Symbiotic Plant–Microbe Interactions: Stress Protection, Plant Growth Promotion, and Biocontrol by Stenotrophomonas

  • Gabriele BergEmail author
  • Dilfuza Egamberdieva
  • Ben Lugtenberg
  • Martin Hagemann
Part of the Cellular Origin, Life in Extreme Habitats and Astrobiology book series (COLE, volume 17)


The genus Stenotrophomonas is[COMP16] phylogenetically placed[COMP17] in the γ-subclass of Proteobacteria (Moore et al., 1997). The genus was first described with the type species Stenotrophomonas maltophilia (Palleroni and Bradbury, 1993), previously called Pseudomonas maltophilia (Hugh and Ryschenko, 1961) and later changed to Xanthomonas maltophilia (Swings et al., 1983). Actually, the genus comprises eight validly described species: S. maltophilia, S. nitritireducens (Finkmann et al., 2000), S. rhizophila (Wolf et al., 2002), S. acidaminophila (Assih et al., 2002), S. koreensis (Yang et al., 2006), S. terrae, S. humi (Heylen et al., 2007), and S. chelatiphaga (Kaparullina et al., 2009). However, pheno- and genotypic studies revealed much more differentiation at species level (Ryan et al., 2009). Only two species, S. maltophilia and S. rhizophila (Wolf et al., 2002), show a strong association with plant hosts. In comparison with S. maltophilia, the defining phenotypic characteristics of S. rhizophila are: growth at 4°C and no growth at 40°C; the utilization of xylose as a carbon source; higher osmotic tolerance (<5% NaCl [w/v]); and the absence of lipase and β-glucosidase production (Wolf et al., 2002). Both species produce osmoprotective substances (Roder et al., 2005). These are compounds compatible at very high internal concentrations with cellular functions, e.g., DNA replication, DNA–protein interactions, and cellular metabolism; they regulate the osmotic balance and are effective ­stabilizers of enzymes (Welsh, 2000). A molecular protocol was developed for the differentiation of the two Stenotrophomonas species. It targets specifically the ggpS gene responsible for glucosylglycerol (GG) synthesis because this marker occurs only in S. rhizophila strains and was absent from all S. maltophilia isolates ­(Ribbeck-Busch et al., 2005). As a further genetic marker the smeD gene was used, which is part of the operon coding for the multi-drug efflux pump SmeDEF only occurring in S. maltophilia (Alonso and Martinez, 2000).


Salt Stress Compatible Solute Rhizoctonia Solani Stenotrophomonas Maltophilia Marram Grass 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Gabriele Berg would like to thank all the students, who were involved in Stenotrophomonas research: Petra Marten, Jana Monk, Ivonne Suckstorff, Anja Roder, Kathrin Ribbeck-Busch, Dirk Hasse (Rostock), and Doris Zahrl (Graz). The research was supported by the Deutsche Forschungsgemeinschaft, the Austrian Science Foundation FWF and by the INTAS project 04-82-6969.


