Abstract
A Penicillium decumbens strain was collected from a water-damaged building, and the production of microbial volatile organic compounds (MVOCs) was investigated by means of headspace solid-phase microextraction, followed by GC-MS analysis. The strain was characterized by a high production of (+)-thujopsene. The influence of various temperatures, relative humidity (RH) values, substrates, and inoculum concentrations on fungal growth and (+)-thujopsene production was studied. The optimal temperature and relative humidity for P. decumbens growth were 30°C and 100% RH, respectively. In general, the more favourable the incubation parameters were for growth, the faster maximum (+)-thujopsene production was reached. Moreover, the antifungal activity of thujopsene was tested against 16 fungal strains. The growth of five of these fungal strains was negatively affected both by thujopsene alone and when grown in contact with the MVOCs produced by P. decumbens. Following these results and since growth of P. decumbens itself was also inhibited by thujopsene, an autoregulatory function for this compound was proposed. Few data are present in the literature about chemical communication between fungi. The present research could, therefore, contribute to understanding fungal metabolism and behaviour in indoor environments.
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References
Larsen TO, Frisvad JC (1995) Characterization of volatile metabolites from 47 Penicillium taxa. Mycol Res 99(10):1153–1166
Jeleń HH, Latus-Zietkiewicz D, Wasowicz E, Kaminski E (1997) Trichodiene as a volatile marker for trichothecenes biosynthesis. J Microbiol Methods 31:45–49
Fischer G, Dott W (2003) Relevance of airborne fungi and their secondary metabolites for environmental, occupational and indoor hygiene. Arch Microbiol 179:75–82
Kita T, Nishi K, Fujimura M, Abo M, Ohka T, Yasui M, Ogawa H, Minato H, Kurumaya H, Nakao S (2003) A case of hypersensitivity pneumonitis caused by Humicola fuscoatra. Respirology 8:95–98
Sen B, Asan A (2009) Fungal flora in indoor and outdoor air of different residential houses in Tekirdag City (Turkey): seasonal distribution and relationship with climatic factors. Environ Monit Assess 151:209–219
Chen H, Jin S (2006) Effect of ethanol and yeast on cellulase activity and hydrolysis of crystalline cellulose. Enzyme Microb Technol 39:1430–1432
Yuan H, Yang J, Chen W (2006) Production of alkaline materials, surfactants and enzymes by Penicillium decumbens strain P6 in association with lignite degradation/solubilization. Fuel 85:1378–1382
Jimenez A, Borja R, Martin A, Raposo F (2005) Mathematical modelling of aerobic degradation of vinasses with Penicillium decumbens. Process Biochem 40:2805–2811
Kaufman DD, Blake J (1970) Degradation of atrazine by soil fungi. Soil Biol Biochem 2:73–80
Radosevich M, Traina SJ, Hao YL, Tuovinen OH (1995) Degradation and mineralization of atrazine by a soil bacterial isolate. Appl Environ Microbiol 61:297–302
Ghosh PK, Philip L (2006) Environmental significance of atrazine in aqueous systems and its removal by biological processes: an overview. Global NEST J 8:159–178
Crozier A, Clifford MN, Ashihara H (1981) Plant secondary metabolites. Occurrence, structure and role in the human diet. Blackwell, Oxford
Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827
Fäldt 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 25:567–590
Hynes J, Müller CT, Jones TH, Boddy L (2007) Changes in volatile production during the course of fungal mycelial interactions between Hypholoma fasciculare and Resinicium bicolor. J Chem Ecol 33:43–57
Barrero A, Quilez Del Moral J, Lara A, Mar Herrador M (2005) Antimicrobial activity of sesquiterpenes from the essential oil of Juniperus thurifera wood. Planta Med 71:67–71
Edrada RA, Wray V, Witte L, Van Ofwegen L, Proksch P (2000) Bioactive terpenes from the soft coral Heteroxenia sp. from Mindoro, Philippines. Zeitschrift für Naturforschung 55:82–86
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 11:844–854
Nakahara T (2009) Antimicrobial agents containing orange peel-derived terpene fractions and skin preparations containing the agents. Jpn Kokai Tokkyo Koho JP 2009114083 A 20090528
