1932

Abstract

Many volatile organic compounds (VOCs) associated with industry cause adverse health effects, but less is known about the physiological effects of biologically produced volatiles. This review focuses on the VOCs emitted by fungi, which often have characteristic moldy or “mushroomy” odors. One of the most common fungal VOCs, 1-octen-3-ol, is a semiochemical for many arthropod species and also serves as a developmental hormone for several fungal groups. Other fungal VOCs are flavor components of foods and spirits or are assayed in indirect methods for detecting the presence of mold in stored agricultural produce and water-damaged buildings. Fungal VOCs function as antibiotics as well as defense and plant-growth-promoting agents and have been implicated in a controversial medical condition known as sick building syndrome. In this review, we draw attention to the ubiquity, diversity, and toxicological significance of fungal VOCs as well as some of their ecological roles.

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2020-09-08
2024-04-13
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Literature Cited

  1. 1. 
    Agrawal R. 2004. Flavors and aromas. Fungal Biotechnology in Agricultural, Food, and Environmental Applications DK Arora 281–89 New York: Marcel Dekker
    [Google Scholar]
  2. 2. 
    Akacha NB, Gargouri M. 2015. Microbial and enzymatic technologies used for the production of natural aroma compounds: synthesis, recovery modeling, and bioprocesses. Food Bioprod. Process 94:675–706
    [Google Scholar]
  3. 3. 
    Aldrich JR 1988. Chemical ecology of heteroptera. Annu. Rev. Entomol. 33:211–38
    [Google Scholar]
  4. 4. 
    Al-Maliki HS, Martinez S, Piszczatowski P, Bennett J 2017. Drosophila melanogaster as a model for studying Aspergillus fumigatus. Mycobiology 45:233–39
    [Google Scholar]
  5. 5. 
    Alpha CJ, Campos M, Jacobs-Wagner C, Strobel SA 2015. Mycofumigation by the volatile organic compound-producing fungus Muscodor albus induces bacterial cell death through DNA damage. Appl. Environ. Microbiol. 81:1147–56
    [Google Scholar]
  6. 6. 
    Archbold D, Hamilton-Kemp T, Barth M, Langlois B 1997. Identifying natural volatile compounds that control gray mold (Botrytis cinerea) during postharvest storage of strawberry, blackberry, and grape. J. Agricult. Food Chem. 45:4032–37
    [Google Scholar]
  7. 7. 
    Assaf S, Hadar Y, Dosoretz C 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 21:484–90
    [Google Scholar]
  8. 8. 
    Bacon C, White J. 2000. Microbial Endophytes New York: Marcel Dekker
  9. 9. 
    Bazemore RA, Feng J, Cseke L, Podila G 2012. Biomedically important pathogenic fungi detection with volatile biomarkers. J. Breath Res. 6:016002
    [Google Scholar]
  10. 10. 
    Beltran-Garcia M, Estarron-Espinos M, Ogura T 1997. Volatile compounds secreted by the oyster mushroom (Pleurotus ostreatus) and their antibacterial activities. J. Agric. Food Chem. 45:4049–52
    [Google Scholar]
  11. 11. 
    Bentley R, Meganathan R. 1981. Geosmin and methylisoborneol biosynthesis in streptomycetes: evidence for an isoprenoid pathway and its absence in non-differentiating isolates. FEBS Lett 125:220–22
    [Google Scholar]
  12. 12. 
    Berendsen RL, Kalkhove SI, Lugones LG 2013. Effects of the mushroom-volatile 1-octen-3-ol on dry bubble disease. App. Microbiol. Biotechnol. 97:5535–43
    [Google Scholar]
  13. 13. 
    Berger R, Böker A, Fischer M, Taubert J 1999. Microbial flavors. Flavor Chemistry R Teranishi, EL Wick, I Hornstein 229–38 Boston: Springer
    [Google Scholar]
  14. 14. 
    Bhandari S, Chambers S, Pearson J, Syhre M, Epton M, Scott-Thomas A et al. 2011. Determining the limits and confounders for the 2-pentyl furan breath test by gas chromatography/mass spectrometry. J. Chromatogr. B. 879:2815–20
    [Google Scholar]
  15. 15. 
    Bitas V, Kim HS, Bennett JW, Kang S 2013. Sniffing on microbes: diverse roles of microbial volatile organic compounds in plant health. Mol. Plant Microbe Interact. 26:835–43
    [Google Scholar]
  16. 16. 
