Advertisement

18 Fungal and Bacterial Volatile Organic Compounds: An Overview and Their Role as Ecological Signaling Agents

  • J. W. BennettEmail author
  • R. Hung
  • S. Lee
  • S. Padhi
Part of the The Mycota book series (MYCOTA, volume 9)

Abstract

Both fungi and bacteria emit many volatile organic compounds (VOCs) as mixtures of low molecular mass alcohols, aldehydes, esters, terpenoids, thiols, and other small molecules that easily volatilize. Most determination (separation and identification) of VOCs now relies on gas chromatography–mass spectrometry (GC-MS) but developments in “electronic nose” technology promise to revolutionize the field. Microbial VOC profiles are both complex and dynamic: the compounds produced and their abundance vary with the producing species, the age of the colony, water availability, the substrate, the temperature, and other environmental parameters. The single most commonly reported volatile from fungi is 1-octen-3-ol which is a breakdown product of linoleic acid. It functions as a hormone within many fungal species, serves as both an attractant and deterrent for certain species of arthropods, and exhibits toxicity at relatively low concentrations in model systems. Bacterial and fungal VOCs have been studied by scientists from a broad range of subdisciplines in both theoretical and applied contexts. VOCs are exploited for their food and flavor properties, their use as indirect indicators of microbial growth, their ability to stimulate plant growth, and their ability to attract insect pests. Because these compounds can diffuse a long way from their point of origin, they are excellent chemical signaling molecules (semiochemicals) in non-aqueous habitats and facilitate the ability of microbes to engage in “chemical conversations.” The physiological effects of bacterial and fungal VOCs in host–pathogen relationships and in mediating interspecific associations in natural ecosystem functioning is an emerging frontier for future research.

Keywords

Electronic Nose Sick Building Syndrome Fungal Secondary Metabolite Fruit Body Development Bacterial Volatile 
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.

Notes

Acknowledgements

We thank Arati Inamdar, James Mauro, Prakash Masurekar, Shannon Morath, David Pu, and Alisa Schink for their intellectual insights on fungal VOCs; we thank Natalie Naranjo and Shannon Morath for their help with the references, Karl Esser for his mentorship, Berthold Hock for his editorial support, and the Rutgers University Research Fund for financial support.

References

  1. Abramson D, Sinha RN, Mills JT (1980) Mycotoxin and odor formation in moist cereal grain during granary storage. Cereal Chem 57:346–351Google Scholar
  2. Abramson D, Sinha RN, Mills JT (1983) Mycotoxin and odor formation in barley stored at 16 and 20 % moisture in Manitoba. Cereal Chem 60:350–355Google Scholar
  3. Agrios GN (2008) Plant pathology, 5th edn. Academic, San DiegoGoogle Scholar
  4. Aldrich JR (1988) Chemical ecology of the heteroptera. Annu Rev Entomol 33:211–238Google Scholar
  5. Allen PJ (1957) Properties of a volatile fraction of uredospores of Puccinia graminis var. tritici affecting their germination and development. I. Biological activity. Plant Physiol 32:385–389PubMedGoogle Scholar
  6. Arora K, Chand S, Malhotra BD (2006) Recent developments in bio-molecular electronics techniques for food pathogens. Anal Chim Acta 568:259–274PubMedGoogle Scholar
  7. Assaf S, Hadar Y, Dosoretz CG (1997) 1-Octen-3-ol and 13-hydroperoxylinoleate are products of distinct pathways in the oxidative breakdown of linoleic acid by Pleurotus pulmonarius. Enzyme Microb Technol 21:484–490Google Scholar
  8. Atmosukarto I, Castillo U, Hess W, Sears J, Strobel G (2005) Isolation and characterization of Muscodor albus I-41.3s, a volatile antibiotic producing fungus. Plant Sci 169:854–861Google Scholar
  9. Bacon CW, White JW (eds) (2000) Microbial endophytes. Dekker, New YorkGoogle Scholar
  10. Baldwin IT, Halitschke R, Paschold A, von Dahl CC, Preston CA (2006) Volatile signaling in plant-plant interactions: “talking trees” in the genomics era. Science 311:812–815PubMedGoogle Scholar
  11. Banchio E, Xie X, Zhang H, Paré PW (2009) Soil bacteria elevate essential oil accumulation and emissions in sweet basil. J Agric Food Chem 57:653–657PubMedGoogle Scholar
  12. Bassler BL, Losick R (2006) Bacterially speaking. Cell 125:237–246PubMedGoogle Scholar
  13. Bennett JW (1983) Differentiation and secondary metabolism in mycelial fungi. In: Bennett JW, Ciegler A (eds) Secondary metabolism and differentiation in fungi. Dekker, New York, pp 1–32Google Scholar
  14. Bennett JW, Bentley R (1989) What’s In a name? – microbial secondary metabolism. Adv Appl Microbiol 34:1–28Google Scholar