  1. Alonso, A. and Martinez, J.L. (1997) Multiple resistance in Stenotrophomonas maltophilia. Antimicrob. Agents Chemother. 41: 140–1142.Google Scholar
  2. Alonso, A. and Martinez, J.L. (2000) Cloning and characterization of SmeDEF, a novel ­multidrug efflux pump from Stenotrophomonas maltophilia. Antimicrob. Agents Chemother. 44: 3079–3086.PubMedCrossRefGoogle Scholar
  3. Alonso, A. and Martinez, J.L. (2001) Expression of multidrug efflux pump SmeDEF by clinical ­isolates of Stenotrophomonas maltophilia. Antimicrob. Agents Chemother. 45: 1879–1881.CrossRefGoogle Scholar
  4. Assih, E.A., Ouattara, A.S., Thierry, S., Cayol, J.L., Labat, M. and Macarie, H. (2002) Stenotrophomonas acidaminiphila sp. nov., a strictly aerobic bacterium isolated from an upflow anaerobic sludge blanket (UASB) reactor. Int. J. Syst. Evol. Microbiol. 52: 559–568.PubMedGoogle Scholar
  5. Barac, T., Taghavi, S., Borremans, B., Provoost, A., Oeyen, L., Colpaert, J.V., Vangronsveld, J. and van der Lelie, D. (2004) Engineered endophytic bacteria improve phytoremediation of water-soluble, volatile, organic pollutants. Nat. Biotechnol. 22: 583–588.PubMedCrossRefGoogle Scholar
  6. Bais H.P., Weir, T.L., Perry, L.G., Gilroy, S. and Vivanco, J.M. (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Ann. Rev. Plant Biol. 57: 234–266.CrossRefGoogle Scholar
  7. Bharadwaj, D.P., Lundquist, P.O., Persson, P. and Alström, S. (2008) Evidence for specificity of cultivable bacteria associated with arbuscular mycorrhizal fungal spores. FEMS Microbiol. Ecol. 65: 310–322.PubMedCrossRefGoogle Scholar
  8. Berg, G., Knaape, C., Ballin, G. and Seidel, D. (1994) Biological control of Verticillium dahliae KLEB by naturally occurring rhizosphere bacteria. Arch. Phytopathol. Dis. Prot. 29: 249–262.CrossRefGoogle Scholar
  9. Berg, G., Marten, P. and Ballin, G. (1996) Stenotrophomonas maltophilia in the rhizosphere of oilseed rape – occurrence, characterization and interaction with phytopathogenic fungi. Microbiol. Res. 151: 19–27.CrossRefGoogle Scholar
  10. Berg, G., Roskot, N. and Smalla, K. (1999) Genotypic and phenotypic relationships between clinical and environmental isolates of Stenotrophomonas maltophilia. J. Clin. Microbiol. 37: 3594–3600.PubMedGoogle Scholar
  11. Berg, G., Roskot, N., Steidle, A., Eberl, L., Zock, A. and Smalla, K. (2002) Plant-dependent genotypic and phenotypic diversity of antagonistic rhizobacteria isolated from different Verticillium host plants. Appl. Environ. Microbiol. 68: 3328–3338.PubMedCrossRefGoogle Scholar
  12. Berg, G., Eberl, L. and Hartmann, A. (2005) The rhizosphere as a reservoir for opportunistic human pathogenic bacteria. Environ. Microbiol. 7: 1673–1685.PubMedCrossRefGoogle Scholar
  13. Bloemberg, G.V. and Lugtenberg, B.J.J. (2001) Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr. Opin. Plant Biol. 4: 443–350.CrossRefGoogle Scholar
  14. Chatelut, M., Dournes, J. L., Chabanon, G. and Marty, N. (1995) Epidemiological typing of Stenotrophomonas (Xanthomonas) maltophilia by PCR. J. Clin. Microbiol. 33: 912–914.PubMedGoogle Scholar
