Skip to main content
Log in

Stenotrophomonas rhizophila DSM14405T promotes plant growth probably by altering fungal communities in the rhizosphere

  • Original Paper
  • Published:
Biology and Fertility of Soils Aims and scope Submit manuscript

Abstract

Stenotrophomonas rhizophila DSM14405T is of high biotechnological interest as plant growth stimulator, especially for salinated conditions. The objective of this study was to determine the effect of plant species (cotton, tomato, and sweet pepper) on colonisation and plant growth promotion of this beneficial bacterium in gnotobiotic systems and in non-sterile soil. All plant structures (leaves, stems, and roots) were densely colonised by DSM14405T reaching up to 109 cells g−1 fresh weight; under gnotobiotic conditions the abundances were 4–5 orders of magnitude higher than in non-sterile soil. Under non-sterile conditions and ambient humidity, tomato shoots were more densely colonised than shoots of sweet pepper and cotton. S. rhizophila DSM14405T was shown to grow endophytically and colonise the vicinity of root hairs of tomato. Plant growth promotion was particularly apparent in tomato. In general, the impact of plant species on colonisation and plant growth promotion was more pronounced in soil than under gnotobiotic conditions and likely due to the control of diseases and deleterious microorganisms. S. rhizophila DSM14405T was shown to control diseases in sweet pepper and in cotton. Molecular profiling via single strand conformation polymorphism of internal transcribed spacers and 16S rRNA genes (PCR-single strand conformational polymorphism (SSCP)) revealed that S. rhizophila DSM14405T strongly affected fungal, but not bacterial communities in the rhizosphere of tomato and sweet pepper. Major SSCP bands related to uncultured fungi and Candida subhashii, disappeared in tomato rhizosphere after Stenotrophomonas treatment. This suggests an indirect, species-specific plant growth promotion effect of S. rhizophila via the elimination of deleterious rhizosphere organisms.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adam H, Groenewald M, Mohan S, Richardson S, Bunn U, Gibas CF, Poutanen S, Sigler L (2009) Identification of a new species, Candida subhashii, as a cause of peritonitis. Med Mycol 47:305–311

    Article  PubMed  CAS  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman (1997) Gapped BLAST and PSI BLAST: a new generation of protein database search programmes. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA (1990) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56:1919–1925

    PubMed  CAS  Google Scholar 

  • Barret M, Morrissey JP, O’Gara F (2011) Functional genomics analysis of plant growth-promoting rhizobacterial traits involved in rhizosphere competence. Biol Fertils Soils 47:729–743

    Article  CAS  Google Scholar 

  • Bassam BJ, Caetano-Anolles G, Gresshoff PM (1991) Fast and sensitive silver staining of DNA in polyacrylamide gels. Analyt Biochem 80:81–84

    Google Scholar 

  • Berg G (2009) Plant-microbe interactions promoting plant growth and health: perspective for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 84:11–18

    Article  PubMed  CAS  Google Scholar 

  • Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13

    Article  PubMed  CAS  Google Scholar 

  • Berg G, Zachow C (2011) PGPR interplay with rhizosphere communities and effect on plant growth and health. In: Maheshwari DK (ed) Bacteria in agrobiology: crop ecosystems. Springer, Heidelberg, pp 97–110

    Google Scholar 

  • Berg G, Knaape C, Ballin G, Seidel D (1994) Biological control of Verticillium dahliae KLEB by naturally occurring rhizosphere bacteria. Arch Phytopathol Dis Prot 29:249–262

    Article  Google Scholar 

  • Berg G, Eberl L, Hartmann A (2005a) The rhizosphere as a reservoir for opportunistic human pathogenic bacteria. Environ Microbiol 7:1673–1685

    Article  PubMed  CAS  Google Scholar 

  • Berg G, Krechel A, Ditz M, Faupel A, Ulrich A, Hallmann J (2005b) Comparison of endophytic and ectophytic potato-associated bacterial communities and their antagonistic activity against plant pathogenic fungi. FEMS Microbiol Ecol 51:215–229

    Article  PubMed  CAS  Google Scholar 

  • Berg G, Alavi M, Schmidt CS, Zachow C, Egamberdieva D, Kamilova F, Lugtenberg (2012) Biocontrol and osmoprotection for plants under saline conditions. In: de Bruijn (ed). Molecular microbial ecology of the rhizosphere. Wiley: New York

  • Cardinale M, de Castro V, Jr J, Müller H, Berg G, Grube M (2008) In situ analysis of the bacterial community associated with the reindeer lichen Cladonia arbuscula reveals predominance of Alphaproteobacteria. FEMS Microbiol Ecol 66:63–71