  15. Bennett JW, Feibelman T (2001) Fungal bacterial interactions. In: Hock B (ed) The mycota, vol IX. Springer, Berlin, pp 229–240Google Scholar
  16. Bentley R, Maganathan R (1981) Geosmin and methylisoborneol biosynthesis in Streptomycetes. Evidence for an isoprenoid pathway and its absence in nondifferentiating isolates. FEBS Lett 125:220–222PubMedGoogle Scholar
  17. Berg JM, Tymoch JL, Stryer L (2007) Biochemistry. Freeman, New YorkGoogle Scholar
  18. Berger RG, Drawert F, Tiefel P (1992) Naturally occurring flavours from fungi, yeasts, and bacteria. In: Patterson RLS, Charlwood BV, MacLeod G, Williams AA (eds) Bioinformation of flavours. Royal Chemistry Society, Cambridge, pp 1–20Google Scholar
  19. Bloch E, Deorazio R (1994) Chemistry in a salad bowl: comparative organosulfur chemistry of garlic, onion, and shitake mushrooms. Pure Appl Chem 66:2205–2206Google Scholar
  20. Bohbot JD, Dickens JC (2009) Characterization of an enantioselective odorant receptor in the yellow fever mosquito Aedes aegypti. PLoS One 4:7032Google Scholar
  21. Borg-Karlson A-K, Englund F, Unelius CR (1994) Dimethyl oligosulphides, major volatiles released from Sauromatum guttatum and Phallus impudicus. Phytochemistry 35:321–323Google Scholar
  22. Börjesson T, Stöllman UM, Adamek P, Kaspersson A (1989) Analysis of volatile compounds for detection of molds in stored cereals. Cereal Chem 66:300–304Google Scholar
  23. Börjesson T, Stöllman UM, Schnürer J (1993) Off-odorous compounds produced by molds on oatmeal agar: identification and relation to other growth characteristics. J Agric Food Chem 41:2104–2111Google Scholar
  24. Breheret S, Talou T, Rapior S, Bessiere J-M (1997) Monoterpenes in the aromas of fresh wild mushrooms. J Agric Food Chem 45:831–836Google Scholar
  25. Brodhagen M, Tsitsigiannis DI, Hornung E, Goebel C, Feussner I, Keller NP (2008) Reciprocal oxylipin-mediated cross-talk in the Aspergillus–seed pathosystem. Mol Microbiol 67:378–391PubMedGoogle Scholar
  26. Brodhun F, Feussner I (2011) Oxylipins in fungi. FEBS J 278:1047–1063PubMedGoogle Scholar
  27. Brown WL (1968) An hypothesis concerning the function of the metapleural glands in ants. Am Nat 102:188–191Google Scholar
  28. Bruce A, Verrall S, Hackett CA, Wheatley RE (2004) Identification of volatile organic compounds (VOCs) from bacteria and yeast causing growth inhibition of sapstain fungi. Holzforschung 58:193–198Google Scholar
  29. Burge PS (2004) Studies on the role of fungi in sick building syndrome. Occup Environ Med 61:185–190PubMedGoogle Scholar
  30. Camilli A, Bassler BL (2006) Bacterial small-molecule signaling pathways. Science 311:1113–1116PubMedGoogle Scholar
  31. Champe SP, el-Zayat AA (1989) Isolation of a sexual sporulation hormone from Aspergillus nidulans. J Bacteriol 171:3982–3988PubMedGoogle Scholar
  32. Champe SP, Rao P, Chang A (1987) An endogenous inducer of sexual development in Aspergillus nidulans. J Gen Microbiol 133:1383–1387PubMedGoogle Scholar
  33. Chiron N, Michelot D (2005) Odeurs de champignons: chimie et rôle dans les interactions biotiques – une revue. Cryptogam Mycol 26:299–364Google Scholar
  34. Chitarra GS, Abee T, Rombouts FM, Posthumus MA, Dijksterhuis J (2004) Germination of Penicillium paneum conidia is regulated by 1-octen-3-ol, a volatile self-inhibitor. Appl Environ Microbiol 70:2823–2829PubMedGoogle Scholar
  35. Chitarra GS, Abee T, Rombouts FM, Dijksterhuis J (2005) 1-Octen-3-ol inhibits conidia germination of Penicillium paneum despite of mild effects on membrane permeability, respiration, intracellular pH, and changes the protein composition. FEMS Microbiol Ecol 54:67–75PubMedGoogle Scholar
  36. Cho IH, Namgung H-J, Choi H-K, Kim YS (2008) Volatiles and key odorants in the pileus and stipe of pine-mushroom (Tricholoma matsutake sing). Food Chem 106:71–76Google Scholar
  37. Choudhary DK, Johri BN, Prakash A (2008) Volatiles as priming agents that initiate plant growth and defence responses. Curr Sci 94:595–604Google Scholar
  38. Claeson A-S, Levin J-O, Gr B, Sunesson A-L (2002) Volatile metabolites from microorganisms grown on humid building materials and synthetic media. J Environ Monit 4:667–672PubMedGoogle Scholar
  39. Clough SJ, Schell MA, Denny TP (1994) Evidence for involvement of a volatile extracellular factor in Pseudomonas solonacearum virulence gene expression. MPMI 7:621–630Google Scholar
  40. Cole R, Schweikert M (2003) Handbook of secondary fungal metabolites, vol 1–3. Academic, AmsterdamGoogle Scholar
  41. Combet E, Henderson J, Eastwood DC, Burton KS (2006) Eight-carbon volatiles in mushrooms and fungi: properties, analysis, and biosynthesis. Mycoscience 47:317–326Google Scholar
  42. Cronin DA, Ward MK (1971) The characterisation of some mushroom volatiles. J Sci Food Agric 22:477–479Google Scholar
