[en] Quorum sensing (QS) is often defined as a mechanism of microbial communication that can regulate microbial behaviors in accordance with population density. Much is known about QS mechanisms in bacteria, but fungal QS research is still in its infancy. In this study, the molecules constituting the volatolomes of the plant pathogenic fungi Fusarium culmorum and Cochliobolus sativus have been identified during culture conditions involving low and high spore concentrations, with the high concentration imitating overpopulation conditions (for QS stimulation). We determined that volatolomes emitted by these species in conditions of overpopulation have a negative impact on their mycelial growth, with some of the emitted molecules possibly acting as QSM. Candidate VOCs related to QS have then been identified by testing the effect of individual volatile organic compounds (VOCs) on mycelial growth of their emitting species. The antifungal effect observed for the volatolome of F. culmorum in the overpopulation condition could be attributed to ethyl acetate, 2-methylpropan-1-ol, 3-methylbutyl ethanoate, 3-methylbutan-1-ol, and pentan-1-ol, while it could be attributed to longifolene, 3-methylbutan-1-ol, 2-methylpropan-1-ol, and ethyl acetate for C. sativus in the overpopulation condition. This work could pave the way to a sustainable alternative to chemical fungicides.
Disciplines :
Agriculture & agronomy Chemistry
Author, co-author :
De Clerck, Caroline ; Université de Liège - ULiège > TERRA Research Centre > Plant Sciences
Josselin, Laurie ; Université de Liège - ULiège > TERRA Research Centre
Barriuso J. Hogan D.A. Keshavarz T. Martínez M.J. Role of quorum sensing and chemical communication in fungal biotechnology and pathogenesis FEMS Microbiol. Rev. 2018 42 627 638 10.1093/femsre/fuy022
Miller M.B. Bassler B.L. Quorum sensing in bacteria Annu. Rev. Microbiol. 2001 55 165 199 10.1146/annurev.micro.55.1.165 11544353
Barriuso J. Quorum sensing mechanisms in fungi AIMS Microbiol. 2015 1 37 47 10.3934/microbiol.2015.1.37
Williams P. Quorum sensing, communication and cross-kingdom signalling in the bacterial world Microbiology 2007 153 3923 3938 10.1099/mic.0.2007/012856-0 18048907
Albuquerque P. Casadevall A. Quorum sensing in fungi a review Med. Mycol. 2012 50 337 345 10.3109/13693786.2011.652201
Hornby J.M. Jensen E.C. Lisec A.D. Tasto J.J. Jahnke B. Shoemaker R. Dussault P. Nickerson K.W. Quorum Sensing in the Dimorphic Fungus Candida albicans Is Mediated by Farnesol Appl. Environ. Microbiol. 2001 67 2982 2992 10.1128/AEM.67.7.2982-2992.2001
Lingappa B.T. Prasad M. Lingappa Y. Hunt D.F. Biemann K. Phenethyl alcohol and tryptophol: Autoantibiotics produced by the fungus Candida albicans Science 1969 163 192 194 10.1126/science.163.3863.192
Kügler S. Sebghati T.S. Eissenberg L.G. Goldman W.E. Phenotypic variation and intracellular parasitism by Histoplasma capsulatum Proc. Natl. Acad. Sci. USA 2000 97 8794 8798 10.1073/pnas.97.16.8794
Hornby J.M. Jacobitz-Kizzier S.M. McNeel D.J. Jensen E.C. Treves D.S. Nickerson K.W. Inoculum Size Effect in Dimorphic Fungi: Extracellular Control of Yeast-Mycelium Dimorphism in Ceratocystis ulmi Appl. Environ. Microbiol. 2004 70 1356 1359 10.1128/AEM.70.3.1356-1359.2004
Roca M.G. Arlt J. Jeffree C.E. Read N.D. Cell biology of conidial anastomosis tubes in Neurospora crassa Eukaryot. Cell 2005 4 911 919 10.1128/EC.4.5.911-919.2005
Severin F.F. Meer M.V. Smirnova E.A. Knorre D.A. Skulachev V.P. Natural causes of programmed death of yeast Saccharomyces cerevisiae Biochim. Biophys. Acta-Mol. Cell Res. 2008 1783 1350 1353 10.1016/j.bbamcr.2008.02.001 18319066
