haas D (1992) Global control in Pseudomonas fluorescens mediating antibiotic synthesis and suppression of black root rot of tobacco. Proc Nat Acad Sci U S A 89:1562–1566
Lekfeldt JDS, 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
Manfield M, Whiteley A, Curtis T, Watanabe K (2007) Influence of sustainability and immigration in assembling bacterial populations of known size and function. Microb Ecol 53:348–354
Matz C, Kjelleberg S (2005) Off the hook—how bacteria survive protozoan grazing. Trends Microbiol 13:302–307
Matz C, Bergfeld T, Rice SA, Kjelleberg S (2004) Microcolonies, quorum sensing and cytotoxicity determine the survival of Pseudomonas aeruginosa biofilms exposed to protozoan grazing. Environ Microbiol 6:218–226
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
Mohapatra BR, Fukami K (2004) Comparison of the numerical grazing response of two marine heterotrophic nanoflagellates with different bacteria. J Sea Res 52:99–107
Page FC (1988) A New Key to Freshwater and Soil Gymnamoebae. Freshwater Biological Association, Ambleside
Rønn R, McCaig AE, Griffiths BS, Prosser JI (2002) Impact of protozoan grazing on bacterial community structure in soil microcosms. Appl Environ Microbiol 68:6094–6105
Rønn R, Grunert J, Ekelund F (2001) Protozoan response to addition of the bacteria Mycobacterium chlorophenolicum and Pseudomonas chlororaphis to soil microcosms. Biol Fertil Soil 33:126–131
Sørensen D, Nielsen TH, Christophersen C, Sørensen J, Gajhede M (2001) Cyclic lipoundecapeptide amphisin from Pseudomonas sp. strain DSS73. Acta Crystallogr 57:1123–1124
Van Elsas JD, Hill P, Chroňáková A, Grekova M, Topalova Y, Elhottová D, Krištůfeh V (2007) Survival of genetically marked Escherichia coli O157:H7 in soil as affected by soil microbial community shifts. ISME J 1:204–214
Weisskopf L, Fromin N, Tomasi N, Aragno M, Martinoia E (2005) Secretion activity of white lupins cluster roots influences bacterial abundance, function and community structure. Plant Soil 268:181–194
Vennette RC, Ferris H (1998) Influence of bacterial type and density on population of bacterial feeding nematodes. Soil Biol Biochem 7:949–960
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
Zhang Y, Lu H, Bargmann CI (2005) Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans. Nature 438:179–184
Acknowledgement
We thank Christoph Keel for providing the CHA0 strain. We are grateful to Ole Sjøholm and Marianne Schmidt for assistance on FCM and to Susanne Iversen for assistance with GFP-tagging of Pseudomonas fluorescens DSM50090. The manuscript has been improved, thanks to the constructive comments we have received from the anonymous reviewers. Lisa Bjørnlund and Annette Pedersen were supported by separate grants from the Danish Veterinary and Agricultural Research Council, grant no 23-04-0201 and 23-04-00089.
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Pedersen, A.L., Nybroe, O., Winding, A. et al. 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 (2009). https://doi.org/10.1007/s00248-008-9455-y
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DOI: https://doi.org/10.1007/s00248-008-9455-y