  43. de Pinho PG, Ribeiro B, Goncalves RF, Baptista P, Valentao P, Seabra RM, Andrade PB (2008) Correlation between the pattern volatiles and the overall aroma of wild edible mushrooms. J Agric Food Chem 56:1704–1712PubMedGoogle Scholar
  44. Dicke M, Sabelis MW (1988) Infochemical terminology: based on cost–benefit analysis rather than origin of compounds? Funct Ecol 2:131–139Google Scholar
  45. Dickschat JS, Martens R, Brinkhoff T, Simon M, Schulz S (2005a) Volatiles releases by Streptomyces species isolated from the North Sea. Chem Biodivers 2:837–865PubMedGoogle Scholar
  46. Dickschat JS, Wenzel SC, Bode HB, Müller R, Schulz S (2005b) Biosynthesis of volatiles by the Myxobacterium Myxococcus xanthus. Chembiochem 5:778–787Google Scholar
  47. Dowd PF, Bartelt RJ (1991) Host-derived volatiles as attractants and pheromone synergists for dried fruit beetle, Carpophilus hemipterus. J Chem Ecol 17:285–308Google Scholar
  48. 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) SuperScent – a database of flavors and scents. Nucleic Acids Res 37(Database Issue):D291–D294PubMedGoogle Scholar
  49. Eberhard A, Burlingame AL, Eberhard C, Kenyon GL, Nealson KH, Oppenheimer NJ (1981) Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry 20:2444–2449PubMedGoogle Scholar
  50. Eisner T (2003) For love of insects. Harvard University Press, CambridgeGoogle Scholar
  51. Ellis DI, Broadhurst D, Kell DB, Rowland JJ, Goodacre R (2002) Rapid and quantitative detection of the microbial spoilage of meat by Fourier transform infrared spectroscopy and machine learning. Appl Environ Microbiol 68:2822–2828PubMedGoogle Scholar
  52. Fäldt J, Jonsell M, Nordlander G, Borg-Karlson A-K (1999) Volatiles of bracket fungi Fomitopsis pinicola and Fomes fomentarius and their functions as insect attractants. J Chem Ecol 25:567–590Google Scholar
  53. Farag MA, Ryu CM, Sumner LW, Pare PW (2006) GC-MS SPME profiling of rhizobacterial volatiles reveals prospective inducers of growth promotion and induced systemic resistance in plants. Phytochemistry 67:2262–2268PubMedGoogle Scholar
  54. Fernando WGD, Ramarathnam R, Krishnamoorthy AS, Savchuk SC (2005) Identification and use of potential bacterial organic antifungal volatiles in biocontrol. Soil Biol Biochem 37:955–964Google Scholar
  55. Fiedler N, Laumbach R, Kelly-McNeil K, Lioy P, Fan Z-H, Zhang J, Ottenweller J, Ohman-Strickland P, Kipen H (2005) Health effects of a mixture of indoor air volatile organics, their ozone oxidation products, and stress. Environ Health Perspect 113:1542–1548PubMedGoogle Scholar
  56. Fischer G, Schwalbe R, Möller M, Ostrowski R, Dott W (1999) Species-specific production of microbial volatile organic compounds (MVOC) by airborne fungi from a compost facility. Chemosphere 39:779–810Google Scholar
  57. Flavier AB, Ganova-Raeva LM, Schell MA, Denny TP (1997) Hierarchial autoinduction in Ralstonia solanacearum: control of actyl- homoserine lactone production by a novel autoregulatory system responsive to 30- hydroxypalmitic acid methyl ester. J Bacteriol 179:7089–7097PubMedGoogle Scholar
  58. Fraatz MA, Zorn H (2010) Fungal flavours. In: Hofrichter M (ed) The Mycota X: industial applications, vol X, 2nd edn, Industrial applications. Springer, Berlin Heidelberg New York, pp 249–264Google Scholar
  59. Fuqua WC, Winans SC, Greenberg EP (1994) Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176:269–275PubMedGoogle Scholar
  60. Gallois A, Langlois D (1990) New results in the volatile odorous compounds of French cheeses. Lait 70:89–106Google Scholar
  61. Griffin MA, Spakowicz DJ, Gianoulis TA, Strobel SA (2010) Volatile organic compound production by organisms in the genus Ascocoryne and a re-evaluation of myco-diesel production by NRRL 50072. Microbiology 156:3814–3829PubMedGoogle Scholar
  62. Griffith RT, Jayachandran K, Shetty KG, Whitstine W, Furton KG (2007) Differentiation of toxic molds via headspace SPME-GC/MS and canine detection. Sensors 7:1496–1508Google Scholar
  63. Gutiérrez-Luna FM, López-Bucio J, Altamirano-Hernández J, Valencia-Cantero E, Cruz HR, Macías-Rodríguez L (2010) Plant growth-promoting rhizobacteria modulate root-system architecture in Arabidopsis thaliana through volatile organic compound emission. Symbiosis 51:75–83Google Scholar
  64. Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59:19–42PubMedGoogle Scholar
  65. Herrero-Garcia E, Garzia A, Cordobés S, Espeso EA, Ugalde U (2011) 8-Carbon oxylipins inhibit germination and growth, and stimulate aerial conidiation in Aspergillus nidulans. Fungal Biol 115:393–400PubMedGoogle Scholar
  66. Hogan DA (2006) Talking to themselves: autoregulation and quorum sensing in fungi. Eukaryot Cell 5:613–619PubMedGoogle Scholar
  67. Hooper AM, Pickett JA (2004) Semiochemistry. In: Atwood JL, Steed JW (eds) Encyclopedia of supramolecular chemistry, vol 2. Dekker, New York, pp 1270–1277Google Scholar