Lee H. Chang Y.C. Nardone G. Kwon-Chung K.J. TUP1 disruption in Cryptococcus neoformans uncovers a peptide-mediated density-dependent growth phenomenon that mimics quorum sensing Mol. Microbiol. 2007 64 591 601 10.1111/j.1365-2958.2007.05666.x
Berrocal A. Oviedo C. Nickerson K.W. Navarrete J. Quorum sensing activity and control of yeast-mycelium dimorphism in Ophiostoma floccosum Biotechnol. Lett. 2014 36 1503 1513 10.1007/s10529-014-1514-5 24737073
Williams H.E. Steele J.C.P. Clements M.O. Keshavarz T. γ-Heptalactone is an endogenously produced quorum-sensing molecule regulating growth and secondary metabolite production by Aspergillus nidulans Appl. Microbiol. Biotechnol. 2012 96 773 781 10.1007/s00253-012-4065-5 22543352
Horowitz Brown S. Zarnowski R. Sharpee W.C. Keller N.P. Morphological transitions governed by density dependence and lipoxygenase activity in Aspergillus flavus Appl. Environ. Microbiol. 2008 74 5674 5685 10.1128/AEM.00565-08
Raina S. Odell M. Keshavarz T. Quorum sensing as a method for improving sclerotiorin production in Penicillium sclerotiorum J. Biotechnol. 2010 148 91 98 10.1016/j.jbiotec.2010.04.009
Vitale S. Di Pietro A. Turrà D. Autocrine pheromone signalling regulates community behaviour in the fungal pathogen Fusarium oxysporum Nat. Microbiol. 2019 4 1443 1449 10.1038/s41564-019-0456-z
Bartnicki-Garcia S. Nickerson W.J. Nutrition, Growth, and Morphogenesis of Muscor rouxii J. Bacteriol. 1962 84 841 858 10.1128/jb.84.4.841-858.1962
Muthukumar G. Jensen E.C. Nickerson A.W. Eckles M.K. Nickerson K.W. Photomorphogenesis in Penicillium isariaeforme: Exogenous calcium substitutes for light Photochem. Photobiol. 1991 53 287 291 10.1111/j.1751-1097.1991.tb03936.x
Gómez-Gil E. Franco A. Madrid M. Vázquez-Marín B. Gacto M. Fernández-Breis J. Vicente-Soler J. Soto T. Cansado J. Quorum sensing and stress-activated MAPK signaling repress yeast to hypha transition in the fission yeast schizosaccharomyces Japonicus PLoS Genet. 2019 15 e1008192 10.1371/journal.pgen.1008192
Mehmood A. Liu G. Wang X. Meng G. Wang C. Liu Y. Fungal quorum-sensing molecules and inhibitors with potential antifungal activity: A review Molecules 2019 24 1950 10.3390/molecules24101950
Trinidad V. Bouzas M. Developmental Biology in Prokaryotes and Lower Eukaryotes Springer Cham, Switzerland 2021 9783030775940
Chitarra G.S. Abee T. Rombouts F.M. Posthumus M.A. Dijksterhuis J. Germination of Penicillium paneum conidia is regulated by 1-octen-3-ol, a volatile self-inhibitor Appl. Environ. Microbiol. 2004 70 2823 2829 10.1128/AEM.70.5.2823-2829.2004 15128538
Chitarra G.S. Abee T. Rombouts F.M. Dijksterhuis J. 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. 2005 54 67 75 10.1016/j.femsec.2005.02.013 16329973
Morath S.U. Hung R. Bennett J.W. Fungal volatile organic compounds: A review with emphasis on their biotechnological potential Fungal Biol. Rev. 2012 26 73 83 10.1016/j.fbr.2012.07.001
Tian X. Ding H. Ke W. Wang L. Quorum Sensing in Fungal Species Annu. Rev. Microbiol. 2021 75 449 469 10.1146/annurev-micro-060321-045510 34348030
Franco A. Gacto M. Gómez-Gil E. Madrid M. Vicente-Soler J. Vázquez-Marín B. Cansado J. Soto T. Quorum Sensing: A Major Regulator of Fungal Development Developmental Biology in Prokaryotes and Lower Eukaryotes Villa T.G. de Miguel Bouzas T. Springer International Publishing Cham, Switzerland 2021 331 366 978-3-030-77595-7
Jamil M. Ali A. Ali N. Mujeeb-Kazi A. Spot Blotch in Bread Wheat: Virulence, Resistance, and Breeding Perspectives Elsevier Inc. Amsterdam, The Netherlands 2020 9780128195277
Scherm B. Balmas V. Spanu F. Pani G. Delogu G. Pasquali M. Migheli Q. Fusarium culmorum: Causal agent of foot and root rot and head blight on wheat Mol. Plant Pathol. 2013 14 323 341 10.1111/mpp.12011 23279114
