Skip to main content
SpringerLink
Log in

Is l-arabinose important for the endophytic lifestyle of Pseudomonas spp.?

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Twenty endophytic bacteria were isolated from surface-sterilized stems and roots of cucumber plants. After removal of potential siblings and human pathogens, the remaining seven strains were identified based on their 16S rDNA as Pseudomonas fluorescens (2 strains) and P. putida (5 strains). Three strains, namely P. fluorescens CS1, P. fluorescens CR2 and P. putida CR3, were able to suppress tomato foot and root rot (TFRR). Special attention was paid to the characterization of the BIOLOG carbon oxidation profiles of the isolated pseudomonads in order to identify nutrients which might be important for their endophytic lifestyle. Comparative analysis of the profiles of these seven strains with those of seven rhizospheric Pseudomonas spp. revealed that endophytes were able to oxidize l-arabinose and 2,3-butanediol significantly more often than the rhizospheric group. An independent growth experiment performed in tubes using l-arabinose and 2,3-butanediol as sole carbon sources showed the same results as seen using BIOLOG for l-arabinose, but not for 2,3-butanediol. Since l-arabinose is one of the most abundant sugars in xylem of cucumber plants and was not detected in their rhizosphere, our data suggest that utilization of l-arabinose might be a trait contributing to the endophytic lifestyle of the isolated Pseudomonas endophytes.

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

Fig. 1

Similar content being viewed by others

References

  • Anonymous (1998) Sichere Biotechnologie. Eingruppierung biologischer Agenzien: Bacterien, BG Chemie, Merkblatt B 006 8/98 ZH 1/346. Heidelberg, Germany: Jedermann-Verlag Dr Otto Pfeffer oHG

  • Bacon CW, Hinton DM (2006) Bacterial endophytes: the endophytic niche, its occupants, and its utility. In: Gnanamanickam SS (ed) Plant-associated bacteria. Springer, The Netherlands, pp 155–194

    Chapter  Google Scholar 

  • Belimov AA, Hontzeas N, Safronova VI, Demchinskaya SV, Piluzza G, Bullitta S, Glick BR (2005) Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biol Biochem 37:241–250

    Article  CAS  Google Scholar 

  • Berg G, Hallmann J (2006) Control of plant pathogenic fungi with bacterial endophytes. In: Schulz B, Boyle C, Sieber T (eds) Microbial root endophytes. Springer, Berlin, pp 53–69

    Chapter  Google Scholar 

  • Berg G, Krechel A, Ditz M, Sikora RA, Ulrich A, Hallmann J (2005) Endophytic and ectophytic potato-associated bacterial communities differ in structure and antagonistic function against plant pathogenic fungi. FEMS Microbiol Ecol 51:215–229

    Article  PubMed  CAS  Google Scholar 

  • Cho S, Lim W, Hong S et al (2003) Endophytic colonization of balloon flower by antifungal strain Bacillus sp. CY22. Biosci Biotech Biochem 67:2132–2138

    Article  CAS  Google Scholar 

  • Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678

    Article  CAS  Google Scholar 

  • Downing K, Thomson J (2000) Introduction of the Serratia marcescens chiA gene into an endophytic Pseudomonas fluorescens for the biocontrol of phytopathogenic fungi. Can J Microbiol 46:363–369

    PubMed  CAS  Google Scholar 

  • Egamberdiyeva D, Kamilova F, Validov S, Gafurova L, Kucharova Z, Lugtenberg B (2008) High incidence of plant growth-stimulating bacteria associated with the rhizosphere of wheat grown in salinated soil in Uzbekistan. Environ Microbiol 10:1–9

    Google Scholar 

  • Frankenberger WT, Chang AC, Arshad M (1990) Response of Raphanus sativus to the auxin precursor, l-tryptophan applied to soil. Plant Soil 129:235–241

    CAS  Google Scholar 

  • Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 251:1–7

    Article  PubMed  CAS  Google Scholar 

  • Hardoim PR, van Overbeek LS, Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471

    Article  PubMed  CAS  Google Scholar 

  • Iwai H, Usui M, Hoshino H, Kamada H, Matsunaga T, Kakegawa K, Ishii T, Satoh S (2003) Analysis of sugars in squash xylem sap. Plant Cell Physiol 44:582–587