    Bitas V, McCartney N, Li N, Demers J, Kim J, Kim H et al. 2015. Fusarium oxysporum volatiles enhance plant growth via affecting auxin transport and signaling. Front. Microbiol. 6:1248
    [Google Scholar]
  17. 17. 
    Bone E. 2011. Mycophilia: Revelations from the Weird World of Mushrooms New York: Rodale
  18. 18. 
    Borjesson T, Johnsson L. 1998. Detection of common bunt (Tilletia caries) infestation in wheat with an electronic nose and a human panel. J. Plant Dis. Prot. 105:306–13
    [Google Scholar]
  19. 19. 
    Chambers ST, Syhre M, Murdoch DR, McCartin F, Epton M 2009. Detection of 2-pentylfuran in the breath of patients with Aspergillus fumigatus. Med. Mycol 47:468–76
    [Google Scholar]
  20. 20. 
    Chiron N, Michelot D. 2005. Odeurs de champignons: chimie et rôle dans les interactions biotiques—une revue. Cryptogam. Mycol. 4:299–364
    [Google Scholar]
  21. 21. 
    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. 70:2823–29
    [Google Scholar]
  22. 22. 
    Cho I, Namgung H, Choi H, Kim Y 2008. Volatiles and key odorants in the pileus and stipe of pine-mushroom (Tricholoma matsutake Sing.). Food Chem 106:71–76
    [Google Scholar]
  23. 23. 
    Combet E, Henderson J, Eastwood DC, Burton K, Combet E et al. 2006. Eight-carbon volatiles in mushrooms and fungi: properties, analysis, and biosynthesis. Mycoscience 47:317–26
    [Google Scholar]
  24. 24. 
    Davis T, Crippen T, Hofstetter R 2013. Microbial volatile emissions as insect semiochemicals. J. Chem. Ecol. 39:840–59
    [Google Scholar]
  25. 25. 
    de Heer K, Kok MG, Fens N, Weersink EJ, Zwinderman AH, van der Schee MP et al. 2016. Detection of airway colonization by Aspergillus fumigatus by use of electronic nose technology in patients with cystic fibrosis. J. Clin. Microbiol. 54:569–75
    [Google Scholar]
  26. 26. 
    Dennis C, Webster J. 1971. Antagonistic properties of species-groups of Trichoderma: II. Production of volatile antibiotics. Trans. Br. Mycol. Soc. 57:41–48
    [Google Scholar]
  27. 27. 
    Dunkel M, Schmidt U, Struck S, Berger L, Gruening B et al. 2009. SuperScent—a database of flavors and scents. Nucleic Acids Res 37:D291–94
    [Google Scholar]
  28. 28. 
    Elke K, Begerow J, Oppermann H, Krämer U, Jermann E, Dunemann L 1999. Determination of selected microbial volatile organic compounds by diffusive sampling and dual-column capillary GC-FID—a new feasible approach for the detection of an exposure to indoor mould fungi. J. Environ. Monit. 1:445–52
    [Google Scholar]
  29. 29. 
    Empting L. 2009. Neurologic and neuropsychiatric syndrome features of mold and mycotoxin exposure. Toxicol. Ind. Health 25:577–81
    [Google Scholar]
  30. 30. 
    Environ. Prot. Agency 2003. 1-Octen-3-ol fact sheet Fact Sheet, Environ. Prot. Agency Washington, DC: https://www3.epa.gov/pesticides/chem_search/reg_actions/registration/fs_PC-069037_28-Apr-03.pdf
  31. 31. 
    Faldt J, Jonsell M, Nordlander G, Borg-Karlson A 1999. Volatiles of bracket fungi Fomitopsis pinicola and Fomes fomentarius and their functions as insect attractants. J. Chem. Ecol. 25:567–90
    [Google Scholar]
  32. 32. 
    Garcia-Alcega S, Nasir ZA, Ferguson R, Whitby C, Dumbrell AJ et al. 2017. Fingerprinting outdoor air environment using microbial volatile organic compounds (MVOCs)—A review. Trends Anal. Chem. 86:75–83
    [Google Scholar]
  33. 33. 
    Gilbert A. 2008. What the Nose Knows: The Science of Scent in Everyday Life Scotts Valley, CA: CreateSpace
  34. 34. 
