Review

Quorum sensing mechanisms in fungi

  • Received: 28 September 2015 Accepted: 18 November 2015 Published: 20 November 2015
  • In the environment, cells from microorganisms can communicate to each other through the secretion of signal molecules, so-called autoinducers, which accumulate in the medium as the population density grows. When the concentration of these molecules reaches a threshold, different genes are induced or repressed, and processes such as sporulation, pathogenesis or symbiosis are initiated. These mechanisms, known as quorum sensing (QS), were first discovered in bacteria, and more recently have been identified in fungi. The model eukaryote organism for this kind of studies is the dimorphic pathogenic yeast Candida albicans. However, QS mechanisms have been described in a variety of fungi with clinical or biotechnological interest. Hence, the study of these mechanisms may be useful to prevent fungal infections, and interesting for its exploitation in industrial biotechnology.

    Citation: Jorge Barriuso. Quorum sensing mechanisms in fungi[J]. AIMS Microbiology, 2015, 1(1): 37-47. doi: 10.3934/microbiol.2015.1.37

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  • In the environment, cells from microorganisms can communicate to each other through the secretion of signal molecules, so-called autoinducers, which accumulate in the medium as the population density grows. When the concentration of these molecules reaches a threshold, different genes are induced or repressed, and processes such as sporulation, pathogenesis or symbiosis are initiated. These mechanisms, known as quorum sensing (QS), were first discovered in bacteria, and more recently have been identified in fungi. The model eukaryote organism for this kind of studies is the dimorphic pathogenic yeast Candida albicans. However, QS mechanisms have been described in a variety of fungi with clinical or biotechnological interest. Hence, the study of these mechanisms may be useful to prevent fungal infections, and interesting for its exploitation in industrial biotechnology.