  15. Chernin, L. and Chet, I. (2002) Microbial enzymes in biocontrol of plant pathogens and pests, In: R. Burns and R. Dick (eds.) Enzymes in the Environment. Marcel Dekker, New York, pp. 171–225.Google Scholar
  16. Crossman, L.C., Gould, V.C., Dow, J.M., Vernikos, G.S., Okazaki, A., Sebaihia, M., Saunders, D., Arrowsmith, C., Carver, T., Peters, N., Adlem, E., Kerhornou, A., Lord, A., Murphy, L., Seeger, K., Squares, R., Rutter, S., Quail, M.A., Rajandream, M.A., Harris, D., Churcher, C., Bentley, S.D., Parkhill, J., Thomson, N.R., and Avison M.B. (2008) The complete genome, comparative and functional analysis of Stenotrophomonas maltophilia reveals an organism heavily shielded by drug resistance determinants. Genome Biol. 9: 74–81.CrossRefGoogle Scholar
  17. Debette, J. (1991) Isolation and characterization of an extracellular proteinase produced by a soil strain of Xanthomonas maltophilia. Curr. Microbiol. 22: 85–90.CrossRefGoogle Scholar
  18. Denton, M. and Kerr, K.G. (1998) Microbiological and clinical aspects of infections associated with Stenotrophomonas maltophilia. Clin. Microbiol. Rev. 11: 7–80.Google Scholar
  19. De Boer, W., Klein Gunnewiek, P.J., Kowalchuk, G.A. and Van Veen, J.A. (2001) Growth of chitinolytic dune soil beta-subclass Proteobacteria in response to invading fungal hyphae. Appl. Environ. Microbiol. 67: 3358–3362.PubMedCrossRefGoogle Scholar
  20. Dunne, C., Moënne-Loccoz, Y., de Bruijn F.J. and O´Gara, F. (2000) Overproduction of an inducile extracellular serine protease improves biological control of Pythium ultimum by Stenotrophomonas maltophilia strain W81. Microbiology 146: 2069–2078.PubMedGoogle Scholar
  21. Elad, Y., Chet, I. and Baker, R. (1987) Increased growth response of plants induced by rhizobacteria antagonistic to soilborne pathogenic fungi. Plant and Soil 98: 325–339.CrossRefGoogle Scholar
  22. Finkmann, W., Altendorf, K., Stackebrandt, E. and Lipski, A. (2000) Characterization of N2O-­producing Xanthomonas-like isolates from biofilters as Stenotrophomonas nitritireducens sp. nov., Luteimonas mephitis gen. nov., sp. nov. and Pseudoxanthomonas broegbernensis gen. nov., sp. nov. Int. J. Syst. Evol. Microbiol. 50: 273–282.PubMedCrossRefGoogle Scholar
  23. Fouhy, Y., Scanlon, K., Schouest, K., Spillane, C., Crossman, L., Avison, M.B., Ryan, R.P. and Dow, J.M. (2007) Diffusible signal factor-dependent cell-cell signaling and virulence in the nosocomial pathogen Stenotrophomonas maltophilia. J. Bacteriol. 189: 4964–4968.PubMedCrossRefGoogle Scholar
  24. Garbeva, P., Overbeek, L.S., Vuurde, J.W. and Elsas, J.D. (2001) Analysis of endophytic bacterial communities of potato by plating and Denaturing Gradient Gel Electrophoresis (DGGE) of 16S rDNA based PCR Fragments. Microb. Ecol. 41: 369–383.PubMedGoogle Scholar
  25. Galai, S., Limam, F. and Marzouki, M.N. (2008) A new Stenotrophomonas maltophilia strain producing laccase use in decolorization of synthetics dyes. Appl. Biochem. Biotechnol. [Epub ahead of print]Google Scholar
  26. Gerner-Smidt, P., Bruun, B., Arpi, M. and Schmidt, J. (1995) Diversity of nosocomial Xanthomonas maltophilia (Stenotrophomonas maltophilia) as determined by ribotyping. Eur. J. Clin. Microbiol. Infect. Dis. 14: 137–140.PubMedCrossRefGoogle Scholar