    Gonzalez M, Celis A, Guevara-Suarez M, Molina J, Carazzone C 2019. Yeast smell like what they eat: analysis of volatile organic compounds of Malassezia furfur in growth media supplemented with different lipids. Molecules 24:419
    [Google Scholar]
  35. 35. 
    Haschek WM, Boyd MR, Hakkinen PJ, Owenby CS, Witschi H 1984. Acute inhalation toxicity of 3-methylfuran in the mouse: pathology, cell kinetics, and respiratory rate effects. Toxicol. Appl. Pharmacol. 72:124–33
    [Google Scholar]
  36. 36. 
    Heddergott C, Calvo AM, Latge J 2014. The volatome of Aspergillus fumigatus. Eukaryot. Cell 13:1014–25
    [Google Scholar]
  37. 37. 
    Herrmann A 2010. The Chemistry and Biology of Volatiles Chichester, UK: John Wiley
  38. 38. 
    Hodgson M. 2000. Sick building syndrome. Occup. Med. 15:571–85
    [Google Scholar]
  39. 39. 
    Hooper AM, Pickett JA. 2004. Semiochemistry. Encyclopedia of Supramolecular Chemistry JL Atwood, JW Steed 1270–77 New York: Marcel Dekker
    [Google Scholar]
  40. 40. 
    Horner W, Morey P, Black M 1999. MVOC and VOC emission pattern from multiple strains of indoor fungi. Proc. Indoor Air. 4:915–20
    [Google Scholar]
  41. 41. 
    Hudler GW. 1998. Magical Mushrooms, Mischievous Molds Princeton, NJ: Princeton Univ. Press
  42. 42. 
    Hung R, Lee S, Bennett J 2014. The effects of low concentrations of the enantiomers of mushroom alcohol (1-octen-3-ol) on Arabidopsis thaliana. Mycology 5:73–80
    [Google Scholar]
  43. 43. 
    Hung R, Lee S, Bennett J 2015. Fungal volatile organic compounds and their role in ecosystems. Appl. Microbiol. Biotechnol. 99:3395–405
    [Google Scholar]
  44. 44. 
    Hung R, Lee S, Rodriguez-Saona C, Bennett J 2014. Common gas phase molecules from fungi affect seed germination and plant health in Arabidopsis thaliana. AMB Express 4:53
    [Google Scholar]
  45. 45. 
    Inamdar AA, Bennett J. 2014. A common fungal volatile organic compound induces a nitric oxide mediated inflammatory response in Drosophila melanogaster. Sci. Rep 4:3833
    [Google Scholar]
  46. 46. 
    Inamdar AA, Hossain MM, Bernstein AI, Miller GW, Richardson JR, Bennett J 2013. Fungal-derived semiochemical 1-octen-3-ol disrupts dopamine packaging and causes neurodegeneration. PNAS 110:19561–66
    [Google Scholar]
  47. 47. 
    Inamdar AA, Masurekar P, Bennett J 2010. Neurotoxicity of fungal volatile organic compounds in Drosophila melanogaster. Toxicol. Sci 117:418–26
    [Google Scholar]
  48. 48. 
    Inamdar AA, Moore J, Cohen R, Bennett J 2012. A model to evaluate the cytotoxicity of the fungal volatile organic compound 1-octen-3-ol in human embryonic stem cells. Mycopathologia 173:13–20
    [Google Scholar]
  49. 49. 
    Inst. Med 2004. Damp Indoor Spaces and Health Washington, DC: Natl. Acad.
  50. 50. 
    Jeleń H. 2003. Use of solid phase microextraction (SPME) for profiling fungal volatile metabolites. Lett. Appl. Microbiol. 36:263–67
    [Google Scholar]
  51. 51. 
    Jeleń H, Błaszczyk L, Chełkowski J, Rogowicz K, Strakowska J 2014. Formation of 6-n-pentyl-2H-pyran-2-one (6-PAP) and other volatiles by different Trichoderma species. Mycol. Progress 13:589–600
    [Google Scholar]
  52. 52. 
    Jelen H, Latus-Zierkiewicz D, Wasowicz E, Kaminski E 1997. Trichodiene as a volatile marker for trichothecenes biosynthesis. J. Microbiol. Methods 31:45–49
    [Google Scholar]
  53. 53. 
    Jelen H, Mirocha C, Wasowicz E, Kaminshki E 1995. Production of volatiles sesquiterpenes by Fusarium sambucinum strains with different abilities to synthesize trichotehecenes. Appl. Environ. Microbiol. 61:3815–20
    [Google Scholar]
  54. 54. 
