Abstract
During the past few years, an increasing awareness concerning the emission of an unexpected high number of bacterial volatiles has been registered. Humans sense, intensively and continuously, microbial volatiles that are released during food transformation and fermentation, e.g., the aroma of wine and cheese. Recent investigations have clearly demonstrated that bacteria also employ their volatiles during interactions with other organisms in order to influence populations and communities. This review summarizes the presently known bioactive compounds and lists the wide panoply of effects possessed by organisms such as fungi, plants, animals, and bacteria. Because bacteria often emit highly complex volatile mixtures, the determination of biologically relevant volatiles remains in its infancy. Part of the future goal is to unravel the structure of these volatiles and their biosynthesis. Nevertheless, bacterial volatiles represent a source for new natural compounds that are interesting for man, since they can be used, for example, to improve human health or to increase the productivity of agricultural products.
This is a preview of subscription content, access via your institution.





References
Alstrom S (2001) Characteristics of bacteria from oil seed rape in relation to their biocontrol of activity against Verticillium dahliae. J Phytopathol 149:57–64
Azcon-Aguiler C, Barea JM (1985) Effect of soil microorganisms on formation of vesicular–arbuscular mycorrhizas. Trans Br Mycol Soc 84:536–537
Azcon-Aguiler C, Diaz-Rodriguez RM, Barea JM (1986) Effects of soil microorganisms in spore germination and growth of the vesicular–arbuscular mycorrhizal fungus Glomus mossae. Trans Br Mycol Soc 86:337–340
Bargmann CI, Hartwieg E, Horvitz HR (1993) Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell 74:515–527
Bentley R, Meganathan R (1981) Geosmin and methylisoborneol biosynthesis in Streptomycetes: evidence for an isoprenoid pathway and the absence in non-differentiating isolates. FEBS Lett 125:220–222
Bonkowski M (2004) Protozoa and plant growth: the microbial loop in soil revisited. New Phytol 162:617–631
Bunge M, Araghipour N, Mikoviny T, Dunkl J, Schnitzhofer R, Hansel A, Schinner F, Wisthaler A, Marfesin R, Märk TD (2008) On-line monitoring of microbial volatile metabolites by proton transfer reaction-mass spectrometry. Appl Environ Microbiol 74:2179–2186
Cane DE, Watt RM (2003) Expression and mechanistic analysis of a germacradienol synthase from Streptomyces coelicolor implicated in geosmin biosynthesis. PNAS 100:1547–1551
Chaurasia B, Pandey A, Palni LMS, Trivedi P, Kumar B, Colvin N (2005) Diffusible and volatile compounds produced by an antagonistic Bacillus subtilis strain cause structural deformation in pathogenic fungi in vitro. Microbiol Res 160:75–81
Chuankun X, Minghe M, Leming Z, Keqin Z (2004) Soil volatile fungistasis and volatile fungistatic compounds. Soil Biol Biochem 36:1997–2004
Dainty RH, Edwards RA, Hibbard C (1985) Time course of volatile compound formation during refrigerated storage of naturally contaminated beef in air. J Appl Bacteriol 59:303–309
Dainty RH, Edwards RA, Hibbard CM, Marewick JJ (1989) Volatile compounds associated with microbial growth on normal and high pH beef stored at chill temperature. J Appl Microbiol 66:281–289
Dickschat JS, Wenzel SC, Bode HB, Müller R, Schulz S (2004) Biosynthesis of volatiles by the Myxobacterium Myxococcus xanthus. Chem Biol Chem 5:778–787
Dunkel M, Schmidt U, Struck S, Berger L, Gruening B, Hossbach J, Jaeger IS, Effmert U, Piechulla B, Eriksson R, Knudsen J, Preissner R (2009) Super Scent—a database of flavors and scents. Nucleic Acid Res 37. doi:https://doi.org/10.1093/nar/gkn695
