Skip to main content
SpringerLink
Log in

Monitoring temporal and spatial variation in rhizosphere bacterial population diversity: A community approach for the improved selection of rhizosphere competent bacteria

  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

The potential for developing a reliable strategy for selecting rhizosphere competent bacteria, based on an improved understanding of the community diversity and population dynamics of fluorescent pseudomonads, was investigated. Isolates from a collection of over 690 fluorescent pseudomonads, obtained from sugar beet and wheat plants grown in field soils in laboratory microcosms, were genotypically and phenotypically characterised. RFLP rRNA analysis (ribotyping) revealed that the sampled population was composed of 385 related but distinct ribotypes. Most ribotypes were isolated only once and represented a transient colonising population. However, representatives of 26 ribotypes were detected more often, of which five were isolated from rhizosphere soils sampled 7 months after the first sampling. Comparative phenotypic analysis of isolates (motility, antibiotic resistance and production, adherence, fatty acid composition, substrate utilisation patterns) demonstrated that the ability to utilise organic acids as carbon sources correlated with rhizosphere competence. Single inoculum and competitive colonisation studies in planted microcosms confirmed rhizosphere competence, but also demonstrated synergistic interactions. The colonisation ability and population densities of transient strains were significantly increased when co-inoculated with rhizosphere competent isolates. These data demonstrate potential cross-feeding and combined niche exploitation, rather than direct competition, confirming the multi-factorial nature of rhizosphere competence in diverse fluorescent pseudomonad communities. They also highlight the need to consider the use of mixed inocula for plant growth promotion and the systematic selection of strains for effective biotechnological exploitation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Bakker P A H M, Raaymakers J M and Schippers B 1993 Role of iron in the suppression of bacterial plant pathogens by fluorescent pseudomonads. In Iron Chelation in Plants and Soil Microorganisms. Eds. LL Barton and BC Hemmings. pp 269–281. San Diego: Academic Press.

    Google Scholar 

  • Bailey M J, Lilley A K, Thompson I P, Rainey R B and Ellis R J 1995 Site-directed chromosomal marking of a fluorescent pseudomonad isolated from the phytosphere of sugar beet: Stability and potential for marker gene transfer. Mol. Ecol. 4, 755–763.

    Google Scholar 

  • Bangera M G and Thomashow L S 1996 Characterization of a genomic locus required for synthesis of the antibiotic 2,4-diacetylphloroglucinol by the biological control agent Pseudomonas fluoresces Q2-87. Mol. Plant-Microbe Interact. 9, 83–90.

    Google Scholar 

  • Crowley D E, Brennerova M V, Irwin C, Brenner V and Focht D D 1996 Rhizosphere effects on biodegradation of 2,5-dichlorobenzoate by a bioluminescent strain of root-colonising Pseudomonas fluorescens. FEMS Microbiol. Ecol. 20, 79–89.

    Google Scholar 

  • De Weger L A, van der Vlugt C I M, Wijfjes A H M, Baker P A H M, Schipper B, Lugtenberg B J J 1987 Flagella of a plantgrowth-stimulating Pseudomonas fluorescens strain are required for colonization of potato roots. J. Bacteriol. 169, 2769–2773.

    Google Scholar 

  • De Weger L A, Bakker P A H M, Schippers B, Van Loosddrecht MC Mand Lugtenberg B J J 1989 Pseudomonas spp. with mutational changes in the O-antigenic side chain of their lipopolysaccharide are affected in their ability to colonise potato roots. NATO ASI series 36. Ed. BJJ Lugtenberg. pp 197–202. Springer Verlag, Berlin.

    Google Scholar 

  • Di Cello F, Bevivino A, Chiarini L, Fani R, Paffetti D, Tabacchioni M and Dalmastri C 1997 Biodiversity of a Burkholderia cepacia population isolated from the maize rhizosphere at different plant growth stages. Appl. Environ. Microbiol. 11, 4485–4493.

    Google Scholar 

  • Ellis R J, Thompson I P, Bailey M J 1995 Metabolic profiling as a means of characterising plant-associated microbial communities. FEMS Microbiol. Ecol. 16, 9–18.

    Google Scholar 

  • Ellis R J, Thompson I P and Bailey M J 1999 Temporal fluctuations in the pseudomonad population associated with sugar beet leaves. FEMS Microbiol. Ecol. 28, 345–356.