  27. Hallmann, J. and Berg, G. (2006) Spectrum and population dynamics of root endophytes, In: B. Schulz, C. Boyle and T. Sieber (eds.) Microbial Root Endophytes. Springer Verlag, Berlin/Heidelberg/New York, pp. 15–32.CrossRefGoogle Scholar
  28. Hagemann, M., Hasse, D. and Berg, G. (2006) Detection of a phage genome carrying a zonula occludens like toxin gene (zot) in clinical isolates of Stenotrophomonas maltophilia. Arch. Microbiol. 185: 449–458.PubMedCrossRefGoogle Scholar
  29. Hagemann, M., Ribbeck-Busch, K., Klähn, S., Hasse, D., Steinbruch, R. and Berg, G. (2008) The plant-associated bacterium Stenotrophomonas rhizophila expresses a new enzyme for the synthesis of the compatible solute glucosylglycerol. J. Bacteriol. 190: 5898–5906.PubMedCrossRefGoogle Scholar
  30. Hauben, L., Vauterin, L., Moore, E.R.B., Hoste, M. and Swings, J. (1999) Genomic diversity of the genus Stenotrophomonas. Int. J. Syst. Bacteriol. 49: 1749–1760.PubMedCrossRefGoogle Scholar
  31. Heylen, K., Vanparys, B., Peirsegaele, F., Lebbe, L., and De Vos, P. (2007) Stenotrophomonas terrae sp. nov. and Stenotrophomonas humi sp. nov., two nitrate-reducing bacteria isolated from soil. Int. J. Syst. Evol. Microbiol. 57: 2056–2061.PubMedCrossRefGoogle Scholar
  32. Hiltner, L. (1904) Über neuere Erfahrungen und Probleme auf dem Gebiete der Bodenbakteriologie unter bessonderer Berücksichtigung der Gründung und Brache. Arb. Dtsch. Landwirtsch. Ges. Berl. 98: 59–78.Google Scholar
  33. Hugh, R. and Ryschenko, E. (1961) Pseudomonas maltophilia, an Alcaligenes like species. J. Gen. Microbiol. 26: 123–132.PubMedGoogle Scholar
  34. Ikemoto, S., Suzuki, K., Kaneko, T. and Komagata, K. (1980) Characterization of strains of Pseudomonas maltophilia which do not require methionine. Int. J. Syst. Bacteriol. 30: 437–447.CrossRefGoogle Scholar
  35. Ingram, L.O. and Buttke, T.M. (1984) Effects of alcohols on micro-organisms. Adv. Microb. Physiol. 25: 253–300.PubMedCrossRefGoogle Scholar
  36. Jacobi, M., Kaiser, D., Berg, G., Jung, G., Winkelmann, G. and Bahl, H. (1996) Maltophilin – a new antifungal compound produced by Stenotrophomomas maltophilia R3089. J. Antib. 49: 1101–1104.CrossRefGoogle Scholar
  37. Juhnke, M. E. and Des Jardin, E. (1989) Selective medium for isolation of Xanthomonas maltophilia from soil and rhizosphere Environments. Appl. Environ. Microbiol. 55: 747–750.PubMedGoogle Scholar
  38. Jurkevitch, E., Hadar, Y. and Chen, Y. (1992) Differential siderophore utilization and iron uptake by soil and rhizosphere bacteria. Appl. Environ. Microbiol. 58: 119–124.PubMedGoogle Scholar
  39. Kai, M., Effmert, U., Berg, G. and Piechulla, B. (2007) Volatiles of bacterial antagonists inhibit mycelial growth of the plant pathogen Rhizoctonia solani. Arch. Microbiol. 187: 351–360.PubMedCrossRefGoogle Scholar
  40. Kan, F.L., Chen, Z.Y., Wang, E.T., Tian, C.F., Sui, X.H. and Chen, W.X. (2007) Characterization of symbiotic and endophytic bacteria isolated from root nodules of herbaceous legumes grown in Qinghai-Tibet plateau and in other zones of China. Arch. Microbiol. 188: 103–115.PubMedCrossRefGoogle Scholar
