Advertisement

Applied Microbiology and Biotechnology

, Volume 88, Issue 4, pp 965–976 | Cite as

Serratia odorifera: analysis of volatile emission and biological impact of volatile compounds on Arabidopsis thaliana

  • Marco Kai
  • Elena Crespo
  • Simona M. Cristescu
  • Frans J. M. Harren
  • Wittko Francke
  • Birgit PiechullaEmail author
Applied Microbial and Cell Physiology

Abstract

Bacteria emit a wealth of volatiles. The combination of coupled gas chromatography/mass spectrometry (GC/MS) and proton-transfer-reaction mass spectrometry (PTR-MS) analyses provided a most comprehensive profile of volatiles of the rhizobacterium Serratia odorifera 4Rx13. An array of compounds, highly dominated by sodorifen (approximately 50%), a bicyclic oligomethyl octadiene, could be detected. Other volatiles included components of the biogeochemical sulfur cycle such as dimethyl disulfide (DMDS), dimethyl trisulfide and methanethiol, terpenoids, 2-phenylethanol, and other aromatic compounds. The composition of the bouquet of S. odorifera did not change significantly during the different growth intervals. At the beginning of the stationary phase, 60 μg of volatiles per 24 h and 60 easily detectable components were released. Ammonia was also released by S. odorifera, while ethylene, nitric oxide (NO) and hydrogen cyanide (HCN) could not be detected. Dual culture assays proved that 20 μmol DMDS and 2.5 μmol ammonia, individually applied, represent the IC50 concentrations that cause negative effects on Arabidopsis thaliana.

Keywords

Rhizobacteria Serratia odorifera Volatiles Plant growth promotion and inhibition Dimethyl disulfide Sodorifen 

Notes

Acknowledgements

The authors thank the students Falko Lange and Carolin Westendorf for initial investigations. We thank Claudio Valverde (University of Quilmes, Argentina) for providing the Pseudomonas wildtype and mutant strain and Aleksandra Laska-Oberndorff for technical assistance during the experiments in Nijmegen. This project was financially supported by the EU-FP6-project-026183, Life Science Trace Gas Facility to FvH/SC and the DFG to BP (PI 153/26-1) and to WF (FR 507/19-1).

Supplementary material

253_2010_2810_MOESM1_ESM.pdf (57 kb)
Table 1 Compilation of all compounds emitted by S. odorifera 4Rx13 as distinctly recorded by GC/MS (PDF 56 kb)
253_2010_2810_MOESM2_ESM.pdf (30 kb)
Table 2 Compilation of all compounds emitted by S. odorifera 4Rx13 as analyzed by PTR-MS (PDF 30 kb)
253_2010_2810_MOESM3_ESM.pdf (351 kb)
Fig. 1 Temporal volatile emission profiles of S. odorifera during 96 h of growth. Masses are indicated in each panel, m33 = methanol, m47 = ethanol, m79 = (benzene?), m95 = dimethyl disulfide, m127 = dimethyltrisulfide, m137 = monoterpene hydrocarbons. Emission intensity (μg h−1) of two independent cultures are depicted (black lines), emission of medium without bacteria (gray lines), CFU are indicated by solid dots. n = 3 (PDF 350 kb)