    Google Scholar 

  • Ellis R J, Timms-Wilson T M and Bailey M J 2000 Identification of conserved traits in fluorescent pseudomonads with anti-fungal activity. Environ. Microbiol. 2, 274–284.

    Google Scholar 

  • Fenton A M, Stephens P M, Crowley J, O'Callaghan M and O'Gara F 1992 Exploitation of gene(s) involved in 2,4-diacetylphloroglucinol biosynthesis to confer a new biocontrol capability to a Pseudomonas strain. Appl. Environ. Microbiol. 58, 3873–3878.

    Google Scholar 

  • Glandorf D C M, Peters L G I, Van Der Sluis I, Bakker P A H M and Schippers B 1993 Crop specificity of rhizosphere pseudomonads and the involvement of root agglutins. Soil Biol. Biochem. 25, 981–989.

    Google Scholar 

  • Grewal S I S and Rainey P B 1991 Phenotypic variation of Pseudomonas putida and P. tolaasii affects the chemotactic response to Agaricus bisporus mycelial exudate. J. Gen. Micro. 137, 2761–2768.

    Google Scholar 

  • Handelsmann J and Stabb E V 1996 Biocontrol of soil borne plant pathogens. Plant Cell. 8, 1855–1869.

    Google Scholar 

  • Herrero M, De Lorenzo V and Timmis K N 1990 Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in Gram-negative bacteria. J. Bacteriol. 172, 6557–6567.

    Google Scholar 

  • Latour X, Corberand T, Laguerre G and Lemanceau P 1996 The composition of fluorescent pseudomonad populations associated with roots is influenced by plant and soil type. Appl. Environ. Microbiol. 62, 2449–2456.

    Google Scholar 

  • Lemanceau P, Corberand T, Gardan L, Latour X, Laguerre G, Boeufgras J-M and Alabouvette C 1995 Effect of two plant species, flax (Linum usitatissinum L.) and tomato (Lycopersicon esculentum Mill.) on the diversity of soil borne populations of fluorescent pseudomonads. Appl. Environ. Microbiol. 61, 1004–1012.

    Google Scholar 

  • Lugtenberg B J and Dekker L C 1999 What makes Pseudomonas bacteria rhizosphere competent? Environ. Microbiol. 1, 9–13.

    Google Scholar 

  • Mazzola M, Cook R J, Thomashow L S, Weller D M and Pierson L S 1992 Contribution of phenazine antibiotic biosynthesis to the ecological competence of fluorescent pseudomonads in soil habitats. Appl. Environ. Microbiol. 58, 2616–2624.

    Google Scholar 

  • McClure N C, Fry J C and Weightman A J 1991 Survival and catabolic activity of natural and genetically engineered bacteria in a laboratory-scale activated-sludge unit. Appl. Environ. Microbiol. 57, 366–373.

    Google Scholar 

  • Oresnik I J, Pacarynuk L A, O'Brien S A P, Yost C K and Hynes M F 1998 Plasmid-encoded catabolic genes in Rhizobium leguminosarum bv. Trifolii: evidence for a plant-inducible rhamnose locus involves in competition for nodulation. Mol Plant Microbe Interact 11, 1175–1185.

    Google Scholar 

  • Osburn R M, Schroth M N, Hancock J G and Hendson M 1989 Dynamics of sugar beet seed colonization by Pythium ultimum and Pseudomonas species: effects on seed rot and damping-off. Phytopath. 79, 709–716.

    Google Scholar 

  • Pierson E A and Weller D M 1994 Use of mixtures of fluorescent pseudomonads to suppress take-all and improve the growth of wheat. Phytopathology 84, 841–947.

    Google Scholar 

  • Rainey P B, Bailey M J and Thompson I P 1994 Phenotypic and genotypic diversity of fluorescent pseudomonads isolated from the phyllosphere of field-grown sugar beet. Microbiology (UK) 140, 2315–2331.

    Google Scholar 

  • Rainey P B and Bailey M J 1996 Physical and genetic map of the Pseudomonas fluorescens SBW25 chromosome. Mol. Microbiol. 19, 521–533.

    Google Scholar 

  • Rainey P B 1999 Adaptation of Pseudomonas fluorescens to the plant rhizosphere. Environ. Microbiol. 1, 243–257.