Wu C, Chien S, Wang S, Kuo Y, Chang S (2005) Structure-activity relationships of cadinane-type sesquiterpene derivatives against wood-decay fungi. Holzforschung 59(6):620–627
Kim JL, Elfman L, Mi Y, Wieslander G, Smedje G, Norbaeck D (2007) Indoor molds, bacteria, microbial volatile organic compounds and plasticizers in schools-associations with asthma and respiratory symptoms in pupils. Indoor Air 17:153–163
Maggi F, Cecchini C, Cresci A, Coman MM, Tirillini B, Sagratini G, Papa F (2009) Chemical composition and antimicrobial activity of the essential oil from Ferula glauca L. (F. communis L. subsp. glauca) growing in Marche (central Italy). Fitoterapia 80:68–72
Adams RP, Li S (2008) The botanical source of Chinese cedarwood oil: Cupressus funebris or Cupressaceae species? J Essent Oil Res 20:235–242
Srikrishna A, Anebouselvy K (2001) An enantiospecific approach to tricyclic sesquiterpenes mayurone and thujopsenes. J Org Chem 66:7102–7106
Matsuo A, Nakayama N, Nakayama M (1985) Enantiomeric type sesquiterpenoids of the liverwort Marchantia polymorpha. Phytochem 24(4):777–781
Chen F, Tholl D, D’auria JC, Farooq A, Pichersky E, Gershenzon J (2003) Biosynthesis and emission of terpenoid volatiles from Arabidopsis flowers. Plant Cell 15:481–494
Manter DK, Kelsey RG, Karchesy JJ (2007) Antimicrobial activity of extractable conifer heartwood compounds toward Phytophthora ramorum. J Chem Ecol 33(11):2133–2147
Polizzi V, Delmulle B, Adams A, Moretti A, Susca A, Picco AM, Rosseel Y, Kindt TR, Van Bocxlaer J, De Kimpe N, Van Peteghem C, De Saeger S (2009) Fungi, mycotoxins and microbial volatile organic compounds in mouldy interiors from water-damaged buildings. J Environ Monit 11:1849–1858
Ellis MB (1971) Dematiaceous hyphomycetes. Commonwealth Mycological Institute, Kew, Surrey
Ellis MB (1976) More dematiaceous hyphomycetes. Commonwealth Mycological Institute, Kew, Surrey
Pitt JI (1979) The genus Penicillium and its teleomorphic states Eupenicillium and Talaromyces. Academic, London
Klich MA (2002) Identification of common Aspergillus species. Centraalbureau voor Schimmelcultures, Utrecht
Chang JCS (1995) Growth evaluation of fungi (Penicillium and Aspergillus spp.) on ceiling tiles. Atmospheric Environ 29(17):2331–2337
Pasanen P, Korpi A, Kalliokoski P, Pasanen A (1997) Growth and volatile metabolite production of Aspergillus versicolor in house dust. Environ Int 23(4):425–432
Adams R (2007) Identification of essential oil components by gas chromatography/mass spectrometry. Allured, Illinois
Demyttenaere JCR, De Pooter HL (1998) Biotransformation of citral and nerol by spores of Penicillium digitatum. Flavour Fragr J 13:173–176
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 70:2823–2829
Börjesson T, Stöllman U, Schnürer J (1992) Volatile metabolites produced by six fungal species compared with other indicators of fungal growth on cereal grains. Appl Environ Microbiol 58:2599–2605
Elke K, Begerow J, Oppermann H, Kramer 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 1:445–452
Skaltsa HD, Demetzos C, Lazari D, Sokovic M (2003) Essential oil analysis and antimicrobial activity of eight Stachys species from Greece. Phytochemistry 64:743–752
Demyttenaere JCR, Moriña RM, De Kimpe N, Sandra P (2004) Use of headspace solid-phase microextraction and headspace sorptive extraction for the detection of the volatile metabolites produced by toxigenic Fusarium species. J Chromatogr A 1027:147–154
Wihlborg R, Pippitt D, Marsili R (2008) Headspace sorptive extraction and GC-TOFMS for the identification of volatile fungal metabolites. J Microbiol Methods 75:244–250
Li C, Krewer GW, Ji P, Scherm H, Kays SJ (2010) Gas sensor array for blueberry fruit disease detection and classification. Postharvest Biol Technol 55:144–149
Halim AF, Narciso JA, Collins RP (1975) Odorous constituents of Penicillium decumbens. Mycologia 67:1158–1165
Collins RP (1976) Terpenes and odoriferous materials from microorganisms. Lloydia 39(1):20–24