    Article  PubMed  CAS  Google Scholar 

  • Da Silva JC, Albuquerque MC, de Mendonça EAF, Eliane M (2006) Cotton seed performance after processing and storage. Revista Brasileira de Sementes 28:79–85

    Google Scholar 

  • Daims H, Brühl A, Amann R, Schleifer K-H, Wagner M (1999) The domain-specific probe EUB338 is insufficient for the detection of all bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22:434–444

    Article  PubMed  CAS  Google Scholar 

  • Daims H, Stoecker K, Wagner M (2005) Fluorescence in situ hybridization for the detection of prokaryotes. In: Osborn AM, Smith CJ (eds) Advanced methods in molecular microbial ecology. Bios-Garland, Abingdon, UK, pp 213–239

    Google Scholar 

  • Dubuis C, Haas D (2007) Cross-species GacA-controlled induction of antibiosis in pseudomonads. Appl Environ Microbiol 73:650–654

    Article  PubMed  CAS  Google Scholar 

  • Dubuis C, Keel C, Haas D (2007) Dialogues of root colonizing pseudomonads. Eur J Plant Pathol 119:311–328

    Article  Google Scholar 

  • Dunne C, Moënne-Loccoz Y, McCarthy J, Higgins P, Powell J, Dowling DN, O’Gara F (1998) Combining proteolytic and phloroglucinol-producing bacteria for improved biocontrol of Pythium-mediated damping-off of sugar beet. Plant Pathol 47:299–307

    Article  Google Scholar 

  • Egamberdieva D, Kucharova Z, Davranov K, Berg G, Makarova N, Azarova T, Chebotar V, Tikhonovich I, Kamilova F, Validov SZ, Lugtenberg B (2011) Bacteria able to control foot and root rot and to promote growth of cucumber in salinated soils. Biol Fertil Soils 47:197–205

    Article  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 on salinated soil in Uzbekistan. Environ Microbiol 10:1–9

    Google Scholar 

  • FAO, Rome (Italy), Land and Water Development Div.; International Programme for Technology and Research in Irrigation and Drainage, Rome (Italy). Secretariat; Centre Virtuel de l’Eau Agricole et ses Usages, Rome (Italy). Centre d’Information sur l’Eau Agricole et ses Usage (2005) Management of irrigation-induced salt-affected soils. CISEAU/FAO/IPTRID, Rome

  • Fujita Y, Nakahara H (2006) Variations in the microalgal structure in paddy soil in Osaka, Japan: comparison between surface and subsurface soils. Limnology 7:83–91

    Article  CAS  Google Scholar 

  • Fürnkranz M, Müller H, Berg G (2009) Characterization of plant growth promoting bacteria from crops in Bolivia. J Plant Dis Plant Prot 116:149–155

    Google Scholar 

  • Gantner S, Schmid M, Duerr C, Schuhegger R, Steidle A, Hutzler P, Langebartels C, Eberl L, Hartmann A, Dazzo FB (2006) In situ quantitation of the spatial scale of calling distances and population density-independent N-acylhomoserine lactone mediated communication by rhizobacteria colonized on plant roots. FEMS Microbiol Ecol 56:188–194

    Article  PubMed  CAS  Google Scholar 

  • Götz M, Gomes NCM, Dratwinski A, Costa R, Berg G, Peixoto R, Mendonc L, Hagler LM, Smalla K (2006) Survival of gfp-tagged antagonistic bacteria in the rhizosphere of tomato plants and their effects on the indigenous bacterial community. FEMS Microbiol Ecol 52:207–218

    Article  Google Scholar 

  • Gould JH, Magallenes-Cedeno M (1998) Adaptation of cotton shoot apex culture to Agrobacterium mediated transformation. Plant Mol Biol Reporter 16:1–10

    Article  Google Scholar 

  • Hagemann M, Hasse D, 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

    Article  PubMed  CAS  Google Scholar 

  • Hagemann M, Ribbeck-Busch K, Klähn S, Hasse D, Steinbruch R, Berg G (2008) Synthesis of the compatible solute glucosylglycerol in Stenotrophomonas rhizophila. J Bac 190:5898–5906

    Article  CAS  Google Scholar 

  • Hartmann A, Schmid M, van Tuinen D, Berg G (2009) Plant-driven selection of microbes. Plant Soil 321:235–257