Fiers M. Lognay G. Fauconnier M.L. Jijakli M.H. Volatile Compound-Mediated Interactions between Barley and Pathogenic Fungi in the Soil PLoS ONE 2013 8 e66805 10.1371/journal.pone.0066805 23818966
Smiley R.W. Gourlie J.A. Easley S.A. Patterson L.M. Whittaker R.G. Crop damage estimates for crown rot of wheat and barley in the Pacific Northwest Plant Dis. 2005 89 595 604 10.1094/PD-89-0595
Vandendool H. Kratz P.D. A generalization of the retention index system including linear temperature programmed gas-liquid partition chromatography J. Chromatogr. 1963 11 463 471 10.1016/S0021-9673(01)80947-X
Savel’Eva E.I. Gavrilova O.P. Gagkaeva T.Y. Study of the composition of volatile organic compounds emitted by the filamentous fungus Fusarium culmorum by gas chromatography-mass spectrometry combined with solid phase microextraction Russ. J. Gen. Chem. 2014 84 2603 2610 10.1134/S1070363214130180
Takeuchi T. Kimura T. Tanaka H. Kaneko S. Ichii S. Kiuchi M. Suzuki T. Analysis of volatile metabolites emitted by soil-derived fungi using head space solid-phase microextraction/gas chromatography/mass spectrometry: I. Aspergillus fumigatus, Aspergillus nidulans, Fusarium solani and Penicillium paneum Surf. Interface Anal. 2012 44 694 698 10.1002/sia.4870
Savelieva E.I. Gustyleva L.K. Kessenikh E.D. Khlebnikova N.S. Leffingwell J. Gavrilova O.P. Gagkaeva T.Y. Study of the Vapor Phase Over Fusarium Fungi Cultured on Various Substrates Chem. Biodivers. 2016 13 891 903 10.1002/cbdv.201500284 27253722
Lee S. Hung R. Yap M. Bennett J.W. Age matters: The effects of volatile organic compounds emitted by Trichodermaatroviride on plant growth Arch. Microbiol. 2015 197 723 727 10.1007/s00203-015-1104-5 25771960
Wang F. Cale J.A. Hussain A. Erbilgin N. Exposure to Fungal Volatiles Can Influence Volatile Emissions From Other Ophiostomatoid Fungi Front. Microbiol. 2020 11 567462 10.3389/fmicb.2020.567462 33042073
Rinkel J. Babczyk A. Wang T. Stadler M. Dickschat J.S. Volatiles from the hypoxylaceous fungi Hypoxylon griseobrunneum and Hypoxylon macrocarpum Beilstein J. Org. Chem. 2018 14 2974 2990 10.3762/bjoc.14.277
Ponce M.A. Lizarraga S. Bruce A. Kim T.N. Morrison W.R. Grain Inoculated with Different Growth Stages of the Fungus, Aspergillus flavus, Affect the Close-Range Foraging Behavior by a Primary Stored Product Pest, Sitophilus oryzae (Coleoptera: Curculionidae) Environ. Entomol. 2022 51 927 939 10.1093/ee/nvac061
Wu W. Tran W. Taatjes C.A. Alonso-Gutierrez J. Lee T.S. Gladden J.M. Rapid discovery and functional characterization of terpene synthases from four endophytic xylariaceae PLoS ONE 2016 11 e0146983 10.1371/journal.pone.0146983
Liu P. Cheng Y. Yang M. Liu Y. Chen K. Long C.A. Deng X. Mechanisms of action for 2-phenylethanol isolated from Kloeckera apiculata in control of Penicillium molds of citrus fruits BMC Microbiol. 2014 14 242 10.1186/s12866-014-0242-2
Korsak Z. Rydzyński K. Neurotoxic effects of acute and subchronic inhalation exposure to trimethylbenzene isomers (pseudocumene, mesitylene, hemimellitene) in rats Int. J. Occup. Med. Environ. Health 1996 9 341 349
Josselin L. De Clerck C. De Boevre M. Moretti A. Haïssam Jijakli M. Soyeurt H. Fauconnier M.L. Volatile organic compounds emitted by Aspergillus flavus strains producing or not aflatoxin B1 Toxins 2021 13 705 10.3390/toxins13100705
del Pilar Marquez-Villavicencio M. Weber B. Witherell R.A. Willis D.K. Charkowski A.O. The 3-hydroxy-2-butanone pathway is required for pectobacterium carotovorum pathogenesis PLoS ONE 2011 6 e22974 10.1371/journal.pone.0022974
Xiao Z. Lu J.R. Generation of acetoin and its derivatives in foods J. Agric. Food Chem. 2014 62 6487 6497 10.1021/jf5013902 25000216