References

  1. Alborn HT, Turlings TCJ, Jones TH, Stenhagen G, Loughrin JH, Tumlinson JH (1997) An elicitor of plant volatiles from beet armyworm oral secretion. Science 276:945–949CrossRefGoogle Scholar
  2. Alstrom S (2001) Characteristics of bacteria from oil seed rape in relation to their biocontrol of activity against Verticillium dahliae. J Phytopathol 149:57–64CrossRefGoogle Scholar
  3. Aochi YO, Farmer WJ (2005) Impact of soil microstructure on the molecular transport dynamics of 1, 2-dichloroethane. Geoderma 127:137–153CrossRefGoogle Scholar
  4. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizoshere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266CrossRefGoogle Scholar
  5. Berg G, Roskot N, Steidle A, Eberl L, Zock A, Smalla K (2002) Plant-dependent genotypic and phenotypic diversity of antagonistic rhizobacteria isolated from different Verticillium host plants. Appl Environ Microbiol 68:3328–3338CrossRefGoogle Scholar
  6. Blumer C, Heeb S, Pessi G, Haas D (1999) Global GacA-steered control of cyanide and exoprotease production in Pseudomonas fluorescens involves specific ribosome binding sites. Proc Natl Acad Sci USA 96:14073–14078CrossRefGoogle Scholar
  7. Boamfa EI, Steeghs MML, Cristescu SM, Harren FJM (2004) Trace gas detection from fermentation processes in apples and rice; a comparison between proton-transfer-reaction mass spectrometry and laser photoacoustics. Int J Mass Spectrom 239:193–201CrossRefGoogle Scholar
  8. Bunge M, Araghipour N, Mikoviny T, Dunkl J, Schnitzhofer R, Hansel A, Schinner F, Wisthaler A, Margesin R, Märk TD (2008) On-line monitoring of microbial volatile metabolites by proton transfer reaction-mass spectrometry. Appl Environ Microbiol 74:2179–2186CrossRefGoogle Scholar
  9. Castric KF, Castric PA (1983) Method for rapid detection of cyanogenic bacteria. Appl Environ Microbiol 45:701–702Google Scholar
  10. Chuankun X, Minghe M, Leming Z, Kegin Z (2004) Soil volatile fungistasis and volatile fungistatic compounds. Soil Biol Biochem 36:1997–2004CrossRefGoogle Scholar
  11. Clarke SM, Cristescu SM, Miersch O, Harren FJM, Wasternack C, Mur LAJ (2009) Jasmonates act with salicylic acid to confer basal thermotolerance in Arabidopsis thaliana. New Phytol 182:175–187CrossRefGoogle Scholar
  12. Cristescu SM, Persijn ST, Te Lintel Hekkert S, Harren FJM (2008) Laser-based systems for trace gas detection in life sciences. Appl Phys B 92:343–349CrossRefGoogle Scholar
  13. Critchley A, Elliott T, Harrison G, Mayhew C, Thompson J, Worthington T (2004) The proton transfer reaction mass spectrometer and its use in medical science: applications to drug assays and the monitoring of bacteria. Int J Mass Spectrom 239:235–241CrossRefGoogle Scholar
  14. de Gouw J, Warneke C, Karl T, Eerdekens G, van der Veen C, Fall R (2003) Sensitivity and specificity of atmospheric trace gas detection by proton-transfer-reaction mass spectrometry. Int J Mass Spectrom 223:365–382CrossRefGoogle Scholar
  15. Dickschat JS, Wenzel SC, Bode HB, Müller R, Schulz S (2004) Biosynthesis of volatiles by the Myxobacterium Myxococcus xanthus. Chem Biol Chem 5:778–787Google Scholar
  16. Dickschat JS, Martens R, Brinkhoff T, Simon M, Schulz S (2005) Volatiles released by a Streptomyces species isolated from the North Sea. Chem Biodivers 2:837–865CrossRefGoogle Scholar
  17. Drath M, Kloft N, Batschaer A, Marin K, Novak J, Forchhammer K (2008) Ammonia triggers photodamage of photosystem II in the cyanobacterium Synechocystis sp. Strain PCC 6803. Plant Physiol 147:206–215CrossRefGoogle Scholar
  18. Dugravot S, Grolleau F, Macherel D, Rochetaing A, Hue B, Stankiewicz M, Huignard J, Lapied B (2003) Dimethyl disulfide exerts insecticidal neurotoxicity through mitochondrial dysfunction and activation of insect KATP channels. J Neurophysiol 90:259–270CrossRefGoogle Scholar