    Google Scholar 

  • Ripp S, Nivens D E, Ahn Y, Werner C, Jarrell J, Easter J P, Cox C D, Burlage R S and Sayler G S 2000 Controlled field release of a bioluminescent genetically engineered micro-organism for bioremediation process monitoring and control. Environ. Sci. Technol. 34, 846–853.

    Google Scholar 

  • Rohlf and Sokal 1994 Statistical Tables F. James Rohlf, Robert R. Sokal 3rd edition. NY: W H Freeman & Co.

    Google Scholar 

  • Rovira A D 1969 Plant root exudates. Botan. Rev. 35, 35–57.

    Google Scholar 

  • Sambrook J, Fritsch E F and Manniatis T 1989 Molecular Cloning: A Laboratory Manual. Cold Spring Harbour, NY: Cold Spring Harbour Laboratory Press.

    Google Scholar 

  • Schnider U, Keel C, Blumer C, Troxler J, Defago G and Haas D 1995 Amplification of the housekeeping sigma factor in Pseudomonas fluorescens CHA0 enhances antibiotic production and improves biocontrol abilities. J. Bacteriol. 177, 5387–5392.

    Google Scholar 

  • Simons M, Van Der Bij A J, Brand I, De Weger L A, Wijffelman C A and Lugtenberg B J J 1996 Gnotobiotic systems for rhizosphere colonisation by plant-promoting Pseudomonas bacteria. Mol. Plant-Microbe. Interact. 9, 600–607.

    Google Scholar 

  • Simons M, Permentier H J, De Weger L A, Wijffelman C A and Lugtenberg B J J 1997 Amino acid synthesis is necessary for tomato root colonisation by Pseudomonas fluorescens strain WCS365. Mol. Plant-Microbe. Interact. 10, 102–106.

    Google Scholar 

  • Tchelet R, Meckenstock P, Steinle P and Van Der Meer J R 1999 Population dynamics of an introduced bacterium degrading chlorinated benezenes in a soil column and in sewage sludge. Biodegrad. 10,13–125.

    Google Scholar 

  • Thompson I P, Bailey M J, Ellis R J and Purdy K J 1993 Sub grouping of bacterial populations by cellular fatty acid composition. FEMS Microbiol. Ecol. 102: 75–84.

    Google Scholar 

  • Thompson I P, Bailey M J, Ellis R J, Maguire N and Meharg A 1999 Response of soil microbial communities to single and multiple doses of an organic pollutant. Soil Biol. Biochem. 31, 95–105.

    Google Scholar 

  • Timms-Wilson T M, Ellis R J and Bailey M J 2000a Immunocapture differential display method (IDDM) for the detection of environmentally induced promoters in rhizobacteria. J. Microbiol. Methods. 41, 77–84.

    Google Scholar 

  • Timms-Wilson T M, Ellis R J, Renwick A, Rhodes D J, Weller D M, Mavrodi D V, Thomashow L S and Bailey M J 2000b Chromosomal insertion of the phenazine biosynthetic pathway (phzABCDEFG) enhances the efficacy of damping off disease control by Pseudomonas fluorescens. Mol. Plant-Microbe. Interact. 13, 1293–1300.

    Google Scholar 

  • Weller D M and Cook R J 1983 Suppression of take-all of wheat by fluorescent pseudomonads. Phytopathology 73, 463–469.

    Google Scholar 

  • Weller DM 1988 Biological control of soil borne plant pathogens in the rhizosphere with bacteria. Ann. Rev. Phytopath. 26, 379–407.

    Google Scholar 

Download references

Author information

Author notes

  1. V.J Goddard

    Present address: NERC, Plymouth Marine Laboratory, Plymouth, UK

Authors and Affiliations

  1. Natural Environment Research Council, Centre for Ecology and Hydrology Oxford, Oxford, OX1 3SR, UK

    V.J Goddard, M.J. Bailey, A.K. Lilley & I.P. Thompson

  2. Department of Plant Sciences, University of Oxford, Oxford, UK

    P. Darrah

Authors
  1. V.J Goddard
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M.J. Bailey
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. Darrah
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A.K. Lilley
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. I.P. Thompson
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Goddard, V., Bailey, M., Darrah, P. et al. Monitoring temporal and spatial variation in rhizosphere bacterial population diversity: A community approach for the improved selection of rhizosphere competent bacteria. Plant and Soil 232, 181–193 (2001). https://doi.org/10.1023/A:1010302607616

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1010302607616

Search

Navigation