  41. Kaparullina, E., Doronina, N., Chistyakova, T. and Trotsenko, Y. (2009) Stenotrophomonas chelatiphaga sp. nov., a new aerobic EDTA-degrading bacterium. Syst. Appl. Microbiol. 32: 157–162.PubMedCrossRefGoogle Scholar
  42. Kataoka, D., Fujiwara, H., Tanimoto, A., Ikawa, S. and Tanaka, Y. (2003) The differential ­beta-lactamase activity of Stenotrophomonas maltophilia. J. Hosp. Infect. 54: 247–248.PubMedCrossRefGoogle Scholar
  43. Kloepper, J.W. (1992) Plant growth-promoting rhizobacteria as biological control agents, In: F.B. ­Metting Jr. (ed.) Soil Microbial Ecology: Applications in Agricultural and Environmental Management. Marcel Dekker, New York, pp. 255–274.Google Scholar
  44. Krechel, A., Faupel, A., Hallmann, J., Ulrich, A. and Berg, G. (2002) Potato-associated bacteria and their antagonistic potential towards plant pathogenic fungi and the plant parasitic nematode Meloidogyne incognita (Kofoid & White) Chitwood. Can. J. Microbiol. 48: 772–786.PubMedCrossRefGoogle Scholar
  45. Krimm, U., Abanda-Nkpwatt D., Schwab, W. and Schreiber, L. (2005) Epiphytic microorganisms on strawberry plants (Fragaria ananassa cv. Elsanta): identification of bacterial isolates and analysis of their interaction with leaf surfaces. FEMS Microbiol. Ecol. 53: 483–492.PubMedCrossRefGoogle Scholar
  46. Kobayashi, D.Y., Gugliemoni, M. and Clarke, B.B. (1995) Isolation of chitinolytic bacteria Xanthomonas maltophilia and Serratia marcescens as biological control agents for summer patch disease of turf grass. Soil Biol. Biochem. 27: 1479–1487.CrossRefGoogle Scholar
  47. Kwok, O.C.H., Fahy, P.C., Hoitink, H.A.J. and Kuter, G.A. (1987) Interactions between bacteria and Trichoderma hamatum in suppression of Rhizoctonia damping-off in bark compost media. Phytopathology 77: 1206–1212.CrossRefGoogle Scholar
  48. Lambert, T., Ploy, M.C., Denis, F. and Courvalin, P. (1999) Characterization of the chromosomal aac(6’)-Iz gene of Stenotrophomonas maltophilia. Antimicrob. Agents Chemother. 43: 2366–2371.PubMedGoogle Scholar
  49. Li, X.Z., Zhang, L. and Poole, K. (2002) SmeC, an outer membrane multidrug efflux protein of Stenotrophomonas maltophilia. Antimicrob. Agents Chemother. 46: 333–343.PubMedCrossRefGoogle Scholar
  50. Li, X.Z., Zhang, L., McKay, G.A. and Poole, K. (2003) Role of the acetyltransferase AAC(6’)-Iz modifying enzyme in aminoglycoside resistance in Stenotrophomonas maltophilia. J. Antimicrob. Chemother. 51: 803–811.PubMedCrossRefGoogle Scholar
  51. Liba, C.M., Ferrara, F.I., Manfio, G.P., Fantinatti-Garboggini, F., Albuquerque, R.C., Pavan, C., Ramos, P.L., Moreira-Filho, C.A. and Barbosa, H.R. (2006) Nitrogen-fixing chemo-­organotrophic bacteria isolated from cyanobacteria-deprived lichens and their ability to solubilize phosphate and to release amino acids and phytohormones. J. Appl. Microbiol. 101: 1076–1086.PubMedCrossRefGoogle Scholar
  52. Lockhart, S.R., Abramson, M.A., Beekmann, S.E., Gallagher, G., Riedel, S., Diekema, D.J., Quinn, J.P. and Doern, G.V. (2007) Antimicrobial resistance among Gram-negative bacilli causing infections in intensive care unit patients in the United States between 1993 and 2004. J. Clin. Microbiol. 45: 3352–3359.PubMedCrossRefGoogle Scholar