    Jelen H, Wasowicz E. 1998. Volatile fungal metabolites and their relation to the spoilage of agricultural commodities. Food Rev. Int. 14:391–426
    [Google Scholar]
  55. 55. 
    Kaminski E, Libbey L, Stawicki S, Wasowicz E 1972. Identification of the predominant volatile compounds produced by Aspergillus flavus. Appl. Microbiol 24:721–26
    [Google Scholar]
  56. 56. 
    Kauhanen E, Harri M, Nevalainen A, Nevalainen T 2002. Validity of detection of microbial growth in buildings by trained dogs. Environ. Int. 28:153–57
    [Google Scholar]
  57. 57. 
    Keller NP, Turner G, Bennett J 2005. Fungal secondary metabolism—from biochemistry to genomics. Nat. Rev. Microbiol. 3:937–47
    [Google Scholar]
  58. 58. 
    Khaldi N, Seifuddin F, Turner G, Haft D, Nierman W et al. 2010. SMURF: genomic mapping of fungal secondary metabolite clusters. Fungal Genet. Biol. 47:736–41
    [Google Scholar]
  59. 59. 
    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 73:35–37
    [Google Scholar]
  60. 60. 
    Kitamoto K. 2002. Molecular biology of the Koji molds. Adv. Appl. Microbiol. 51:129–53
    [Google Scholar]
  61. 61. 
    Kline D, Allan S, Bernier U, Welch C 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, U.S.A. Med. Vet. Entomol. 21:323e331
    [Google Scholar]
  62. 62. 
    Koo S, Thomas H, Daniels S, Lynch R, Fortier S et al. 2014. A breath fungal secondary metabolite signature to diagnose invasive aspergillosis. Clin. Infect. Dis. 59:1733–40
    [Google Scholar]
  63. 63. 
    Korpi A, Järnberg J, Pasanen A 2009. Microbial volatile organic compounds. Crit. Rev. Toxicol. 39:139–93
    [Google Scholar]
  64. 64. 
    Korpi A, Kasanen JP, Pasanen AL 1999. Sensory irritation of microbially produced volatile organic compounds in mice during repeated exposures. Proceedings of the 3rd International Conference: Bioaerosols, Fungi and Mycotoxins; Health Effects, Assessment, Prevention and Control E Johanning 106–11 Albany, NY: Boyd
    [Google Scholar]
  65. 65. 
    Korpi A, Pasanen AL, Pasanen P 1998. Volatile compounds originating from mixed microbial cultures on building materials under various humidity conditions. Appl. Environ. Microbiol. 64:2914–19
    [Google Scholar]
  66. 66. 
    Kottb M, Gigolashvili T, Großkinsky DK, Piechulla P 2015. Trichoderma volatiles effecting Arabidopsis: from inhibition to protection against phytopathogenic fungi. Front. Microbiol. 6:995
    [Google Scholar]
  67. 67. 
    Kreja L, Seidel H. 2002. Evaluation of the genotoxic potential of some microbial volatiles organic compounds (MVOC) with the comet assay, the micronucleus assay and the HPRT gene mutation assay. Mut. Res. 513:143–50
    [Google Scholar]
  68. 68. 
    Kreja L, Seidel H. 2002. On the cytotoxicity of some microbial volatile organic compounds as studied in the human lung cell line A549. Chemosphere 49:105–10
    [Google Scholar]
  69. 69. 
    Kuske M, Roman A, Nicholas J 2005. Microbial volatile organic compounds as indicators of fungi: Can an electronic nose detect fungi in indoor environments. Build Environ 40:824–31
    [Google Scholar]
  70. 70. 
    Larsen TO, Frisvad JC. 1995. Comparison of different methods for collection of volatile chemical markers from fungi. J. Microbiol. Methods 24:135–44
    [Google Scholar]
  71. 71. 
    LeBouf RF, Schuckers S, Rossner A 2010. Preliminary assessment of a model to predict mold contamination based on microbial volatile organic compound profiles. Sci. Total Environ. 408:3648–53
    [Google Scholar]
  72. 72. 
    Lee S, Behringer G, Hung R, Bennett J 2018. Effects of fungal volatile organic compounds on Arabidopsis thaliana growth and gene expression. Fungal Ecol 37:1–9
    [Google Scholar]
  73. 73. 