  68. Horswill A, Stoodley P, Stewart P, Parsek M (2007) The effect of the chemical, biological, and physical environment on quorum sensing in structured microbial communities. Anal Bioanal Chem 387:371–380PubMedGoogle Scholar
  69. Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66PubMedGoogle Scholar
  70. Hutchinson SA (1973) Biological activities of volatile fungal metabolites. Annu Rev Phytopathol 11:223–246Google Scholar
  71. Inamdar AA, Masurekar P, Bennett JW (2010) Neurotoxicity of fungal volatile organic compounds in Drosophila melanogaster. Toxicol Sci 117:418–426PubMedGoogle Scholar
  72. Inamdar AA, Moore JC, Cohen RI, Bennett JW (2011) A model to evaluate the cytotoxicity of the fungal volatile organic compound 1-octen-3-ol in human embryonic stem cells. Mycopathologia 173:13–20PubMedGoogle Scholar
  73. IOM (2004) Damp indoor spaces and health. National Academies, WashingtonGoogle Scholar
  74. Jarvis BB, Miller JD (2005) Mycotoxins as harmful indoor air contaminants. Appl Microbiol Biotechnol 66:367–372PubMedGoogle Scholar
  75. Jeleń HH (2003) Use of solid phase microextraction (SPME) for profiling fungal volatile metabolites. Lett Appl Microbiol 36:263–267PubMedGoogle Scholar
  76. Joblin Y, Moularat S, Anton R, Bousta F, Orial G, Robine E, Picon O, Bourouina T (2010) Detection of moulds by volatile organic compounds; application to heritage conservation. Int Biodeterior Biodegrad 64:210–217Google Scholar
  77. Kai M, Haustein M, Molina F, Petri A, Scholz B, Piechulla B (2009) Bacterial volatiles and their action potential. Appl Microbiol Biotechnol 81:1001–1012PubMedGoogle Scholar
  78. Kaminski E, LIbbey LM, Stawicki S, Wasowicz E (1972) Identification of the predominant volatile compounds produced by Aspergillus flavus. Appl Microbiol 24:721–726PubMedGoogle Scholar
  79. Kaplan HB, Greenberg EP (1985) Diffusion of autoinducer is involved in regulation of the Vibrio fischeri luminescence system. J Bacteriol 163:1210–1214PubMedGoogle Scholar
  80. Karahadian C, Josephson DB, Lindsay RC (1985) Contribution of Penicillium sp. to the flavour of Brie and Camembert cheese. J Dairy Sci 68:1865–1877Google Scholar
  81. Karlovsky P (ed) (2008) Secondary metabolites in soil ecology. Springer, Berlin Heidelberg New YorkGoogle Scholar
  82. Karlshøj K, Nielsen PV, Larsen TO (2007) Fungal volatiles biomarkers of good and bad food quality. In: Dijksterhuis J, Samson RA (eds) Food mycology. CRC, Boca Raton, pp 279–302Google Scholar
  83. Karlson P, Luscher M (1959) ‘Pheromones’: a new term for a class of biologically active substances. Nature 183:55–56PubMedGoogle Scholar
  84. Keller NP, Turner G, Bennett JW (2005) Fungal secondary metabolism – from biochemistry to genomics. Nat Rev Microbiol 3:937–947PubMedGoogle Scholar
  85. Kesselmeier J, Staudt M (1999) Biogenic volatile organic compounds (VOC): an overview on emission, physiology and ecology. J Atmos Chem 33:23–88Google Scholar
  86. Kishimoto K, Matsui K, Ozawa R, Takabayashi J (2007) Volatile 1-octen-3-ol induces a defensive response in Arabidopsis thaliana. J Gen Plant Pathol 73:35–37Google Scholar
  87. Kline D, Allan SA, Bernier UR, Welch CH (2007) Evaluation of the enantiomers of 1-octen-3-ol and 1-octyn-3-ol as attractants for mosquitoes associated with a freshwater swamp in Florida, USA. Med Vet Entomol 21:323–331PubMedGoogle Scholar
  88. Kolter R, Greenberg EP (2006) Microbial sciences: the superficial life of microbes. Nature 441:300–302PubMedGoogle Scholar
  89. Korpi A, Jarnberg J, Pasanen A-L (2009) Microbial volatile organic compounds. Crit Rev Toxicol 39:139–193PubMedGoogle Scholar
  90. Kües U, Navarro-González M (2009) Communication of fungi on individual, species, kingdom, and above kingdom levels. In: Anke T, Weber D (eds) The Mycota XV. Physiology and genetics. Springer, Berlin Heidelberg New York, pp 79–106Google Scholar
  91. Kuske M, Romain A-C, Nicolas J (2005) Microbial volatile organic compounds as indicators of fungi. Can an electronic nose detect fungi in indoor environments? Build Environ 40:824–831Google Scholar
  92. La Camera S, Gouzerh G, Sandrine D, Laurent H, Bernard F, Michel F, Thierry H (2004) Metabolic reprogramming in plant innate immunity: the contributions of phenylpropanoid and oxylipin pathways. Immunol Rev 198:267–284PubMedGoogle Scholar
  93. Lam K, Tsang M, Labrie A, Gries R, Gries G (2010) Semiochemical-mediated oviposition avoidance by female house flies, Musca domestica, on animal feces colonized with harmful fungi. J Chem Ecol 36:141–147PubMedGoogle Scholar
  94. Larsen TO, Frisvad JC (1995) Comparison of different methods for collection of volatile chemical markers from fungi. J Microbiol Methods 24:135–144Google Scholar
  95. Lax AR, Templeton GE, Meyer WL (1985) Isolation, purification, and biological activity of a self-inhibotor from conidia of Colletotrichum gloeosporioides. Phytopathology 75:386–390Google Scholar