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    [1] Nealson KH, Platt T, Hastings JW (1970) Cellular control of the synthesis and activity of the bacterial luminescent system. J Bacteriol 104: 313-322.
    [2] Williams HE, Steele JC, Clements MO, et al. (2012) gamma-Heptalactone is an endogenously produced quorum-sensing molecule regulating growth and secondary metabolite production by Aspergillus nidulans. App Microbiol Biotech 96:773-781. doi: 10.1007/s00253-012-4065-5
    [3] Lu Y, Su C, Unoje O, et al. (2014) Quorum sensing controls hyphal initiation in Candida albicans through Ubr1-mediated protein degradation. P Natl Acad Sci U S A 111:1975-1980. doi: 10.1073/pnas.1318690111
    [4] Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55: 165-199. doi: 10.1146/annurev.micro.55.1.165
    [5] Wuster A, Babu MM (2010) Transcriptional control of the quorum sensing response in yeast. Mol Biosyst 6: 134-141.
    [6] Fuqua WC, Winans SC, Greenberg EP (1994) Quorum sensing in bacteria - the Luxr-Luxi family of cell density-responsive transcriptional regulators. J Bacteriol 176: 269-275.
    [7] Bandara HMHN, Lam OLT, Jin LJ, et al. (2012) Microbial chemical signaling: a current perspective. Crit Rev Microbiol 38: 217-249. doi: 10.3109/1040841X.2011.652065
    [8] Puskas A, Greenberg EP, Kaplan S, et al. (1997) A quorum-sensing system in the free-living photosynthetic bacterium Rhodobacter sphaeroides. J Bacteriol 179: 7530-7537.
    [9] Pesci EC, Milbank JB, Pearson JP, et al. (1999) Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 96: 11229-31124. doi: 10.1073/pnas.96.20.11229
    [10] Hornby JM, Jensen EC, Lisec AD, et al. (2001) Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. App Environ Microbiol 67: 2982-2992. doi: 10.1128/AEM.67.7.2982-2992.2001
    [11] Hogan DA (2006) Talking to themselves: Autoregulation and quorum sensing in fungi. Eukaryot Cell 5: 613-619. doi: 10.1128/EC.5.4.613-619.2006
    [12] Barriuso J, Solano BR, Fray RG, et al. (2008) Transgenic tomato plants alter quorum sensing in plant growth-promoting rhizobacteria. Plant Biotech J 6: 442-452. doi: 10.1111/j.1467-7652.2008.00331.x
    [13] Camara M, Williams P, Hardman A (2002) Controlling infection by tuning in and turning down the volume of bacterial small-talk. Lancet Infect Dis 2: 667-676. doi: 10.1016/S1473-3099(02)00447-4
    [14] Geiger J, Wessels D, Lockhart SR, et al. (2004) Release of a potent polymorphonuclear leukocyte chemoattractant is regulated by white-opaque switching in Candida albicans. Infect Immun 72: 667-677. doi: 10.1128/IAI.72.2.667-677.2004
    [15] Pérez-Montaño F, Jiménez-Guerrero I, Contreras Sánchez-Matamoros R, et al. (2013) Rice and bean AHL-mimic quorum-sensing signals specifically interfere with the capacity to form biofilms by plant-associated bacteria. Res Microbiol 164: 749-760. doi: 10.1016/j.resmic.2013.04.001
    [16] Zhu J, Kaufmann GF (2013) Quo vadis quorum quenching? Curr Opin Pharmacol 13: 688-698. doi: 10.1016/j.coph.2013.07.003
    [17] Barrios AFG, Covo V, Medina LM, et al. (2009) Quorum quenching analysis in Pseudomonas aeruginosa and Escherichia coli: network topology and inhibition mechanism effect on the optimized inhibitor dose. Bioprocess BiosystEng 32: 545-556. doi: 10.1007/s00449-008-0276-7
    [18] Medina-Martinez MS, Uyttendaele M, Rajkovic A, et al. (2007) Degradationof N-acyl-L-homoserine lactones by Bacillus cereus in culture media and pork extract. Appl Environ Microbiol 73: 2329-2332. doi: 10.1128/AEM.01993-06
    [19] Nucci M, Queiroz-Telles F, Tobon AM, et al. (2010)Epidemiology of opportunistic fungal infections in Latin America. Clin Infec Dis 51: 561-570.
    [20] Lo HJ, Köhler JR, DiDomenico B, et al (1997) Nonfilamentous C. albicans mutants are avirulent. Cell 90: 939-949.
    [21] Chen H, Fujita M, Feng Q, et al. (2004) Tyrosol is a quorum sensing molecule in Candida albicans. Proc Natl Acad Sci U S A 101: 5048-5052. doi: 10.1073/pnas.0401416101
    [22] Cordeiro A, Teixeira CE, Brilhante RS, et al. (2015) Exogenous tyrosol inhibits planktonic cells and biofilms of Candida species and enhances their susceptibility to antifungals. FEMS Yeast Res 15: 12.
    [23] Hogan DA, Vik A, Kolter R (2004) A Pseudomonas aeruginosa quorum- sensing molecule influences Candida albicans morphology. Mol Microbiol 54: 1212-1223. doi: 10.1111/j.1365-2958.2004.04349.x
    [24] Davis-Hanna A, Piispanen AE, Stateva LI, et al. (2008) Farnesol and dodecanol effects on the Candida albicans Ras1-cAMP signaling pathway and the regulation of morphogenesis. Mol Microbiol 67: 47-62.
    [25] Hall RA, Turner KJ, Chaloupka J, et al. (2011) The quorum-sensing molecules farnesol/homoserine lactone and dodecanol operate via distinct modes of action in Candida albicans. Eukaryot Cell 10: 1034-1042. doi: 10.1128/EC.05060-11
    [26] Klengel T, Liang WJ, Chaloupka J, et al. (2005) Fungal adenylyl cyclase integrates CO2 sensing with cAMP signaling and virulence. Curr Biol 15: 2021-2026. doi: 10.1016/j.cub.2005.10.040
    [27] Kebaara BW, Langford ML, Navarathna DH, et al. (2008) Candida albicans Tup1 is involved in farnesol-mediated inhibition of filamentous-growth induction. Eukaryot Cell 7: 980-987. doi: 10.1128/EC.00357-07
    [28] Langford ML, Hargarten JC, Patefield KD, et al. (2013) Candida albicans Czf1 and Efg1 Coordinate the Response to Farnesol during Quorum Sensing, White-Opaque Thermal Dimorphism, and Cell Death. Eukaryot Cell 12: 1281-1292. doi: 10.1128/EC.00311-12