    Lemfack MC, Gohlke BO, Toguem SMT, Preissner S, Piechulla B et al. 2018. mVOC 2.0: a database of microbial volatiles. Nucleic Acids Res 46:D1261–65
    [Google Scholar]
  74. 74. 
    Li N, Wang W, Bitas V, Subbarao K, Liu X et al. 2018. Volatile compounds emitted by diverse Verticillium species enhance plant growth by manipulating auxin signaling. Mol. Plant Microbe Interact. 31:1021–31
    [Google Scholar]
  75. 75. 
    Lomascolo A, Stentelaire C, Asther M, Lesage-Meessen L 2009. Basidiomycetes as new biotechnological tools to generate natural aromatic flavours for the food industry. Trends Biotechnol 17:282–89
    [Google Scholar]
  76. 76. 
    Longo MA, Sanroman MA. 2006. Production of food aroma compounds: microbial and enzymatic methodologies. Food Technol. Biotechnol. 44:335–53
    [Google Scholar]
  77. 77. 
    Luntz A. 2003. Arthropod semiochemicals: mosquitoes, midges and sealice. Biochem. Soc. Trans. 31:128–33
    [Google Scholar]
  78. 78. 
    Maarse H. 1991. Volatile Compounds in Foods and Beverages New York: CRC
  79. 79. 
    Mansurova M, Ebert BE, Blank LS, Ibanez A 2018. A breath of information: the volatilome. Curr. Genet. 64:959–64
    [Google Scholar]
  80. 80. 
    Mau L, Chyau C, Li J, Tseng Y 1997. Flavor compounds in straw mushrooms Volvariella volvacea harvest at different stages of maturity. J. Agric. Food Chem. 45:4726–29
    [Google Scholar]
  81. 81. 
    Mercier J, Jimenez I. 2007. Potential of the volatile-producing fungus Muscodor albus for control of building molds. Can. J. Microbiol. 53:404–10
    [Google Scholar]
  82. 82. 
    Mercier J, Jimenez-Santamaria J, Tamez-Guerra P 2007. Development of the volatile-producing fungus Muscodor albus Worapong, Strobel and Hess as a novel antimicrobial biofumigant. Rev. Mexicana Fitopatol. 25:173–79
    [Google Scholar]
  83. 83. 
    Morawicki RO, Beelman RB, Peterson D 2005. Recovery and purification of 10-oxo-trans-8-decenoic acid enzymatically produced using a crude homogenate of Agaricus bisporus. J. Food Sci 70:490–94
    [Google Scholar]
  84. 84. 
    Mosandl A, Heusinger G, Gessner M 1986. Analytical and sensory differentiation of 1-octen-3-ol enantiomers. J. Agric. Food Chem. 34:119–22
    [Google Scholar]
  85. 85. 
    Nakajima D, Ishii R, Kageyama S, Onji Y, Mineki S et al. 2006. Genotoxicity of microbial volatile organic compounds. J. Health Sci. 52:148–53
    [Google Scholar]
  86. 86. 
    Natl. Acad. Sci 2017. Microbiomes of the Built Environment: A Research Agenda for Indoor Microbiology, Human Health and Buildings Washington, DC: Natl. Acad.
  87. 87. 
    Nemcovic M, Jakubíková L, Víden I, Farkas V 2008. Induction of conidiation by endogenous volatile compounds in Trichoderma spp. FEMS Microbiol. Lett. 284:231–36
    [Google Scholar]
  88. 88. 
    Neri F, Mari M, Brigati S, Bertolini P 2007. Fungicidal activity of plant volatile compounds for controlling Monilinia laxa in stone fruit. Plant. Dis. 91:30–35
    [Google Scholar]
  89. 89. 
    Newell SY. 1992. Estimating fungal biomass and productivity in decomposing litter. The Fungal Community—Its Organization and Role in the Ecosystem GC Caroll, DT Wicklow 521–61 New York: Marcel Dekker, 2nd ed..
    [Google Scholar]
  90. 90. 
    Nijssen C, Visscher C, Maarse H, Willemsens L, Boehms M 1996. Volatiles Compounds in Food: Qualitative and Quantitative Data Zeist, Neth: TNO-CIVO Food Anal. Inst. , 7th ed..
  91. 91. 
    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 Protect. 66:1503–5
    [Google Scholar]
  92. 92. 
