Biotechnology Letters

, Volume 36, Issue 7, pp 1503–1513 | Cite as

Quorum sensing activity and control of yeast-mycelium dimorphism in Ophiostoma floccosum

  • Alexander Berrocal
  • Claudia Oviedo
  • Kenneth W. Nickerson
  • José Navarrete
Original Research Paper


Quorum sensing (QS) activity in Ophiostoma fungi has not been described. We have examined the growth conditions on the control of dimorphism in Ophiostoma floccosum, an attractive biocontrol agent against blue-stain fungi, and its relationship with QS activity. In a defined culture medium with l-proline as the N source, a high inoculum size (107 c.f.u. ml−1) was the principal factor that promoted yeast-like growth. Inoculum size effect can be explained by the secretion of a QS molecule(s) (QSMs) responsible for inducing yeast morphology. QSM candidates were extracted from spent medium and their structure was determined by GC–MS. Three cyclic sesquiterpenes were found. The most abundant molecule, and therefore the principal candidate to be the QSM responsible for yeast growth of O. floccosum, was 1,1,4a-trimethyl-5,6-dimethylene-decalin (C15H24). Other two compounds were also detected.


Cyclic sesquiterpenes Fungal dimorphism Inoculum size Ophiostoma floccosum Quorum sensing molecules Trimethyl-dimethylene-decalin 



The principal author would like to thank the personal of the Laboratory of Biodegradation in the Department of Wood Engineering at the University of Bio–Bio (Chile) for all support. To the Graduate School and Department of Wood Engineering at the University of Bio–Bio, the OEA Scholarship Program and the Scholarship Program of the Technology Institute of Costa Rica for providing the funds to carry out this research. We also thank Ph.D. Juanita Freer and Susana Casas from the Laboratory of Renewable Resources at the University of Concepcion for providing the facilities for GC–MS analyses.