    [29] Madhani HD (2011) Quorum sensing in fungi: Q&A. PLoS Pathog 7: e1002301. doi: 10.1371/journal.ppat.1002301
    [30] Cao YY, Cao YB, Xu Z, et al. (2005) cDNA microarray analysis of differential gene expression in Candida albicans biofilm exposed to farnesol. Antimicrob Agents Chemother 49: 584-589. doi: 10.1128/AAC.49.2.584-589.2005
    [31] Ramage G, Saville SP, Wickes BL, et al. (2002) Inhibition of Candida albicans biofilm formation by farnesol, a quorum-sensing molecule. Appl Environ Microbiol 68: 5459-5463.
    [32] De Sordi L, Mühlschlegel FA (2009) Quorum sensing and fungal-bacterial interactions in Candida albicans: a communicative network regulating microbial coexistence and virulence. FEMS Yeast Res 9: 990-999.
    [33] Jabra-Rizk MA, Meiller TF, James CE, et al. (2006) Effect of farnesol on Staphylococcus aureus biofilm formation and antimicrobial susceptibility. Antimicrob Agents Chemother 50: 1463-1469. doi: 10.1128/AAC.50.4.1463-1469.2006
    [34] Semighini CP, Hornby JM, Dumitru R, et al. (2006) Farnesol-induced apoptosis in Aspergillus nidulans reveals a possible mechanism for antagonistic interactions between fungi. Mol Microbiol 59: 753-764. doi: 10.1111/j.1365-2958.2005.04976.x
    [35] Sztajer H, Szafranski SP, Tomasch J, et al. (2014) Cross-feeding and interkingdom communication in dual-species biofilms of Streptococcusmutans and Candida albicans. ISME J 8: 2256-2271.
    [36] Cruz MR, Graham CE, Gagliano BC, et al. (2013) Enterococcus faecalis inhibits hyphal morphogenesis and virulence of Candida albicans. Infect Immun 81: 189-200. doi: 10.1128/IAI.00914-12
    [37] Hogan DA (2006) Quorum sensing: Alcohols in a social situation. Curr Biol 16: R457-R458. doi: 10.1016/j.cub.2006.05.035
    [38] Romano A (1966) Dimorphism, In:G.C. Ainsworth and A. S. Sussman, The Fungi, 2 Eds., New York: Academic Press, 181-209.
    [39] de Salas F, Martínez MJ, Barriuso J (2015) Quorum-Sensing Mechanisms Mediated by Farnesol in Ophiostoma piceae: Effect on Secretion of Sterol Esterase. Appl Environ Microbiol 81: 4351-4357. doi: 10.1128/AEM.00079-15
    [40] Nickerson KW, Atkin AL, Hornby JM (2006) Quorum sensing in dimorphic fungi: Farnesol and beyond. App Environ Microbiol 72: 3805-3813. doi: 10.1128/AEM.02765-05
    [41] Khoshraftar S, Hung S, Khan S, et al. (2013) Sequencing and annotation of the Ophiostoma ulmi genome. BMC Genomics 14: 162. doi: 10.1186/1471-2164-14-162
    [42] Hornby JM, Jacobitz-Kizzier SM, Mcneel DJ, et al. (2004) Inoculum size effect in dimorphic fungi: Extracellular control of yeast-mycelium dimorphism in Ceratocystis ulmi. App Environ Microbiol 70: 1356-1359. doi: 10.1128/AEM.70.3.1356-1359.2004
    [43] Berrocal A, Navarrete J, Oviedo C, et al. (2012) Quorum sensing activity in Ophiostoma ulmi: effects of fusel oils and branched chain amino acids on yeast-mycelial dimorphism. J App Microbiol 113: 126-134. doi: 10.1111/j.1365-2672.2012.05317.x
    [44] Krokene P, Solheim H (1998) Pathogenicity of four blue-stain fungi associated with aggressive and nonaggressive bark beetles. Phytopathology 88: 39-44. doi: 10.1094/PHYTO.1998.88.1.39
    [45] Calero-Rueda O, Plou FJ, Ballesteros A, et al. (2002) Production, isolation and characterization of a sterol esterase from Ophiostoma piceae. BBA-Proteins Proteom 1599: 28-35. doi: 10.1016/S1570-9639(02)00378-3
    [46] Berrocal A, Oviedo C, Nickerson KW, et al. (2014) Quorum sensing activity and control of yeast-mycelium dimorphism in Ophiostoma floccosum. Biotechnol Lett 36: 1503-1513. doi: 10.1007/s10529-014-1514-5
    [47] Albuquerque P, Nicola AM, Nieves E, et al. (2014) Quorum Sensing-Mediated, Cell Density-Dependent Regulation of Growth and Virulence in Cryptococcus neoformans. mBio 5: e00986-13.
    [48] Lee H, Chang YC, Nardone G, et al. (2007) TUP1 disruption in Cryptococcus neoformans uncovers a peptide-mediated density-dependent growth phenomenon that mimics quorum sensing. Mol Microbiol 64: 591-601. doi: 10.1111/j.1365-2958.2007.05666.x
    [49] Wynendaele E, Bronselaer A, Nielandt J, et al. (2013) Quorumpeps database: chemical space, microbial origin and functionality of quorum sensing peptides. Nucleic Acids Res 41: D655-659. doi: 10.1093/nar/gks1137
    [50] Raina S, Odell M, Keshavarz T (2010) Quorum sensing as a method for improving sclerotiorin production in Penicillium sclerotiorum. J Biotechnol 148: 91-98. doi: 10.1016/j.jbiotec.2010.04.009
    [51] Sorrentino F, Roy I, Keshavarz T (2010) Impact of linoleic acid supplementation on lovastatin production in Aspergillus terreus cultures. App Microbiol Biotech 88: 65-73. doi: 10.1007/s00253-010-2722-0
    [52] Guo H, Ma A, Zhao G, et al. (2011) Effect of farnesol on Penicillium decumbens's morphology and cellulase production. Bioresources 6: 3252-3259.
    [53] Raina S, De Vizio D, Palonen EK, et al. (2012) Is quorum sensing involved in lovastatin production in the filamentous fungus Aspergillus terreus? Process Biochem 47: 843-852. doi: 10.1016/j.procbio.2012.02.021
    [54] Williams HE, Steele JC, Clements MO, et al. (2012) gamma-Heptalactone is an endogenously produced quorum-sensing molecule regulating growth and secondary metabolite production by Aspergillus nidulans. App Microbiol Biotech 96: 773-781. doi: 10.1007/s00253-012-4065-5
    [55] Barnard AM, Bowden SD, Burr T, et al. (2007) Quorum sensing, virulence and secondary metabolite production in plant soft-rotting bacteria. Philos Trans R Soc Lond B Biol Sci 362: 1165-1183. doi: 10.1098/rstb.2007.2042
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