    Pacioni G. 1991. Effects of Tuber metabolites on the rhizospheric environment. Mycol. Res. 95:1355–58
    [Google Scholar]
  93. 93. 
    Padhi S, Dias I, Bennett J 2016. Two volatile-phase alcohols inhibit growth of Pseudogymnoascus destructans, causative agent of white-nose syndrome in bats. Mycology 8:11–16
    [Google Scholar]
  94. 94. 
    Perl T, Jünger M, Vautz W, Nolte J, Kuhns M et al. 2011. Detection of characteristic metabolites of Aspergillus fumigatus and Candida species using ion mobility spectrometry-metabolic profiling by volatile organic compounds. Mycoses 54:e828–37
    [Google Scholar]
  95. 95. 
    Piechulla B, Lemfack MC, Kai M 2017. Effects of discrete bioactive microbial volatiles on plants and fungi. Plant Cell Environ 40:2042–67
    [Google Scholar]
  96. 96. 
    Ramsbottom J. 1953. Mushrooms and Toadstools: A Study of the Activities of Fungi London, UK: Collins
  97. 97. 
    Rolfe RT, Rolfe FW. 2014. The Romance of the Fungus World: An Account of Fungus Life in Its Numerous Guises, Both Real and Legendary Mineola, NY: Dover
  98. 98. 
    Roze L, Beaudry R, Arthur A, Calvo A, Linz J 2007. Aspergillus volatiles regulate aflatoxin synthesis and asexual sporulation in Aspergillus parasiticus. Appl. Environ. Microbiol 73:7268–76
    [Google Scholar]
  99. 99. 
    Roze L, Calvo A, Gunterus A, Beaudry R, Kail M, Linz E 2004. Ethylene modulates development and toxin biosynthesis in Aspergillus possibly via an ethylene sensor-mediated signaling pathway. J. Food Prot. 67:438–47
    [Google Scholar]
  100. 100. 
    Russell G, Hills J. 1971. Odor differences between enantiomeric isomers. Science 172:1043–44
    [Google Scholar]
  101. 101. 
    Sahlberg B, Norback D. 2013. Airborne molds and bacteria, microbial volatile organic compounds (MVOC), plasticizers and formaldehyde in dwellings in three North European cities in relation to sick building syndrome (SBS). Sci. Total Environ. 444:433–40
    [Google Scholar]
  102. 102. 
    Sardans J, Penuelas J, Rivas-Ubach A 2011. Ecological metabolomics: overview of current developments and future challenges. Chemoecology 21:191–225
    [Google Scholar]
  103. 103. 
    Schiestl P, Steinebrunner F, Schulz C, Von Reuss S, Francke W et al. 2006. Evolution of ‘pollinator’—attracting signals in fungi. Biol. Lett. 2:401–4
    [Google Scholar]
  104. 104. 
    Schleibinger H, Laussmann D, Bornehag CG, Eis D, Rueden H 2008. Microbial volatile organic compounds in the air of moldy and mold-free indoor environments. Indoor Air 18:113–24
    [Google Scholar]
  105. 105. 
    Schnurer J, Olsson J, Borjesson T 1999. Fungal volatiles as indicators of food and feeds spoilage. Fungal Genet. Biol. 27:209–17
    [Google Scholar]
  106. 106. 
    Schöller CE, Gürtler H, Pedersen R, Molin S, Wilkins K 2002. Volatile metabolites from actinomycetes. J. Agric. Food Chem. 50:2615–21
    [Google Scholar]
  107. 107. 
    Schulz S, Dickschat J. 2007. Bacterial volatiles: the smell of small organisms. Nat. Prod. Rep. 24:814–42
    [Google Scholar]
  108. 108. 
    Seifert R, King A. 1982. Identification of some volatile constituents of Aspergillus clavatus. J. Agric. Food Chem 30:786–90
    [Google Scholar]
  109. 109. 
    Sexton AC, Howlett BJ. 2006. Parallels in fungal pathogenesis on plant and animal hosts. Eukaryot. Cell 5:1941–49
    [Google Scholar]
  110. 110. 
    Shirasu M, Touhara K. 2011. The scent of disease: volatile organic compounds of the human body related to disease and disorder. J. Biochem. 150:257–66
    [Google Scholar]
  111. 111. 
    Sneeden E, Harris H, Pickering I, Prince R, Johnson S et al. 2004. The sulfur chemistry of shiitake mushroom. J. Amer. Chem. Soc. 126:458–59
    [Google Scholar]
  112. 112. 