  53. Lugtenberg, B.J.J. and Dekkers, L.C. (1999) What makes Pseudomonas bacteria rhizosphere competent? Environ. Microbiol. 1:9–13.PubMedCrossRefGoogle Scholar
  54. Lugtenberg, B.J.J., Dekkers, L.C. and Bloemberg, G.V. (2001) Molecular determinants of rhizosphere colonization by Pseudomonas. Annu. Rev. Phytopathol. 39: 461–490.PubMedCrossRefGoogle Scholar
  55. Marecik, R., Króliczak, P., Czaczyk, K., Białas, W., Olejnik, A., and Cyplik, P. (2008) Atrazine ­degradation by aerobic microorganisms isolated from the rhizosphere of sweet flag (Acorus ­calamus L.). Biodegradation 19: 293–301.PubMedCrossRefGoogle Scholar
  56. Messiha, N.A.S., van Diepeningen, A.D., Farag, N. S., Abdallah, S.A., Janse, J.D. and van Bruggen, A.H.C. (2007) Stenotrophomonas maltophilia: a new potential biocontrol agent of Ralstonia solanacearum, causal agent of potato brown rot. Eur. J. Plant Pathol. 118: 211–225.CrossRefGoogle Scholar
  57. Minerdi, D., Moretti, M., Gilardi, G., Barberio, C., Gullino, M.L., and Garibaldi, A. (2008) Bacterial ectosymbionts and virulence silencing in a Fusarium oxysporum strain. Environ. Microbiol. 10: 1725–1741.PubMedCrossRefGoogle Scholar
  58. Minkwitz, A. and Berg, G. (2001) Comparison of antifungal activities and 16S ribisomal DNA sequences of clinical and environmental isolates of Stenotrophomonas maltophilia. J. Clin. Microbiol. 39: 139–145.PubMedCrossRefGoogle Scholar
  59. Moore, E., Krüger, A., Hauben, L., Seal, S., De Baere, R., De Wachter, K., Timmis, K. and Swings, J. (1997) 16S rRNA gene sequence analyses and inter- and intrageneric relationship of Xanthomonas species and Stenotrophomonas maltophilia. FEMS Microbiol. Lett. 151: 145–153.PubMedCrossRefGoogle Scholar
  60. Miller, K.J. and Wood, J.M. (1996) Osmoadaption by rhizosphere bacteria. Ann. Rev. Microbiol. 50: 101–136.CrossRefGoogle Scholar
  61. Nakayama, T., Homma, Y., Hashidoko, Y., Mitzutani, J. and Tahara, S. (1999a) Possible role of ­xanthobaccins produced by Stenotrophomonas sp. strain SB-K88 in suppression of sugar beet damping-off disease. Appl. Environ. Microbiol. 65: 4334–4339.PubMedGoogle Scholar
  62. Nakayama, T., Homma, Y., Hashidoko, Y., Mitzutani, J. and Tahara, S. (1999b) Possible role of ­xanthobaccins produced by Stenotrophomonas sp. strain SB-K88 in suppression of sugar beet damping-off disease. Appl. Environ. Microbiol. 65: 4334–4339.PubMedGoogle Scholar
  63. Nesme, X., Vaneechoutte, M., Orso, S., Hoste, B. and Swings, J. (1995) Diversity and genetic relatedness within genera Xanthomonas and Stenotrophomonas using restriction endonuclease site differences of PCR-amplified 16S rRNA gene. Syst. Appl. Microbiol. 18: 127–135.CrossRefGoogle Scholar
  64. Opelt, K., Berg, C. and Berg, G. (2007) The bryophyte genus Sphagnum is a reservoir for powerful and extraordinary antagonists and potentially facultative human pathogens. FEMS Microb. Ecol. 61: 38–53.CrossRefGoogle Scholar
  65. Palleroni, N.J. and Bradbury, J.F. (1993) Stenotrophomonas, a new bacterial genus for Xanthomonas maltophilia (Hugh 1980) Swings et al. 1983. Int. J. Syst. Bacteriol. 43: 606–609.PubMedCrossRefGoogle Scholar