Chen Y. Gozz K. Yan F. Chai Y. Acetic acid acts as a volatile signal to stimulate bacterial biofilm formation MBio 2015 6 406 408 10.1128/mBio.00392-15 26060272
Fialho M.B. de Moraes M.H.D. Tremocoldi A.R. Pascholati S.F. Potential of antimicrobial volatile organic compounds to control Sclerotinia sclerotiorum in bean seeds Pesqui. Agropecu. Bras. 2011 46 137 142 10.1590/S0100-204X2011000200004
Saeidi S. Hassanpour K. Ghamgosha M. Heiat M. Taheri R.A. Mirhosseini A. Farnoosh G. Antibacterial activity of ethyl acetate and aqueous extracts of Mentha longifolia L. and hydroalcoholic extract of Zataria multiflora Boiss. plants against important human pathogens Asian Pac. J. Trop. Med. 2014 7 S186 S189 10.1016/S1995-7645(14)60229-7
Ando H. Hatanaka K. Ohata I. Yamashita-Kitaguchi Y. Kurata A. Kishimoto N. Antifungal activities of volatile substances generated by yeast isolated from Iranian commercial cheese Food Control 2012 26 472 478 10.1016/j.foodcont.2012.02.017
Pimenta L. Ferreira M.A. Pedroso M.P. Campos V.P. Wood-associated fungi produce volatile organic compounds toxic to root-knot nematode Sci. Agric. 2017 74 303 310 10.1590/1678-992x-2015-0472
Chauhan N.M. Shinde R.B. Karuppayil S.M. Effect of alcohols on filamentation, growth, viability and biofilm development in Candida albicans Brazilian J. Microbiol. 2013 44 1315 1320 10.1590/S1517-83822014005000012
Micalizzi E.W. Mack J.N. White G.P. Avis T.J. Smith M.L. Microbial inhibitors of the fungus Pseudogymnoascus destructans, the causal agent of white-nose syndrome in bats PLoS ONE 2017 12 e0179770 10.1371/journal.pone.0179770
Zunino M.P. Herrera J.M. Pizzolitto R.P. Rubinstein H.R. Zygadlo J.A. Dambolena J.S. Effect of Selected Volatiles on Two Stored Pests: The Fungus Fusarium verticillioides and the Maize Weevil Sithophilus zeamais J. Agric. Food Chem. 2015 63 7743 7749 10.1021/acs.jafc.5b02315
Paul D. Park K.S. Identification of volatiles produced by Cladosporium cladosporioides CL-1, a fungal biocontrol agent that promotes plant growth Sensors 2013 13 13969 13977 10.3390/s131013969 24135990
Li Y.Y. Tan X.M. Yang J. Guo L.P. Ding G. Naturally Occurring seco-Sativene Sesquiterpenoid: Chemistry and Biology J. Agric. Food Chem. 2020 68 9827 9838 10.1021/acs.jafc.0c04560 32853522
Bonfante P. Splivallo R. Novero M. Bertea C.M. Bossi S. Truffle volatiles inhibit growth and induce an oxidative burst in Arabidopsis thaliana New Phytol. 2007 175 417 424
Bruce A. Stewart D. Verrall S. Wheatley R.E. Effect of volatiles from bacteria and yeast on the growth and pigmentation of sapstain fungi Int. Biodeterior. Biodegrad. 2003 51 101 108 10.1016/S0964-8305(02)00088-4
Yang Q. Chen Y. Ma Z. Involvement of BcVeA and BcVelB in regulating conidiation, pigmentation and virulence in Botrytis cinerea Fungal Genet. Biol. 2013 50 63 71 10.1016/j.fgb.2012.10.003
Tournu H. Carroll J. Latimer B. Dragoi A.M. Dykes S. Cardelli J. Peters T.L. Eberle K.E. Palmer G.E. Identification of small molecules that disrupt vacuolar function in the pathogen Candida albicans PLoS ONE 2017 12 e0171145 10.1371/journal.pone.0171145 28151949
Josselin L. De Clerck C. De Boevre M. Moretti A. Soyeurt H. Fauconnier M.-L. Fungal volatile organic compounds, can be used to develop aflatoxin-specific sensors? Proceedings of the MycoTWIN-MycoKey-2021 International Conference Bari, Italy 9–12 November 2021
Terra W.C. Campos V.P. Martins S.J. Costa L.S.A.S. da Silva J.C.P. Barros A.F. Lopez L.E. Santos T.C.N. Smant G. Oliveira D.F. Volatile organic molecules from Fusarium oxysporum strain 21 with nematicidal activity against Meloidogyne incognita Crop Prot. 2018 106 125 131 10.1016/j.cropro.2017.12.022