  96. Lee SO, Kim HY, Choi GJ, Lee HB, Jang KS, Choi YH, Kim JC (2009) Mycofumigation with Oxyporus latemarginatus EF069 for control of postharvest apple decay and Rhizoctonia root rot on moth orchid. J Appl Microbiol 106:1213–1219PubMedGoogle Scholar
  97. Leeder AC, Palma-Guerrero J, Glass NL (2011) The social network: deciphering fungal language. Nat Rev Microbiol 9:440–451PubMedGoogle Scholar
  98. Li DW, Yang CS (2004) Fungal contamination as a major contributor to sick building syndrome. Adv Appl Microbiol 55:31–112PubMedGoogle Scholar
  99. Liu W, Mu W, Zhu B, Liu F (2008) Antifungal activities and components of VOCs produced by Bacillus subtilis G8. Curr Res Bacteriol 1:28–34Google Scholar
  100. Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556PubMedGoogle Scholar
  101. Luntz AJ (2003) Arthropod semiochemicals: mosquitoes, midges and sealice. Biochem Soc Trans 31:128–133PubMedGoogle Scholar
  102. Mackie AE, Wheatley RE (1999) Effects and incidence of volatile organic compound interactions between soil bacterial and fungal isolates. Soil Biol Biochem 31:375–385Google Scholar
  103. Mattheis JP, Roberts RG (1992) Identification of geosmin as a volatile metabolite of Penicillium expansum. Appl Environ Microbiol 58:3170–3172PubMedGoogle Scholar
  104. Matysik S, Herbarth O, Mueller A (2008) Determination of volatile metabolites originating from mould growth on wall paper and synthetic media. J Microbiol Methods 75:182–187PubMedGoogle Scholar
  105. Matysik S, Herbarth O, Mueller A (2009) Determination of microbial volatile organic compounds (MVOCs) by passive sampling onto charcoal sorbents. Chemosphere 76:114–119PubMedGoogle Scholar
  106. Mau J-L, Beelman RB, Ziegler GR (1992) Effect of 10-oxo-trans-8-decenoic acid on growth of Agaricus bisporus. Phytochemistry 31:4059–4064Google Scholar
  107. Mau J-L, Chyau C-C, Li J-Y, Tseng Y-H (1997) Flavor compounds in straw mushrooms Volvariella volvacea harvested at different stages of maturity. J Agric Food Chem 45:4726–4729Google Scholar
  108. Mauriello G, Marino R, D’Auria M, Cerone G, Rana GL (2004) Determination of volatile organic compounds from truffles via SPME-GC-MS. J Chromatogr Sci 42:299–305PubMedGoogle Scholar
  109. McFee DR, Zavon P (1988) Solvents. In: Plog BA (ed) Fundamentals of industrial hygiene, 3rd edn. National Safety Council, Chicago, pp 95–121Google Scholar
  110. McNeal KS, Herbert BE (2009) Volatile organic metabolites as indicators of soil microbial activity and community composition shifts. Soil Sci Soc Am J 73:579–588Google Scholar
  111. Meilgaard MC (1975a) Flavor chemistry of beer. I. Flavor interaction between principal volatiles. Tech Q Master Brewers Assoc Am 12:107–117Google Scholar
  112. Meilgaard MC (1975b) Flavor chemistry of beer. II. Flavor and threshold of 239 aroma volatiles. Tech Q Master Brewers Assoc Am 12:151–168Google Scholar
  113. Mercier J, Jiménez JI (2004) Control of fungal decay of apples and peaches by the biofumigant fungus Muscodor albus. Postharvest Biol Tec 31:1–8Google Scholar
  114. Mercier J, Manker D (2005) Biocontrol of soil-borne diseases and plant growth enhancement in greenhouse soilless mix by the volatile-producing fungus Muscodor albus. Crop Prot 24:355–362Google Scholar
  115. 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. Environ Microbiol 11:844–854PubMedGoogle Scholar
  116. Mølhave L (2009) Volatile organic compounds and the sick building syndrome. In: Lippmann M (ed) Environmental toxicants: human exposures and their health effects, 3rd edn. Wiley-Interscience, New York, pp 241–256Google Scholar
  117. Morey P, Wortham A, Weber A, Horner E, Black M, Muller W (1997) Microbial VOCs in moisture damaged buildings. Health Build 1:245–250Google Scholar
  118. Mosandl A, Heusinger G, Gessner M (1986) Analytical and sensory differentiation of 1-octen-3-ol enantiomers. J Agric Food Chem 34:119–122Google Scholar
  119. Nealson KH, Hastings JW (1979) Bacterial bioluminescence: its control and ecological significance. Microbiol Rev 43:496–518PubMedGoogle Scholar
  120. Nealson KH, Platt T, Hastings JW (1970) Cellular control of the synthesis and activity of the bacterial luminescent system. J Bacteriol 104:313–322PubMedGoogle Scholar
  121. Nemcovic M, Jakubikova L, Viden I, Farkas V (2008) Induction of conidiation by endogenous volatile compounds in Trichoderma spp. FEMS Microbiol Lett 284:231–236PubMedGoogle Scholar
  122. Nilssen AC (1998) Effect of 1-octen-3-ol in field trapping Aedes spp. (Dipt., Culicidae) and Hybomitra spp. (Dipt., Tabanidae) in subartic Norway. J Appl Entomol 122:465–468Google Scholar
  123. Nilsson A, Kihlstrom E, Lagesson V, Wessen B, Szponar B, Larsson L, Tagesson C (2004) Microorganisms and volatile organic compounds in airborne dust from damp residences. Indoor Air 14:74–82PubMedGoogle Scholar