  66. Prieto, C., Jara, C., Mas, A. and Romero, J. (2007) Application of molecular methods for analysing the distribution and diversity of acetic acid bacteria in Chilean vineyards. Int. J. Food Microbiol. 115: 348–55.PubMedCrossRefGoogle Scholar
  67. Raaijmakers, J.M., Paulitz, C.T., Steinberg, C., Alabouvette, C. and Moenne-Loccoz, Y. (2008) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil. doi 10.1007/s11104-008-9568-6.Google Scholar
  68. Ribbeck-Busch, K., Roder, A., Hasse, D., de Boer, W., Martínez, J.L., Hagemann, M. and Berg, G. (2005) A molecular biological protocol to distinguish potentially human-pathogenic strains of Stenotrophomonas maltophilia from non-pathogenic S. rhizophila strains. Environ. Microbiol. 7: 1853–1858.PubMedCrossRefGoogle Scholar
  69. Roder, A., Hoffmann, E., Hagemann, M. and Berg, G. (2005) Synthesis of the compatible solutes ­glucosylglycerol and trehalose by salt-stressed cells of Stenotrophomonas strains. FEMS Microbiol. Lett. 243: 219–226.PubMedCrossRefGoogle Scholar
  70. Ryan, R.P., Fouhy, Y., Garcia, B.F., Watt, S.A., Niehaus, K., Yang, L., Tolker-Nielsen, T. and Dow, J.M. (2008) Interspecies signalling via the Stenotrophomonas maltophilia diffusible signal factor influences biofilm formation and polymyxin tolerance in Pseudomonas aeruginosa. Mol. Microbiol. 68: 75–86.PubMedCrossRefGoogle Scholar
  71. Ryan, R.P., Monchy, S., Cardinale, M., Taghavi, S., Crossman, L., Avison, M.B., Berg, G., van der Lelie, D. and Dow, J.M. (2009) The versatility and adaptation of bacteria from the genus Stenotrophomonas. Nat. Rev. Microbiol. 7: 514–25.Google Scholar
  72. Tsavkelova, E.A., Cherdyntseva, T.A., Botina, S.G. and Netrusov, A.I. (2007) Bacteria associated with orchid roots and microbial production of auxin. Microbiol. Res. 162: 69–76.PubMedCrossRefGoogle Scholar
  73. Sader, H.S. and Jones, R.N. (2005) Antimicrobial susceptibility of uncommonly isolated non-enteric Gram-negative bacilli. Int. J. Antimicrob. Agents 25: 95–109.PubMedCrossRefGoogle Scholar
  74. Schreiber, L., Krimm, U., Knoll, D., Sayed, M., Auling, G. and Kroppenstedt, R.M. (2005) Plant–microbe interactions: identification of epiphytic bacteria and their ability to alter leaf surface permeability. New Phytol. 166: 589–594.PubMedCrossRefGoogle Scholar
  75. Sibley, C.D., Parkins, M.D., Rabin, H.R., Duan, K., Norgaard, J.C. and Surette, M.G.. (2008) A polymicrobial perspective of pulmonary infections exposes an enigmatic pathogen in cystic fibrosis patients. Proc. Natl. Acad. Sci. USA 105: 15070–15075.PubMedCrossRefGoogle Scholar
  76. Sørensen, J. (1997) The rhizosphere as a habitat for soil microorganisms, In: Van Elsas, J.D., Trevors, J.T., and Wellington, E.M.H. (eds.) Modern Soil Microbiology. Marcel Dekker, New York/Basel/Hongkong, pp. 21–45.Google Scholar
  77. Suckstorff, I. and Berg, G. (2003) Evidence for dose-dependent effects on plant growth by Stenotrophomonas strains from different origins. J. Appl. Microbiol. 95: 656–663.PubMedCrossRefGoogle Scholar