    Splivallo R, Novero M, Bertea C, Bossi S, Bonfante P 2007. Truffle volatiles inhibit growth and induce an oxidative burst in Arabidopsis thaliana. New Phytol 175:417–24
    [Google Scholar]
  113. 113. 
    Splivallo R, Ottonello S, Mello A, Karlovsky P et al. 2011. Truffle volatiles: from chemical ecology to aroma biosynthesis. New Phytol 189:688–99
    [Google Scholar]
  114. 114. 
    Splivallo R, Valdez N, Kirchhoff N, Ona MC, Schmidt JP et al. 2012. Intraspecific genotypic variability determines concentrations of key truffle volatiles. New Phytol 194:823–35
    [Google Scholar]
  115. 115. 
    Steinkraus KH 1996. Handbook of Indigenous Fermented Foods New York: Marcel Dekker. , 2nd ed..
  116. 116. 
    Strobel G. 2006. Harnessing endophytes for industrial microbiology. Curr. Opin. Microbiol. 9:240–44
    [Google Scholar]
  117. 117. 
    Strobel GA, Dirkse E, Sears J, Markworth C 2001. Volatile antimicrobials from Muscodor albus, a novel endophytic fungus. Microbiology 147:2943–50
    [Google Scholar]
  118. 118. 
    Tsitsigiannis DI, Keller N. 2007. Oxylipins as developmental and host-fungal communication signals. Trends Microbiol 15:109–18
    [Google Scholar]
  119. 119. 
    Venkateshwarlu G, Chandravadana MV, Tewari RP, Selvaraj Y 2000. Volatile flavor compounds from oyster mushroom (Pleurotus florida) in submerged culture. Flavour Fragr. J. 15:320–22
    [Google Scholar]
  120. 120. 
    Wålinder R, Ernstgård L, Johanson G, Norbäck D, Venge P, Wieslander G 2005. Acute effects of a fungal volatile compound. Environ. Health Perspect. 113:1775–78
    [Google Scholar]
  121. 121. 
    Wålinder R, Ernstgård L, Norbäck D, Wieslander G, Johanson G 2008. Acute effects of 1-octen-3-ol, a microbial volatile organic compound (MVOC)—an experimental study. Toxicol. Lett. 181:141–47
    [Google Scholar]
  122. 122. 
    Wilson AD, Baietto M. 2011. Advances in electronic-nose technologies developed for biomedical applications. Sensors 11:1105–76
    [Google Scholar]
  123. 123. 
    World Health Organ 2009. Guidelines for Indoor Air Quality: Dampness and Mold Copenhagen: World Health Organ.
  124. 124. 
    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 794:25–30
    [Google Scholar]
  125. 125. 
    Yamada Y, Ohtani K, Imajo A, Izu H, Nakamura H, Shiraishi K 2015. Comparison of the neurotoxicities between volatile organic compounds and fragrant organic compounds on human neuroblastoma SK-N-SH cells and primary cultured rat neurons. Toxicol. Rep. 2:729–36
    [Google Scholar]
  126. 126. 
    Yin G, Padhi S, Lee S, Hung R, Zhao G, Bennett J 2015. Effects of three volatile oxylipins on colony development in two species of fungi and on Drosophila larval metamorphosis. Curr. Microbiol. 71:347–56
    [Google Scholar]
  127. 127. 
    Zeringue H, Bhatnagar D, Cleveland T 1993. C15H24 volatile compounds unique to aflatoxigenic strains of Aspergillus flavus. Appl. Environ. Microbiol 59:31–51
    [Google Scholar]
  128. 128. 
    Zhang Z, Li G. 2010. A review of advances and new developments in the analysis of biological volatile organic compounds. Microchem. J. 95:127–39
    [Google Scholar]
  129. 129. 
    Zhao G, Yin G, Inamdar A, Luo J, Zhang N et al. 2016. Volatile organic compounds emitted by filamentous fungi isolated from flooded homes after Hurricane Sandy show toxicity in a Drosophila bioassay. Indoor Air 27:518–28
    [Google Scholar]
  130. 130. 
    Zhao L, Ni Y, Su M, Li H, Dong F et al. 2017. High throughput and quantitative measurement of microbial metabolome by gas chromatography/mass spectrometry using automated alkyl chloroformate derivatization. Anal. Chem. 89:5565–77
    [Google Scholar]
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