Nilsson T, Larsen TO, Montanarella L, Madsen JO (1996) Application of head-space solid-phase microextraction for the analysis of volatile metabolites emitted by Penicillium species. J Microbiol Methods 25:245–255
Vázquez BI, Fente C, Franco CM, Vazquez MJ, Cepeda A (2001) Inhibitory effects of eugenol and thymol on Penicillium citrinum strains in culture media and cheese. Int J Food Microbiol 67:157–163
Reddy CS, Reddy KRN, Prameela M, Mangala UN, Muralidharan K (2007) Identification of antifungal component in clove that inhibits Aspergillus sp. colonizing rice grains. J Mycol Plant Pathol 37:87–94
Tullio V, Nostro A, Mandras N, Dugo P, Banche G, Cannatelli MA, Cuffini AM, Alonzo V, Carlone NA (2007) Antifungal activity of essential oils against filamentous fungi determined by broth microdilution and vapour contact methods. J Appl Microbiol 102:1544–1550
Kumar A, Shukla R, Singh P, Dubey NK (2009) Biodeterioration of some herbal raw materials by storage fungi and aflatoxin and assessment of Cymbopogon flexuosus essential oil and its components as antifungal. Int Biodeterior Biodegradation 63:712–716
Bauer K, Garbe D, Surburg H (1990) Common fragrance and flavour materials: preparation, properties and uses. VCH, Weinheim
Lei H, Wang Y, Su C, Liang F, Su W, Hui M, Shaw P, Luo Y (2010) Chemical composition and antifungal activity of essential oils of Thuja sutchuenensis, a critically endangered species endemic to China. Nat Prod Commun 5(10):1673–1676
Kim SG, Ma EC, Je GH, Yoon SY (2009) A composition using antibacterial and antifunga containing Thujopsis dolobrata oil. Repub. Korean Kongkae Taeho Kongbo, Patent KR 2009020227 A 20090226
Hao C, Du X, Zhuang S, Ma B, Zhang X (2007) Chemical constituents and fungicidal activity of essential oil from Mikania micrantha. Xibei Zhiwu Xuebao 27(10):2097–2103
Hogan DA (2006) Talking to themselves: autoregulation and quorum sensing in fungi. Eukaryot Cell 5:613–619
Ugalde U (2006) Autoregulatory signals in mycelial fungi. In: Fischer R, Kües U (eds) The mycota, vol I. Springer, Berlin, pp 2035–2213
Breeuwer P, De Reu JC, Drocourt J, Rombouts FM, Abee T (1997) Nonanoic acid, a fungal self-inhibitor, prevents germination of Rhizopus oligosporus sporangiospores by dissipation of the ph gradient. Appl Environ Microbiol 63(1):178–185
Macko V, Staples RC, Gershon H, Renwick JAA (1970) Self-inhibitor of bean rust uredospores: methyl 3,4-dimethoxycinnamate. Science 170:539–540
Macko V, Staples RC (1973) Regulation of uredospore germination and germ tube development. Bull Torrey Bot Club 100:223–229
Allen PJ (1976) Spore germination and its regulation. In: Heitefuss R, Williams PH (eds) Encyclopedia of plant physiology, vol 4. Springer, Berlin, pp 51–85
Nemcovic M, Jakubikova L, Viden I, Farkas V (2008) Induction of conidiation by endogenous volatile compounds in Trichoderma spp. FEMS Microbiol Lett 284:231–236
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 54:67–75
Claeson A, Levin J, Blomquist G, Sunesson A (2002) Volatile metabolites from microorganisms grown on humid building materials and synthetic media. J Environ Monit 4:667–672
Moularat S, Robine E, Ramalho O, Oturan MA (2008) Detection of fungal development in a closed environment through the identification of specific VOC: demonstration of a specific VOC fingerprint for fungal development. Sci Total Environ 407:139–146
Van Lancker F, Adams A, Delmulle B, De Saeger S, Moretti A, Van Peteghem C, De Kimpe N (2008) Use of headspace SPME-GC-MS for the analysis of the volatiles produced by indoor molds grown on different substrates. J Environ Monit 10:1127–1133
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The authors are indebted to the Research Foundation Flanders (FWO-Vlaanderen) for financial support (research project G.0034.07) and for a Postdoctoral Fellowship of A. Adams.
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Polizzi, V., Fazzini, L., Adams, A. et al. Autoregulatory Properties of (+)-Thujopsene and Influence of Environmental Conditions on Its Production by Penicillium decumbens . Microb Ecol 62, 838–852 (2011). https://doi.org/10.1007/s00248-011-9905-9
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DOI: https://doi.org/10.1007/s00248-011-9905-9