  124. Niu Q, Huang X, Zhang L, Xu J, Yang D, Wei K, Niu X, An Z, Bennett JW, Zou C, Yang J, Zhang KQ (2010) A Trojan horse mechanism of bacterial pathogenesis against nematodes. Proc Natl Acad Sci USA 107:16631–16636PubMedGoogle Scholar
  125. Noble R, Dobrovin-Pennington A, Hobbs PJ, Pederby J, Rodger A (2009) Volatile C8 compounds and pseudomonads influence primordium formation of Agaricus bisporus. Mycologia 101:583–591PubMedGoogle Scholar
  126. Nordlund DA, Lewis WJ (1976) Terminology of chemical releasing stimuli in intraspecific and interspecific interactions. J Chem Ecol 2:211–220Google Scholar
  127. Noverr MC, Erb-Downward JR (2003) Production of eicosanoids and other oxylipins by pathogenic eukaryotic microbes. Clin Microbiol Rev 16:517–533PubMedGoogle Scholar
  128. Okull DO, Beelman RB, Gourama H (2003) Antifungal activity of 10-oxo-trans-8-decenoic acid and 1-octen-3-ol against Penicillium expansum in potato dextrose agar medium. J Food Prot 66:1503–1505PubMedGoogle Scholar
  129. Oldroyd GED, Downie JA (2004) Calcium, kinases and nodulation signalling in legumes. Nat Rev Mol Cell Biol 5:566–576PubMedGoogle Scholar
  130. Ômura H, Kuwahara Y, Tanabe T (2002) 1-Octen-3-ol together with geosmin: new secretion compounds from a polydesmid millipede, Niponia nodulosa. J Chem Ecol 28:2601–2612PubMedGoogle Scholar
  131. Ortiz-Castro R, Contreras-Cornejo H, Macias-Rodriguez L, Lopez-Bucio J (2009) The role of microbial signals in plant growth and development. Plant Signal Behav 4:701–712PubMedGoogle Scholar
  132. Palkova Z, Forstova J (2000) Yeast colonies synchronise their growth and development. J Cell Sci 113:1923–1928PubMedGoogle Scholar
  133. Palkova Z, Janderova B, Gabriel J, Zikanova B, Pospisek M, Forstova J (1997) Ammonia mediates communication between yeast colonies. Nature 390:532–536PubMedGoogle Scholar
  134. Palkova Z, Devaux F, Icicova M, Minarikova L, Le Crom S, Jacq C (2002) Ammonia pulses and metabolic oscillations guide yeast colony development. Mol Biol Cell 13:3901–3914PubMedGoogle Scholar
  135. Pasanen P, Korpi A, Kalliokosi P, Pasanen AL (1997) Growth and volatile metabolite production of Aspergillus versicolor in house dust. Environ Int 23:425–432Google Scholar
  136. Pavlou AD, Turner AP (2000) Sniffing out the truth: clinical diagnosis using the electronic nose. Clin Chem Lab Med 38:99–112PubMedGoogle Scholar
  137. Pelaez F (2005) Biological activities of fungal metabolites. In: An Z (ed) Handbook of industrial mycology. Dekker, New York, pp 49–92Google Scholar
  138. Pierce AM, Pierce HD, Borden JH, Oehlschlager AC (1991a) Fungal volatiles: semiochemicals for stored-product beetles (Coleoptera: Cucujidae). J Chem Ecol 3:567–579Google Scholar
  139. Pierce AM, Pierce HD, Oehlschlager AC, Borden JH (1991b) 1-Octen-3-ol, attractive semiochemical for foreign grain beetle, Ahasverus adevna (Waltl) (Coleoptera: Cucujidae). J Chem Ecol 3:567–579Google Scholar
  140. Poland TM, Pureswaran DS, Ciaramitaro TM, Borden JH (2009) 1-Octen-3-ol is repellent to Ips pini (Coleoptera: Curculionidae: Scolytinae) in the Midwestern United States. Can Entomol 141:158–160Google Scholar
  141. Ramoni R, VIncent F, Grolli S, Conti V, Malosse C, Boyer F, Nagnan-Le Meillour P, Spinelli S, Cambillau C, Tegoni M (2001) The insect attractant 1-octen-3-ol is the natural ligand of bovine odorant-binding protein. J Biol Chem 276:7150PubMedGoogle Scholar
  142. Rapior S, Breheret S, Talou T, Pelissier Y, Bessiere JM (2002) The anise-like odor of Clitocybe odora, Lentinellus cochleatus, and Agaricus essettie. Mycologia 94:373–376PubMedGoogle Scholar
  143. Robinson J (ed) (2006) The Oxford companion to wine, 3rd edn. Oxford, Oxford University PressGoogle Scholar
  144. Rodriguez RJ, White JF, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330PubMedGoogle Scholar
  145. Rude MA, Schirmer A (2009) New microbial fuels: a biotech perspective. Curr Opin Microbiol 12:274–281PubMedGoogle Scholar
  146. Rumbaugh KP, Griswold JA, Hamood AN (2000) The role of quorum sensing in the in vivo virulence of Pseudomonas aeruginosa. Microbes Infect 2:1721–1731PubMedGoogle Scholar
  147. Ryu C-M, Farag MA, Hu C-H, Reddy MS, Wei H-X, Paré PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci USA 100:4927–4932PubMedGoogle Scholar
  148. Ryu C-M, Farag MA, Paré PW, Kloepper JW (2005) Invisible signals from the underground: bacterial volatiles elicit plant growth promotion and induce systemic resistance. Plant Pathol J 21:7–12Google Scholar
  149. Schnürer J, Olsson J, Börjesson T (1999) Fungal volatiles as indicators of food and feeds spoilage. Fungal Genet Biol 27:209–217PubMedGoogle Scholar
  150. Schöller CEG, Gürtler H, Petersen R, Molin S, Wilkins K (2002) Volatile metabolites from Actinomycetes. J Agric Food Chem 50:2615–2621PubMedGoogle Scholar