  1. Abbassy MA, Marei GI (2013) Antifungal and chemical composition of essential oils of Juniperus communis L. and Thymus vulgaris L. against two phytopathogenic fungi. J Appl Sci Res 9:4584–4588Google Scholar
  2. Azuma H, Toyota M, Asakawa Y, Kawano S (1996) Naphthalene—constituent of magnolia flowers. Phytochemistry 42:999–1004CrossRefGoogle Scholar
  3. Berrocal A, Navarrete J, Oviedo C (2012a) Efecto de diferentes condiciones de crecimiento en el dimorfismo levadura-micelio de la cepa albina PcF2A29 de la especie Ophiostoma piceae. Maderas-Cienc Tecnol 14:91–102CrossRefGoogle Scholar
  4. Berrocal A, Navarrete J, Oviedo C, Nickerson KW (2012b) Quorum sensing activity in Ophiostoma ulmi: effects of fusel oils and branched chain amino acids on yeast-mycelial dimorphism. J Appl Microbiol 113:126–134PubMedCrossRefGoogle Scholar
  5. Bisht A, Bisht GRS, Singh M, Gupta R, Singh V (2011) Chemical compsition and antimicrobial activity of essential oil of tubers of Cyperus rotundus Linn. collected from Dehradun (Uttarakhand). J Pharm Biomed Sci 2:661–665Google Scholar
  6. Chang-Bin W, Sheng-Hui L, Yu-Ge L, Ling-Ling L, Wen-Xiu Y, Guang-Ming S (2011) Characteristic aroma compounds from different pineapple parts. Molecules 16:5104–5112CrossRefGoogle Scholar
  7. Chen H, Fink GR (2006) Feedback control of morphogenesis in fungi by aromatic alcohols. Gene Dev 20:1150–1161PubMedCentralPubMedCrossRefGoogle Scholar
  8. Chen J, Henderson G, Grimm CC, Lloyd SW, Laine RA (1998) Termites fumigate their nests with naphthalene. Nature 392:558–559CrossRefGoogle Scholar
  9. Chen H, Fujita M, Feng Q, Clardy J, Fink GR (2004) Tyrosol is a quorum sensing molecule in Candida albicans. Proc Natl Acad Sci USA 101:5048–5052PubMedCentralPubMedCrossRefGoogle Scholar
  10. Daisy BH, Strobel GA, Castillo U, Ezra D, Sears J, Weaver DK, Runyon JB (2002) Naphthalene, an insect repellent, is produced by Muscodor vitigenus, a novel endophytic fungus. Microbiology 148:3737–3741PubMedGoogle Scholar
  11. Ezra D, Hess WM, Strobel GA (2004) New endophytic isolates of Muscodor albus, a volatile-antibiotic-producing fungus. Microbiology 150:4023–4031PubMedCrossRefGoogle Scholar
  12. Ghosh S, Kebaara BW, Atkin AL, Nickerson KW (2008) Regulation of aromatic alcohol production in Candida albicans. Appl Environ Microb 74:7211–7218CrossRefGoogle Scholar
  13. Hanssen HP (1993) Volatile metabolites produced by species of Ophiostoma and Ceratocystis. In: Wingfield MJ, Seifert KA, Webber JF (eds) Ceratocystis and ophiostoma: taxonomy ecology and pathogenicity. APS Press, St. Paul, pp 117–125Google Scholar
  14. Hanssen HP, Abraham WR (1988) Sesquiterpene alcohols with novel skeletons from the fungus Ceratocystis piceae (Ascomycotina). Tetrahedron 44:2175–2180CrossRefGoogle Scholar
  15. Hanssen HP, Sprecher E, Abraham WR (1986) 6-protoilludene, the major volatile metabolite from Ceratocystis piceae liquid cultures. Phytochemistry 25:1979–1980CrossRefGoogle Scholar
  16. Hernández V, Avramidis S, Navarrete J (2012) Albino strains of Ophiostoma spp. fungi effect on radiata pine permeability. Eur J Wood Prod 70:551–556CrossRefGoogle Scholar
  17. Hogan DA (2006) Talking to themselves: autoregulation and quorum sensing in fungi. Eukaryot Cell 5:613–619PubMedCentralPubMedCrossRefGoogle Scholar
  18. Hornby JM, Jensen E, Lisec AD, Tasto JJ, Jahnke B, Shoemaker R, Dussault P, Nickerson KW (2001) Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl Environ Microb 67:2982–2992CrossRefGoogle Scholar
  19. Hornby JM, Jacobitz-Kizzier SM, McNeel DJ, Jensen EC, Treves DS, Nickerson KW (2004) Inoculum size effect in dimorphic fungi: extracellular control of yeast-mycelium dimorphism in Ceratocystis ulmi. Appl Environ Microb 70:1356–1359CrossRefGoogle Scholar
  20. Karamian R, Asadbegy M, Pakzad R (2013) Essential oil compositions and in vitro antioxidant and antibacterial activities of the methanol extracts of two Salvia species (Lamiaceae) from Iran. Intl J Agri Crop Sci 5:1171–1182Google Scholar
  21. Kramer R, Abraham WR (2012) Volatile sesquiterpenes from fungi: what are they good for? Phytochem Rev 11:15–37CrossRefGoogle Scholar
  22. Kulkarni RK, Nickerson KW (1981) Nutritional control of dimorphism in Ceratocystis ulmi. Exp Mycol 5:148–154CrossRefGoogle Scholar
  23. March JC, Bentley WE (2004) Quorum sensing and bacterial cross-talk in biotechnology. Curr Opin Biotechnol 15:495–502PubMedCrossRefGoogle Scholar
  24. Morath SU, Hung R, Bennett JW (2012) Fungal volatile organic compounds: a review with emphasis on their biotechnological potential. Fungal Biol Rev 26:73–83CrossRefGoogle Scholar
  25. Muthukamar G, Nickerson KW (1984) Ca(II)-Calmodulin regulation of fungal dimorphism in Ceratocystis ulmi. J Bacteriol 159:390–392Google Scholar
  26. Nickerson KW, Atkin AL, Hornby JM (2006) Quorum sensing in dimorphic fungi: farnesol and beyond. Appl Environ Microb 72:3805–3813CrossRefGoogle Scholar
  27. Pednekar PP, Vakil BV, Sane RT, Datar AG (2013) Phytochemical profile and antioxidant activity of the essential oil from Blumea eriantha DC. Int J Pharm Sci 5:404–413Google Scholar
  28. Sacchettini JC, Poulter CD (1997) Creating isoprenoid diversity. Science 277:1788–1789PubMedCrossRefGoogle Scholar
  29. Sarsenbayev KN, Sarsenbayeva AB, Balmukanov KU (2013) chemical composition of low-molecular weight organic compounds (LMWOC) of water extracts from Cistanche Deserticola stolones depending on treatment. World Appl Sci J 25:28–35Google Scholar
  30. Shafaghat A (2009) Composition and antibacterial activity of the volatile oils from different parts of Achillea tenuifolia Lam. from Iran. J Med Plants Res 8:93–98Google Scholar
  31. Sprague GF Jr, Winans SC (2006) Eukaryotes learn how to count: quorum sensing by yeast. Gene Dev 20:1045–1049PubMedCrossRefGoogle Scholar
  32. Waksman SA (1941) Antagonistic relations of microorganisms. Bacteriol Rev 5:231–291PubMedCentralPubMedGoogle Scholar
  33. Zeringue HJ Jr, Bhatnagar D, Cleveland TE (1993) C15H24 volatile compounds unique to aflatoxigenic strains of Aspergillus flavus. Appl Environ Microb 59:2264–2270Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Alexander Berrocal
    • 1
  • Claudia Oviedo
    • 2
  • Kenneth W. Nickerson
    • 3
  • José Navarrete
    • 4
  1. 1.Escuela de Ingeniería ForestalInstituto Tecnológico de Costa RicaCartagoCosta Rica
  2. 2.Departamento de Química, Facultad de CienciasUniversidad del Bío BíoConcepciónChile
  3. 3.School of Biological SciencesUniversity of NebraskaLincolnUSA
  4. 4.Departamento de Ingeniería en Maderas, Facultad de IngenieríaUniversidad del Bío BíoConcepciónChile

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