Duponnois R, Kisa M (2006) The possible role of trehalose in the mycorrhiza helper bacterium effect. Can J Bot 84:1005–1008
Farag MA, Ryu CM, Summer LW, Pare PW (2006) GC-MS SPME profiling of rhizobacterial volatiles reveals prospective inducers of growth promotion and induced systemic resistance in plants. Phytochemistry 67:2262–2268
Fernando WGD, Ramarathnam R, Krishnamoorthy AS, Savchuk SC (2005) Identification and use of potential bacterial organic antifungal volatiles in biocontrol. Soil Biol Biochem 37:955–964
Fiddaman PJ, Rossall S (1993) The production of antifungal volatiles by Bacillus subtilis. J Appl Bacteriol 7:119–126
Fiddaman P, Rossall S (1994) Effect of substrate on the production of antifungal volatiles from Bacillus subtilis. J Appl Bacteriol 76:395–405
Fitter AH, Garbaye J (1994) Interactions between mycorrhizal fungi and other soil organisms. Plant Soil 159:123–132
Fries N (1973) Effects of volatile organic compounds on the growth and development of fungi. Trans Br Mycol Soc 60:1
Gu Y-Q, Mo M-H, Zhou JP, Zou C-S, Zhang K-Q (2007) Evaluation and identification of potential organic nematicidal volatiles from soil bacteria. Soil Biol Biochem 39:2567–2575
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 U S A 100:1541–1546
Hayes TS, Randle PE, Last FT (1969) The nature of the microbial stimulus affecting sporophore formation in Agaricus bisporus (Lange) Sing. Ann Appl Biol 64:177–187
Henis Y, Gould JR, Alexander M (1966) Detection and identification of bacteria by gas chromatography. Appl Microbiol 14:513–524
Hinton A Jr, Hume ME (1995) Antibacterial activity of the metabolic by-prodcuts of a Veillonella species and Bacteroides fragilis. Anaerobe 1:121–127
Hora TS, Baker R (1972) Soil fungistasis: microflora producing a volatile inhibitor. Trans Br Mycol 59:491–500
Huang J, Miller JR, Chen S, Vulule JM, Walker ED (2006) Anopheles gambiae (Diptera: Culicidae) oviposition in response to agarose media and cultured bacterial volatiles. J Med Entomol 43:498–504
Kai M, Effmert U, Berg G, Piechulla B (2006) Volatiles of bacterial antagonists inhibit mycelial growth of the plant pathogen Rhizoctonia solani. Arch Microbiol 187:351–360
Kai M, Vespermann A, Piechulla B (2008) The growth of fungi and Arabidopsis thaliana is influenced by bacterial volatiles. Plant Signal Behav 3:1–3
Korpi A, Pasanen A-L, Pasanen P (1998) Volatile compounds originating from mixed microbial cultures on building materials under various humidity conditions. Appl Environ Microbiol 64:2914–2919
Kurita-Ochiai T, Fukushima K, Ochiai K (1995) Volatile fatty acids, metabolitic by-products of periodontopathic bacteria, inhibit lymphocyte proliferation and cytokine production. J Dent Res 74:1367–1373
Kuzuyama T, Takagi M, Takahashi S, Seto H (2000) Cloning and characterization of 1-deoxy-d-xylulose-5-phosphate synthase from Streptomyces sp strain CL190, which uses both the mevalonate and the non-mevalonate pathways for isopentenyl diphosphate biosynthesis. J Bacteriol 182:891–897
Lockard JD, Kneebone LR (1962) Investigation of the metabolic gases produced by Agaricus bisporus (Lange) Sing. Mushroom Sci 5:281–299
Mackie A, Wheatley RE (1998) Effects and incidence of volatile organic compound interactions between soil bacterial and fungal isolates. Soil Biol Biochem 31:375–385
McCain AH (1966) A volatile antibiotic by Streptomyces griseus. Phytopathology 56:150
Moore-Landecker E, Stotzky G (1972) Inhibition of fungal growth and sporulation by volatile metabolites from bacteria. Can J Microbiol 18:957–962
Moore-Landecker E, Stotzky G (1973) Morphological abnormalities of fungi induced by volatile microbial metabolites. Mycologia 65:519–530
Moore-Landecker E, Stotzky G (1974) Effects of concentration of volatile metabolites from bacteria and germinating seeds on fungi in the presence of selective absorbents. Can J Microbiol 20:97–103