  151. Schreier P (1992) Bioflavours: an overview. In: Patterson RLS, Charlwood BV, MacLeod G, Williams AA (eds) Bioinformation of flavours. Royal Society of Chemistry, Cambridge, pp 1–20Google Scholar
  152. Schulz S, Dickschat JS (2007) Bacterial volatiles: the smell of small organisms. Nat Prod Rep 24:814–842PubMedGoogle Scholar
  153. Shapiro JA (1998) Thinking about bacterial populations as multicellular organisms. Annu Rev Microbiol 52:81–104PubMedGoogle Scholar
  154. Shimkets LJ (1999) Intercellular signaling during fruiting-body development of Myxococcus xanthus. Annu Rev Microbiol 53:525–549PubMedGoogle Scholar
  155. Singh SK, Strobel GA, Knighton B, Geary B, Sears J, Ezra D (2011) An endophytic Phomopsis sp. possessing bioactivity and fuel potential with its volatile organic compounds. Microb Ecol 61:729–739PubMedGoogle Scholar
  156. Sneeden EY, Harris HH, Pickering J, Prince RC, Johnson S, Li X, Block E, George GH (2004) The sulfur chemistry of shitake mushroom. J Am Chem Soc 126:458–459PubMedGoogle Scholar
  157. Splivallo R, Bossi S, Maffei M, Bonfante P (2007a) Discrimination of truffle fruiting body versus mycelial aromas by stir bar sorptive extraction. Phytochemistry 68:2584–2598PubMedGoogle Scholar
  158. Splivallo R, Novero M, Bertea CM, Bossi S, Bonfante P (2007b) Truffle volatiles inhibit growth and induce an oxidative burst in Arabidopsis thaliana. New Phytol 175:417–424PubMedGoogle Scholar
  159. Stinson M, Ezra D, Hess WM, Sears J, Strobel G (2003) An endophytic Gliocladium sp. of Eucryphia cordifolia producing selective volatile antimicrobial compounds. Plant Sci 165:913–922Google Scholar
  160. Stoppacher N, Kluger B, Zeilinger S, Krska R, Schuhmacher R (2010) Identification and profiling of volatile metabolites of the biocontrol fungus Trichoderma atroviride by HS-SPME-GC-MS. J Microbiol Methods 81:187–193PubMedGoogle Scholar
  161. Straus DC (2009) Molds, mycotoxins, and sick building syndrome. Toxicol Ind Health 25:617–635PubMedGoogle Scholar
  162. Straus DC, Cooley JD, Wong WC, Jumper CA (2003) Studies on the role of fungi in sick building syndrome. Arch Environ Health 58:475–478PubMedGoogle Scholar
  163. Strobel GA, Dirkse E, Sears J, Markworth C (2001) Volatile antimicrobials from Muscodor albus a novel endophytic fungus. Microbiology 147:2943–2950PubMedGoogle Scholar
  164. Strobel GA, Knighton B, Kluck K, Ren Y, Livinghouse T, Griffin M, Spakowicz D, Sears J (2008) The production of myco-diesel hydrocarbons and their derivatives by the endophytic fungus Gliocladium roseum (NRRL 50072). Microbiology 154:3319–3328PubMedGoogle Scholar
  165. Strobel GA, Singh SK, Riyaz-Ul-Hassan S, Mitchell AM, Geary B, Sears J (2011) An endophytic/pathogenic Phoma sp. from creosote bush producing biologically active volatile compounds having fuel potential. FEMS Microbiol Lett 320:87–94PubMedGoogle Scholar
  166. Ström G, West J, Wessen B, Palmgren U (1994) Health implications of fungi in indoor environments: quantitative analysis of microbial volatiles in damp Swedish houses. Air Qual Monogr 2:291–305Google Scholar
  167. Sunesson AL, Vaes WHJ, Nilsson CA, Blomquist G, Andersson B, Carlson R (1995) Identification of volatile metabolites from five fungal species cultivated on two media. Appl Environ Microbiol 61:2911–2918PubMedGoogle Scholar
  168. Sunesson AL, Nilsson CA, Andersson B, Blomquist G (1996) Volatile metabolites produced by two fungal species cultivated on building materials. Ann Occup Hyg 40:397–410PubMedGoogle Scholar
  169. Takahashi N (1986) Chemistry of plant hormones. CRC, Boca RatonGoogle Scholar
  170. Tan RX, Zou WV (2001) Endophytes: a rich source of functional metabolites. Nat Prod Rep 18:448–459PubMedGoogle Scholar
  171. Tarkka MT, Piechulla B (2007) Aromatic weapons: truffles attack plants by the production of volatiles. New Phytol 175:381–383PubMedGoogle Scholar
  172. Thomson NR, Crow MA, McGowan SJ, Cox A, Salmond GPC (2000) Biosynthesis of carbapenem antibiotic and prodigiosin pigment in Serratia is under quorum sensing control. Mol Microbiol 36:539–556PubMedGoogle Scholar
  173. Thorn J (2001) The inflammatory response in humans after inhalation of bacterial endotoxin: a review. Inflamm Res 50:254–261PubMedGoogle Scholar
  174. Tirillini B, Verdelli G, Paolocci F, Ciccioli P, Frattoni M (2000) The volatile organic compounds from the mycelium of Tuber borchii Vitt. Phytochemistry 55:983–985PubMedGoogle Scholar
  175. Trinci APJ, Whittaker C (1968) Self-inhibition of spore germination in Aspergillus nidulans. Trans Br Mycol Soc 51:594–596Google Scholar
  176. Tsitsigiannis DI, Keller NP (2007) Oxylipins as developmental and host-fungal communication signals. Trends Microbiol 15:109–118PubMedGoogle Scholar
  177. Tsurushima T, Ueno T, Fukami H, Irie H, Inoue M (1995) Germination self-inhibitors from Colletotrichum gloeosporioides f.sp jussiaea. Mol Plant Microbe Interact 8:652–657Google Scholar