  78. Stotzky, G. and Schenk, S. (1976) Volatile organic compounds and microorganisms. CRC Crit. Rev. Microbiol. 4: 333–382.PubMedCrossRefGoogle Scholar
  79. Sun, L., Qiu, F., Zhang, X., Dai, X., Dong, X. and Song, W. (2008) Endophytic bacterial diversity in rice (Oryza sativa L.) roots estimated by 16S rDNA sequence analysis. Microb. Ecol. 55: 415–24.PubMedCrossRefGoogle Scholar
  80. Swings, J., De Vos, P., Van Den Mooter, M. and De Ley, J. (1983) Transfer of Pseudomonas maltophilia Hugh 1981 to the genus Xanthomonas as Xanthomonas maltophilia (Hugh 1981) comb. nov. Int. J. Syst. Bacteriol. 33: 409–413.Google Scholar
  81. Taghavi, S., Garafola, C., Monchy, S., Newman, L., Hoffman, A., Weyens, N., Barac, T., Vangronsveld, J. and van der Lelie, D. (2009) Genome survey and characterization of endophytic bacteria exhibiting a beneficial effect on growth and development of poplar trees. Appl. Environ. Microbiol. 75: 748–757.Google Scholar
  82. Tsavkelova, E.A., Cherdyntseva, T.A., Botina, S.G. and Netrusov, A.I. (2007) Bacteria associated with orchid roots and microbial production of auxin. Microbiol. Res. 162: 69–76.PubMedCrossRefGoogle Scholar
  83. Van Den Mooter, M. and Swings, J. (1990) Numerical analysis of 295 phenotypic features of 266 Xanthomonas strains and related strains and an improved taxonomy of the genus. Int. J. Syst. Bacteriol. 40: 348–369.PubMedCrossRefGoogle Scholar
  84. Vega, F.E., Pava-Ripoll, M., Posada, F. and Buyer, J.S. (2005) Endophytic bacteria in Coffea arabica L. J. Basic Microbiol. 45: 371–80.PubMedCrossRefGoogle Scholar
  85. Vila, J. and Martínez, J.L. (2008) Clinical impact of the over-expression of efflux pump in nonfermentative Gram-negative bacilli, development of efflux pump inhibitors. Curr. Drug Targets 9: 797–807.PubMedCrossRefGoogle Scholar
  86. Welsh, D.T. (2000) Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate. FEMS Microbiol. Rev. 24: 263–290.PubMedCrossRefGoogle Scholar
  87. Whipps, J. (2001) Microbial interactions and biocontrol in the rhizosphere. J. Exp. Bot. 52: 487–511.PubMedCrossRefGoogle Scholar
  88. Wheatley, R.E. (2002) The consequences of volatile organic compound mediated bacterial and fungal interactions. Antonie Van Leeuwenhoek 81: 357–364.PubMedCrossRefGoogle Scholar
  89. Wolf, A., Fritze, A., Hagemann, M. and Berg, G. (2002) Stenotrophomonas rhizophila sp. nov., a novel plant-associated bacterium with antifungal properties. Int. J. Syst. Evol. Microbiol. 52: 1937–1944.PubMedCrossRefGoogle Scholar
  90. Yang, H.C., Im, W.T., Kang, M.S., Shin, D.Y. and Lee, S.T. (2006) Stenotrophomonas koreensis sp. nov. isolated from compost in South Korea. Int. J. Syst. Evol. Microbiol. 56: 81–84.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Gabriele Berg
    • 1
    Email author
  • Dilfuza Egamberdieva
    • 2
  • Ben Lugtenberg
    • 3
  • Martin Hagemann
    • 4
  1. 1.Graz University of Technology, Environmental BiotechnologyGrazAustria
  2. 2.National University of Uzbekistan, VuzgorodokTashkentUzbekistan
  3. 3.Leiden University, Sylvius LaboratoryLeidenThe Netherlands
  4. 4.University of Rostock, Plant PhysiologyRostockGermany

Personalised recommendations