    Article  CAS  Google Scholar 

  • Howell AB, Francois L, Erwin DC (1994) Interactive effect of salinity and Verticillium albo-atrum on verticillium wilt disease severity and yield of two alfalfa cultivars. Field Crops Res 37:247–251

    Article  Google Scholar 

  • Jensen LE, Nybroe O (1999) Nitrogen availability to Pseudomonas fluorescens DF57 is limited during decomposition of barley straw in bulk soil in the barley rhizosphere. Appl Environ Microbiol 65:4320–4328

    PubMed  CAS  Google Scholar 

  • Ji P, Wilson M (2002) Assessment of the importance of similarity in carbon source utilization profiles between the biological control agent and the pathogen in biological control of bacterial speck of tomato. Appl Environ Microbiol 68:4383–4389

    Article  PubMed  CAS  Google Scholar 

  • Johnson JL, Marvin W, Fawley MW, Fawley KP (2007) The diversity of Scenedesmus and Desmodesmus (Chlorophyceae) in Itasca State Park, Minnesota, USA. Phycologia 46:214–229

    Article  Google Scholar 

  • Kai M, Effmert U, Berg G, Piechulla B (2007) Volatiles of bacterial antagonists inhibit mycelial growth of the plant pathogen Rhizoctonia solani. Arch Microbiol 187:351–360

    Article  PubMed  CAS  Google Scholar 

  • Kremer RJ, Kennedy AC (1996) Rhizobacteria as biocontrol agents of weeds. Weed Technol 10:601–609

    Google Scholar 

  • Larena I, Salazar O, González V, Marıá C, Julián MC, Rubio V (1999) Design of a primer for ribosomal DNA internal transcribed spacer with enhanced specificity for ascomycetes. J Biotechnol 75:187–194

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Manz W, Amann R, Ludwig W, Wagner M, Schleifer K-H (1992) Phylogenetic oligodeoxynucleotide probes for the major subclasses of Proteobacteria: problems and solutions. Syst Appl Microbiol 15:593–600

    Article  Google Scholar 

  • Mazzola M (2002) Mechanisms of natural soil suppressiveness to soilborne diseases. Antonie Van Leeuwenhoek 81:557–564

    Article  PubMed  CAS  Google Scholar 

  • Mejri D, Gamalero E, Tombolini R, Musso C, Massa N, Berta G, Souissi T (2010) Biological control of great brome (Bromus diandrus) in durum wheat (Triticum durum): specificity, physiological traits and impact on plant growth and root architecture of the fluorescent pseudomonad strain X33d. BioControl 55:561–572

    Article  Google Scholar 

  • Minkwitz A, Berg G (2001) Comparison of antifungal activities and 16S ribosomal DNA sequences of clinical and environmental isolates of Stenotrophomonas maltophilia. J Clin Microbiol 39:139–145

    Article  PubMed  CAS  Google Scholar 

  • Mo W, Li C, Zheng Y, Yue H, Li H (2006) Effect of relieving salt stress and growth-promoting bacteria on germination of cotton seed under salt stress. Nongye Gongcheng Xuebao/Trans Chin Soc Agric Eng 22:260–263

    CAS  Google Scholar 

  • Mühling M, Woolven-Allen J, Colin Murrell J, Joint I (2008) Improved group-specific PCR primers for denaturing gradient gel electrophoresis analysis of the genetic diversity of complex microbial communities. ISME J 2:379–392

    Article  PubMed  Google Scholar 

  • Müller H, Berg G (2008) Impact of formulation procedures on the effect of the biocontrol agent Serratia plymuthica HRO-C48 on Verticillium wilt in oilseed rape. Biocontrol 53:905–916

    Article  Google Scholar 

  • Müller H, Westendorf C, Leitner E, Chernin L, Riedel K, Schmidt S, Eberl L, Berg G (2009) Quorum-sensing effects in the antagonistic rhizosphere bacterium Serratia plymuthica HRO-C48. FEMS Microbiol Ecol 67:468–478

    Article  PubMed  Google Scholar 

  • Nadeem SM, Zahir ZA, Naveed M, Asghar HN, Arshad M (2010) Rhizobacteria capable of producing ACC-deaminase may mitigate salt stress in wheat. Soil Sci Soc America J 74:533–542

    Article  Google Scholar 

  • Parker BC, Bold HC, Deason TR (1961) Facultative heterotrophy in some chlorococcacean algae. Science 133:761–763