  178. Turner WB (1971) Fungal metabolites. Academic, LondonGoogle Scholar
  179. Turner WB, Aldridge DC (1983) Fungal metabolites II. Academic, LondonGoogle Scholar
  180. Van Delden C, Iglewski BH (1998) Cell-to-cell signaling and Pseudomonas aeruginosa infections. Emerg Infect Dis 4:551–560PubMedGoogle Scholar
  181. Vespermann A, Kai M, Piechulla B (2007) Rhizobacterial volatiles affect the growth of fungi and Arabidopsis thaliana. Appl Environ Microbiol 73:5639–5641. doi: 10.1128/AEM.01078-07 PubMedGoogle Scholar
  182. von Bodman SB, Bauer WD, Coplin DL (2003) Quorum sensing in plant-pathogenic bacteria. Annu Rev Phytopathol 41:455–482Google Scholar
  183. Walinder R, Ernstgard L, Johanson G, Venge P, Wieslander G (2005) Acute effects of a fungal volatile compound. Environ Health Perspect 113:1775–1778PubMedGoogle Scholar
  184. Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346PubMedGoogle Scholar
  185. Watson SB, Brownlee B, Satchwill T, Hargesheimer EE (2000) Quantitative analysis of trace levels of geosmin and MIB in source and drinking water using headspace SPME. Water Res 34:2818–2828Google Scholar
  186. Weeks EN, Birkett MA, Cameron MM, Pickett JA, Logan JG (2011) Semiochemicals of the common bed bug, Cimex lectularius L. (Hemiptera: Cimicidae), and their potential for use in monitoring and control. Pest Manag Sci 67:10–20PubMedGoogle Scholar
  187. Wheatley R, Hackett C, Bruce A, Kundzewicz A (1997) Effect of substrate composition on production of volatile organic compounds from Trichoderma spp. inhibitory to wood decay fungi. Int Biodeterior Biodegrad 39:199–205Google Scholar
  188. Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52(Suppl 1):487–511PubMedGoogle Scholar
  189. Whitehead NA, Barnard ANL, Slater H, Simpson NJL, Salmond GPC (2001) Quorum-sensing in Gram-negative bacteria. FEMS Microbiol Rev 25:365–404PubMedGoogle Scholar
  190. Whittaker RH, Feeny PP (1971) Allelochemics: chemical interactions between species. Science 171:757–770PubMedGoogle Scholar
  191. WHO (2009) Guidelines for indoor air quality: dampness and mold. Druckpartner Moser, GermanyGoogle Scholar
  192. Wilkins K, Larsen K, Simkus M (2000) Volatile metabolites from mold growth on building materials and synthetic media. Chemosphere 41:437–446PubMedGoogle Scholar
  193. Wilson AD, Baietto M (2009) Applications and advances in electronic-nose technologies. Sensors 9:5099–5148PubMedGoogle Scholar
  194. Wilson AD, Baietto M (2011) Advances in electronic-nose technologies developed for biomedical applications. Sensors 11:1105–1176PubMedGoogle Scholar
  195. Wood WF, Fesler M (1986) Mushroom odors: student synthesis of the odoriferous compounds of the matsutake mushroom. J Chem Educ 63:92Google Scholar
  196. Wurzenberger M, Grosch W (1984) The formation of 1-octen-3-ol from the 10-hydroperoxide isomer of linoleic acid by a hydroperoxide lyase in mushrooms (Psalliota bispora). Biochim Biophys Acta Lipids Lipid Metab 794:25–30Google Scholar
  197. Xie X, Zhang H, Pare P (2009) Sustained growth promotion in Arabidopsis with long-term exposure to the beneficial soil bacterium Bacillus subtilis (GB03). Plant Signal Behav 4:948–953PubMedGoogle Scholar
  198. Zhang Z, Li G (2010) A review of advances and new developments in the analysis of biological volatile organic compounds. Microchem J 95:127–139Google Scholar
  199. Zhang QH, Schlyter F (2004) Olfactory recognition and behavioural avoidance of angiosperm nonhost volatiles by conifer-inhabiting bark beetles. Agric For Entomol 6:1–19Google Scholar
  200. Zhang Y-Q, Wilkinson H, Keller NP, Tsitsigiannis D (2005) Secondary metabolite gene clusters. In: An Z (ed) Handbook of industrial microbiology. Dekker, New York, pp 355–386Google Scholar
  201. Zhang H, Kim M-S, Krishnamachari V, Payton P, Sun Y, Grimson M, Farag M, Ryu C-M, Allen R, Melo I, Paré P (2007) Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226:839–851PubMedGoogle Scholar
  202. Zhang H, Xie X, Kim MS, Kornyeyev DA, Holaday S, Pare PW (2008) Soil bacteria augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta. Plant J 56:264–273PubMedGoogle Scholar
  203. Zhang CL, Wang GP, Mao LJ, Komon-Zelazowska M, Yuan ZL, Lin FC, Druzhinina IS, Kubicek CP (2010) Muscodor fengyangensis sp. nov. from southeast China: morphology, physiology and production of volatile compounds. Fungal Biol 114:797–808PubMedGoogle Scholar
  204. Zogorski JS, Carter JM, Ivahnenko T, Lapham WW, Moran MJ, Rowe BL, Squillace PJ, Toccalino PL (2006) The quality of our nation’s waters – volatile organic compounds in the nation’s ground water and drinking-water supply wells. US Geological Survey Circular 1292. US Geological Survey, RestonGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Department of Plant Biology and PathologyRutgers UniversityNew BrunswickUSA

Personalised recommendations