    Article  PubMed  CAS  Google Scholar 

  • Kamilova F, Validov S, Azarova T, Mulders I, Lugtenberg B (2005) Enrichment for enhanced competitive root tip colonizers selects for a new class of biocontrol bacteria. Environ Microbiol 7:1809–1817

    Article  PubMed  CAS  Google Scholar 

  • Kamilova F, Kravchenko LV, Shaposhnikov AI, Azarova T, Makarova N, Lugtenberg BJJ (2006) Organic acids, sugars, and l-tryptophane in exudates of vegetables growing on stonewool and their effects on activities of rhizosphere bacteria. Mol Plant Microbe Interact 19:250–256

    Article  PubMed  CAS  Google Scholar 

  • Kravchenko LV, Azarova TS, Makarova NM, Tikhonovich IA (2004) The Effect of tryptophan present in plant root exudates on the phytostimulating activity of rhizobacteria. Microbiology 73:156–158

    Article  CAS  Google Scholar 

  • Long HH, Schmidt DD, Baldwin IT (2008) Native bacterial endophytes promote host growth in a species-specific manner; phytohormone manipulations do not result in common growth responses. PLoS ONE 3:e2702

    Article  PubMed  Google Scholar 

  • Lopez BR, Bashan Y, Bacilio M (2011) Endophytic bacteria of Mammillaria fraileana, an endemic rock-colonizing cactus of the southern Sonoran Desert. Arch Microbiol 193:527–541

    Article  PubMed  CAS  Google Scholar 

  • Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Ann Rev Microbiol 63:541–556

    Article  CAS  Google Scholar 

  • Malfanova N, Kamilova F, Validov S, Shcherbakov A, Chebotar V, Tikhonovich I, Lugtenberg B (2011) Characterization of Bacillus subtilis HC8, a novel plant-beneficial endophytic strain from giant hogweed. Microb Biotech 4:523–532

    Article  CAS  Google Scholar 

  • Mercado-Blanco J, Bakker PAHM (2007) Interactions between plants and beneficial Pseudomonas spp.: exploiting bacterial traits for crop protection. Antonie Van Leeuwenhoek 92:367–389

    Article  PubMed  Google Scholar 

  • Pedraza RO (2008) Recent advances in nitrogen-fixing acetic acid bacteria. Int J Food Microbiol 125:25–35

    Article  PubMed  CAS  Google Scholar 

  • Prakamhang J, Minamisawa K, Teamtaisong K, Boonkerd N, Teaumroong N (2009) The communities of endophytic diazotrophic bacteria in cultivated rice (Oryza sativa L.). Appl Soil Ecol 42:141–149

    Article  Google Scholar 

  • Ramesh R, Joshi AA, Ghanekar MP (2008) Pseudomonads: major antagonistic endophytic bacteria to suppress bacterial wilt pathogen, Ralstonia solanacearum in the eggplant (Solanum melongena L.). World J Microbiol Biotechnol 25:47–55

    Article  Google Scholar 

  • Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Pare PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Science (USA) 100:4927–4932

    Article  CAS  Google Scholar 

  • Sgroy V, Cassán F, Masciarelli O, Del Papa MF, Lagares A, Luna V (2009) Isolation and characterization of endophytic plant growth-promoting (PGPB) or stress homeostasis-regulating (PSHB) bacteria associated to the halophyte Prosopis strombulifera. Appl Microbiol Biotech 85:371–381

    Article  CAS  Google Scholar 

  • Simons M, van der Bij AJ, Brand I, de Weger LA, Wijffelman CA, Lugtenberg BJJ (1996) Gnotobiotic system for studying rhizosphere colonization by plant growth-pro- moting Pseudomonas bacteria. Mol Plant Microbe Interact 9:600–607

    Article  PubMed  CAS  Google Scholar 

  • Spaepen S, Dobbelaere S, Croonenborghs A, Vanderleyden J (2008) Effects of Azospirillum brasilense indole-3-acetic acid production on inoculated wheat plants. Plant Soil 312:15–23