Ponnusamy L, Yxu N, Nojima S, Wesson DM (2008) Identification of bacteria and bacteria-associated chemical cues that mediate oviposition site preferences by Aedes aegypti. Proc Natl Acad Sci U S A 105:9262–9267
Ryan RP, Dow JM (2008) Diffusible signals and interspecies communication in bacteria. Microbiology 154:1845–1858
Ryu C-M, Farag MA, Hu C-H, Reddy MS, Wei HX, Pare PW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci U S A 100:4927–4932
Schrey SD, Schellhammer M, Ecke M, Hampp R, Tarkka MT (2005) Mycorrhiza helper bacterium Streptomyces AcH505 induces differential gene expression in the ectomycorrhizal fungus Amanita muscaria. New Phytol 168:205–216
Schöller CEG, Gürtler H, Pedersen R, Molin S, Wilkins K (2002) Volatile metabolites from actinomycetes. J Agric Food Chem 50:2615–2621
Schulz S, Dickschat JS (2007) Bacterial volatiles: the smell of small organisms. Nat Prod Rep 24:814–842
Sengupta P, Chou JH, Bargmann CI (1996) odr-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl. Cell 84:578–587
Stotzky G, Schenk S (1976) Volatile organic compounds and microorganisms. CRC Crit Rev Microbiol 4:333–382
Takagi M, Kuzuyama T, Takahashi S, Seto H (2000) A gene cluster for the mevalonate pathway from Streptomyces sp strain CL190. J Bacteriol 182:4153–4157
Tarkka MT, Piechulla B (2007) Aromatic weapons: truffles attack plants by the production of volatiles. New Phytol 175:383–386
Vespermann A, Kai M, Piechulla B (2007) Rhizobacterial volatiles affect the growth of fungi and Arabidopsis thaliana. Appl Environ Microbiol 73:5639–5641
Wang X, Ahearn DG (1997) Effect of bacteria on survival and growth of Acanthamoeba castellanii. Curr Microbiol 34:212–215
Whaley JW, Boyle AM (1967) Antibiotic production by Streptomyces species from the rhizosphere of desert plants. Phytopathology 57:347–351
Wheatley RE (2002) The consequences of volatile organic compounds mediated bacterial and fungal interactions. Antonie van Leeuwenhoek 81:357–364
Wrigley DM (2004) Inhibition of Clostridium perfringens sporulation by Bacteroides fragilis and short-chain fatty acids. Anaerobe 10:295–300
Zechman JM, Labows JNJ (1985) Volatiles of Pseudomonas aeruginosa and related species by automated headspace concentration-gas chromatography. Can J Microbiol 31:232–237
Zhang H, Kim M-S, Krishnamachari V, Payton P, Sun Y, Grimson M, Farag MA, Ryu C-M, Allen R, Melo IS, Pare PW (2007) Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226:839–851
Zoller HF, Mansfield Clark W (1921) The production of volatile fatty acids by bacteria of the dysentery group. J Gen Physiol 3:325–330
Zou C-S, Mo M-H, Gu Y-Q, Zhou J-P, Zhang K-Q (2007) Possible contributions of volatile-producing bacteria to soil fungistasis. Soil Biol Biochem 39:2371–2379
Acknowledgments
The authors thank the University of Rostock and the DFG for financial support to BP. The authors are grateful to the students Caroline Westendorf and Falco Lange for carrying out preliminary experiments. We thank Prof. Michael Bonkowski (Technical University Darmstadt, Germany) for Acanthamoeba castellanii, Prof. Andreas von Tiedemann (University Göttingen, Germany) and Prof. Ulla Bonas (University Halle, Germany) for several bacterial isolates, Prof. Till Roenneberg (University Munich, Germany) for Neurospora crassa wild-type strain.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kai, M., Haustein, M., Molina, F. et al. Bacterial volatiles and their action potential. Appl Microbiol Biotechnol 81, 1001–1012 (2009). https://doi.org/10.1007/s00253-008-1760-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-008-1760-3
Keywords
- Bacterial volatiles
- Volatile antibiotics
- Fungistasis
- Quorum sensing
- Serratia odorifera
- Stenotrophomonas