    Article  PubMed  CAS  Google Scholar 

  • Ribbeck-Busch K, Roder A, Hasse D, de Boer W, Martínez JL, Hagemann M, Berg G (2005) A molecular biological protocol to distinguish potentially human pathogenic Stenotrophomonas maltophilia from plant-associated Stenotrophomonas rhizophila. Environ Microbiol 7:1853–1858

    Article  PubMed  CAS  Google Scholar 

  • Ryan RP, Fouhy Y, Garcia BF, Watt SA, Niehaus K, Yang L, Tolker-Nielsen J, Dow 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

    Article  PubMed  CAS  Google Scholar 

  • Ryan RP, Monchy S, Cardinale M, Taghavi S, Crossman L, Avison MB, Berg G, van de Lelie D, Dow JM (2009) The versatility and adaptation of bacteria from the genus Stenotrophomonas. Nat Rev Microbiol 7:514–525

    Article  PubMed  CAS  Google Scholar 

  • Scherwinski K, Grosch R, Berg G (2008) Effect of bacterial antagonists on lettuce: active biocontrol of Rhizoctonia solani and negligible, short-term effects on non target microorganisms. FEMS Microbiol Ecol 64:106–116

    Article  PubMed  CAS  Google Scholar 

  • Schippers B, Bakker AW, Bakker PAHM (1987) Interactions of deleterious and beneficial rhizosphere microorganisms and the effect of cropping practices. Ann Rev Phytopathol 25:339–358

    Article  Google Scholar 

  • Schmidt CS, Lorenz D, Wolf GA (2001) Biological control of the grapevine dieback fungus Eutypa lata II: Influence of formulation additives and transposon mutagenesis on the antagonistic activity of Bacillus subtilis and Erwinia herbicola. J Phytopathol 149:437–445

    Article  Google Scholar 

  • Schwieger F, Tebbe CC (1998) A new approach to utilize PCR single strand-conformation polymorphism for 16S rRNA gene-based microbial community analysis. Appl Environ Microbiol 64:4870–4876

    PubMed  CAS  Google Scholar 

  • Shoup S, Lewis LA (2003) Polyphyletic origin of parallel basal bodies in swimming cells of Chlorophycean green algae (Chlorophyta). J Phycol 39:789–796

    Article  CAS  Google Scholar 

  • Suckstorff I, Berg G (2003) Evidence for dose-dependent effects on plant growth by Stenotrophomonas strains from different origin. J Appl Microbiol 95:656–663

    Article  PubMed  CAS  Google Scholar 

  • Suslow (2004) Key points of control and management of microbial food safety: Information for producers, handlers and processors of fresh market tomatoes. Publication 8150, University of California Division of Agriculture and Natural Resources, Oakland, CA, USA.

  • Tanji KK, Kielen NC (2002) Agricultural drainage water management in arid and semi-arid areas. FAO irrigation and drainage paper 61. FAO (Food and Agriculture Organisation of the United Nations), Rome

    Google Scholar 

  • Weller DM (2007) Pseudomonas biocontrol agents of soilborne pathogens: looking back over 30 years. Phytopathology 97:250–256

    Article  PubMed  Google Scholar 

  • White TJ, Bruns TD, Lee S, Taylor J (1990) Analysis of phylogenetic relationship by amplification and direct sequencing of ribosomal RNA genes. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic, New York, pp 315–322

    Google Scholar 

  • Williams P (2007) Quorum sensing, communication and cross-kingdom signalling in the bacterial world. Microbiology 153:3923–3938

    Article  PubMed  CAS  Google Scholar 

  • Wiyono S, Schulz D, Wolf GA (2008) Improvement of the formulation and antagonistic activity of Pseudomonas fluorescens B5 through selective additives in the pelleting process. Biol Control 46:348–357

    Article  Google Scholar 

  • Wolf A, Fritze A, Hagemann M, Berg G (2002) Stenotrophomonas rhizophila sp. nov., a novel plant-associated bacterium with antifungal properties. Int J Syst Evol Microbiol 52:1937–1944

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We wish to thank Dilfuza Egamberdiyeva (Tashkent) for the provision of seeds, Michael Fürnkranz (Graz) for very valuable advices and Katja Drofenigg (Graz) for technical support. This study was funded by the Austrian Science Foundation FWF by a grant to G.B.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christoph Stephan Schmidt.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schmidt, C.S., Alavi, M., Cardinale, M. et al. Stenotrophomonas rhizophila DSM14405T promotes plant growth probably by altering fungal communities in the rhizosphere. Biol Fertil Soils 48, 947–960 (2012). https://doi.org/10.1007/s00374-012-0688-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-012-0688-z

Keywords

Navigation