    Article  CAS  Google Scholar 

  • Spaepen S, Vanderleyden J, Okon Y (2009) Plant Growth-promoting actions of rhizobacteria. In: van Loon LC (ed) Plant innate immunity. Elsevier, Amsterdam, pp 283–320

    Google Scholar 

  • Strobel G (2006) Muscodor albus and its biological promise. J Indust Microbiol Biotech 33:514–522

    Article  CAS  Google Scholar 

  • Sun Y, Cheng Z, Glick BR (2009) The presence of a 1-aminocyclopropane-1-carboxylate (ACC) deaminase deletion mutation alters the physiology of the endophytic plant growth-promoting bacterium Burkholderia phytofirmans PsJN. FEMS Microbiol Lett 296:131–136

    Article  PubMed  CAS  Google Scholar 

  • Taurian T, Anzuay MS, Angelini JG, Tonelli ML, Ludueña L, Pena D, Ibáñez F, Fabra A (2009) Phosphate-solubilizing peanut associated bacteria: screening for plant growth-promoting activities. Plant Soil 329:421–431

    Article  Google Scholar 

  • Validov S, Kamilova F, Qi S, Stephan D, Wang JJ, Makarova N, Lugtenberg B (2007) Selection of bacteria able to control Fusarium oxysporum f. sp. radicis lycopersici in stonewool substrate. J Appl Microbiol 102:461–471

    Article  PubMed  CAS  Google Scholar 

  • Validov SZ, Kamilova F, Lugtenberg BJJ (2009) Pseudomonas putida strain PCL1760 controls tomato foot and root rot in stonewool under industrial conditions in a certified greenhouse. Biol Control 48:6–11

    Article  Google Scholar 

  • Van Wees SCM, Van der Ent S, Pieterse CMJ (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11:443–448

    Article  PubMed  Google Scholar 

  • Yasuda M, Isawa T, Shinozaki S, Minamisawa K, Nakashita H (2009) Effects of colonization of a bacterial endophyte, Azospirillum sp. B510, on disease resistance in rice. Biosci Biotech Biochem 73:2595–2599

    Article  CAS  Google Scholar 

  • You M, Nishiguchi T, Saito A, Isawa T, Mitsui H, Minamisawa K (2005) Expression of the nifH gene of a Herbaspirillum endophyte in wild rice species: daily rhythm during the light–dark cycle. Appl Environ Microbiol 71:8183–8190

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The research described here was supported by the Netherlands Organization for Scientific research (NWO, project number 047.018.001) and represents part of the Russian-Dutch collaboration project “Center of Excellence”. We thank Dr. Bernadette Kroon (Syngenta B.V., Enkhuizen, the Netherlands) for providing us with tomato and cucumber seeds. We thank Gerben Voshol for his help in some experiments and for critically reading the manuscript.

Author information

Author notes

  1. Faina Kamilova

    Present address: Koppert Biological Systems, Veilingweg 14, P.O.Box 155, 2650 AD, Berkel en Rodenrijs, The Netherlands

  2. Shamil Validov

    Present address: Federal Centre of Toxicology, Radiation and Biological Security, Nauchny Gorodok, 2, 420075, Kazan, Tatarstan Republic, Russia

Authors and Affiliations

  1. Institute of Biology, Sylvius Laboratory, Leiden University, Sylviusweg 72, 2333 BE, Leiden, The Netherlands

    Natalia Malfanova, Faina Kamilova, Shamil Validov & Ben Lugtenberg

  2. All-Russian Research Institute for Agricultural Microbiology (ARRIAM), Pushkin, Saint-Petersburg, Russia

    Natalia Malfanova & Vladimir Chebotar

Authors
  1. Natalia Malfanova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Faina Kamilova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shamil Validov
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Vladimir Chebotar
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ben Lugtenberg
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Natalia Malfanova.

Additional information

Communicated by Theo Hansen.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 42 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Malfanova, N., Kamilova, F., Validov, S. et al. Is l-arabinose important for the endophytic lifestyle of Pseudomonas spp.?. Arch Microbiol 195, 9–17 (2013). https://doi.org/10.1007/s00203-012-0842-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-012-0842-x

Keywords

Search

Navigation