  19. Etschmann MMW, Bluemke W, Sell D, Schrader J (2002) Biotechnological production of 2-phenylethanol. Appl Microbiol Biotechnol 59:1–8CrossRefGoogle Scholar
  20. Fernando WGD, Ramarathnam R, Krishnamoorthy AS, Savchuk SC (2005) Identification and use of potential bacterial organic antifungal volatiles in biocontrol. Soil Biol Biochem 37:955–964CrossRefGoogle Scholar
  21. Fiddaman PJ, Rossall S (1994) Effect of substrate on the production of antifungal volatiles from Bacillus subtilis. J Appl Bacteriol 76:395–405Google Scholar
  22. Frankowski J, Berg G, Bahl H (2001) Mechanisms involved in the antifungal activity of the rhizobacterium Serratia plymuthica. Biological control of fungal and plant pathogens IOBC bulletin 21:45–50Google Scholar
  23. Fukuda H, Ogawa T, Tanasse S (1993) Ethylene production by microorganisms. Adv Microb Physiol 35:275–306CrossRefGoogle Scholar
  24. Gallois A, Grimont PAD (1985) Pyrazines responsible for the potatolike odor produced by some Serratia and Cedecea strains. Appl Environ Microbiol 50:1048–1051Google Scholar
  25. Gautier H, Auger J, Legros C, Lapied B (2008) Calcium-activated potassium channels in insect pacemaker neurons as unexpected target site for the novel fumigant dimethyl disulfide. J Pharmacol Experim Therapeut 324:149–159CrossRefGoogle Scholar
  26. Grimont PAD, Grimont F, Richard C, Davis BR, Steigerwalt AG, Brenner DJ (1978) Desoxyribonucleic acid relatedness between Serratia plymuthica and other Serratia species, with a description of Serratia odorifera sp.nov. (type strain: ICPB 3995). Intern J Systematic Bacteriol 28:453–463CrossRefGoogle Scholar
  27. Gust B, Challis GL, Fowler K, Kieser T, Chater KF (2003) PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc Natl Acad Sci USA 100:1541–1546CrossRefGoogle Scholar
  28. Kai M, Piechulla B (2009) Plant growth promotions due to rhizobacterial volatiles—an effect of CO2? FEBS Lett 583:3473–3477CrossRefGoogle Scholar
  29. Kai M, Effmert U, Berg G, Piechulla B (2007) Volatiles of bacterial antagonists inhibit mycelial growth of the plant pathogen Rhizoctonia solani. Arch Microbiol 187:351–360CrossRefGoogle Scholar
  30. Kai M, Haustein M, Molina F, Petri A, Scholz B, Piechulla B (2009) Bacterial volatiles and their action potential. Appl Microbiol Biotechnol 81:1001–1012CrossRefGoogle Scholar
  31. Kalbe C, Marten P, Berg G (1996) Members of the genus Serratia as beneficial rhizobacteria of oilseed rape. Microbiol Res 151:4433–4400Google Scholar
  32. Lewis BA (1985) Inhibition of Candida albicans by methanethiol produced by Brevibacterium linens. Microbiologica 8:387–390Google Scholar
  33. Lindinger W, Hansel A, Jordan A (1998a) Proton-transfer reaction mass spectrometry: online monitoring of volatile organic compounds at pptv levels. Chem Soc Rev 27:347–354CrossRefGoogle Scholar
  34. Lindinger W, Hansel A, Jordan A (1998b) Online monitoring of volatile organic compounds at pptv levels by means of Proton-transfer reaction mass spectrometry. Int J Mass Spectrom Ion Process 173:191–241CrossRefGoogle Scholar
  35. Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:351–356CrossRefGoogle Scholar
  36. Lynch JM, Whipps JM (1990) Substrate flow in the rhizosphere. Plant Soil 129:1–10CrossRefGoogle Scholar
  37. Minerdi D, Bossi S, Gullino ML, Garibaldi A (2009) Volatile organic compounds: a potential direct long distance mechanism for antagonistic action of Fusarium oxysporum strain MSA 35. Environm Microbiol 11:844–854CrossRefGoogle Scholar
  38. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497CrossRefGoogle Scholar
  39. Pare PW, Tumlinson JH (1999) Plant volatiles as a defense against insect herbivores. Plant Physiol 121:325–331CrossRefGoogle Scholar
  40. Piechulla B, Pott MB (2003) Plant scents—mediator of inter- and intraorganismic communication. Planta 217:687–689CrossRefGoogle Scholar
  41. Rimbault A, Niel P, Virelizier H, Darbord JC, Leluan G (1988) l-methionine, a precursor of trace methane in some proteolytic clostridia. Appl Environ Microbiol 54:1581–1586Google Scholar
  42. Ryu CM, Farag MA, Hu CH, Reddy MS, Wie HX, Pare PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci 100:4927–4932CrossRefGoogle Scholar
  43. Salman A, Filgueiras H, Cristescu SM, Lopez-Lauri F, Harren FJM, Sallanon H (2009) Inhibition of wound-induced ethylene does not prevent red discoloration in fresh-cut endive (Cichorium intybus L.). Eur Food Res Technol 228:651–657CrossRefGoogle Scholar
  44. Schöller CEG, Gürtler H, Petersen R, Molin S, Wilkins K (2002) Volatile metabolites from actinomycetes. J Agric Food Chem 50:2615–2621CrossRefGoogle Scholar
  45. Schulz S, Dickschat JS (2007) Bacterial volatiles: the smell of small organisms. Nat Prod Rep 24:814–842CrossRefGoogle Scholar
  46. Stall RE, Hall CB, Cook AA (1972) Relationship of ammonia to necrosis of pepper leaf tissue during colonization by Xanthomonas vesicatoria. Phytopathology 62:882–886CrossRefGoogle Scholar
  47. Steeghs MML, Moeskops BWM, van Swam K, Cristescu SM, Scheepers PTJ, Harren FJM (2006) On-line monitoring of UV-induced lipid peroxidation products from human skin in vivo using proton transfer reaction mass spectrometry. Int J Mass Spectrom 253:58–64CrossRefGoogle Scholar
  48. Steeghs MML, Cristescu SM, Munnik P, Zanen P, Harren FJM (2007) The suitability of tedlar bags for breath sampling in medical diagnostic research. Physiological Measurements 28:503–514CrossRefGoogle Scholar
  49. Stotzky G, Schenck S (1976) Volatile organic compounds and microorganisms. CRC Crit Rev Microbiol 4:333–382CrossRefGoogle Scholar
  50. Vespermann A, Kai M, Piechulla B (2007) Rhizobacterial volatiles affect the growth of fungi and Arabidopsis thaliana. Appl Environ Microbiol 73:5639–5641CrossRefGoogle Scholar
  51. Voisard C, Keel C, Haas D, Defago G (1989) Cyanide production by pseudomonas fluorescens helps suppress black root rot of tobacco under gnotobionic conditions. EMBO J 8:351–358Google Scholar
  52. von Reuβ S, Kai M, Piechulla B, Francke W (2010) Octamethylbicyclo(3.2.1)octadienes from Serratia odorifera. Angew Chem Int Ed 49:2009–2010Google Scholar
  53. Wenke K, Kai M, Piechulla B (2010) Belowground volatiles of plant roots, fungi and rhizobacteria facilitate interactions between soil organisms. Planta 231:499–506CrossRefGoogle Scholar
  54. Wheatley RE (2002) The consequences of volatile organic compound mediated bacterial and fungal interactions. Antonie Leeuwenhoek 81:357–364CrossRefGoogle Scholar
  55. Whipps JM (2001) Microbial interaction and biocontrol in the rhizosphere. J Experim Botany 52:487–511Google Scholar
  56. Zou CS, Mo MH, Gu YQ, Zhou JP, Zhang KQ (2007) Possible contribution of volatile-producing bacteria in soil fungistasis. Soil Biol Biochem 39:2371–2379CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Marco Kai
    • 1
  • Elena Crespo
    • 2
  • Simona M. Cristescu
    • 2
  • Frans J. M. Harren
    • 2
  • Wittko Francke
    • 3
  • Birgit Piechulla
    • 1
    • 4
    Email author
  1. 1.Department of Biological SciencesUniversity of RostockRostockGermany
  2. 2.Life Science Trace Gas FacilityRadboud University NijmegenNijmegenNetherlands
  3. 3.Institute of Organic ChemistryUniversity of HamburgHamburgGermany
  4. 4.Institute of Biological SciencesUniversity of RostockRostockGermany

Personalised recommendations