The Bull Effect of Endophytic Fungi: An Approach with Quorum Sensing

  • Subhoshmita Mondal
  • Sarangam Majumdar
Part of the Fungal Biology book series (FUNGBIO)


Quorum sensing is a cell-to-cell communication process. This microbial communication process depends on the cell number density. Candida albicans is one of the most commonly studied fungi for quorum sensing. It has been observed that farnesol (quorum sensing molecules) control this communication system. Moreover, aromatic alcohol tyrosol was identified as another fungal quorum sensing molecule in C. albicans. This chapter details the fungal quorum sensing system, quorum sensing molecules controlling growth, biofilm formation, and morphogenesis. Additionally, the chapter also focuses on other fungal quorum sensing mechanisms (including endophytic fungi) and sheds new light on the fungal kingdom.


  1. Albuquerque P, Casadevall A (2012) Quorum sensing in fungi—a review. Med Mycol 50(4):337–345CrossRefGoogle Scholar
  2. Alem MA, Oteef MD, Flowers TH, Douglas LJ (2006) Production of tyrosol by Candida albicans biofilms and its role in quorum sensing and biofilm development. Eukaryot Cell 5:1770–1779CrossRefGoogle Scholar
  3. Anand R, Rai N, Thattai M (2013) Interactions among quorum sensing inhibitors. PLoS One 8(4):e62254CrossRefGoogle Scholar
  4. Anguige K, King JR, Ward JP, Williams P (2004) Mathematical modelling of therapies targeted at bacterial quorum sensing. Math Biosci 192(1):39–83. CrossRefPubMedGoogle Scholar
  5. Anguige K, King JR, Ward JP (2005) Modelling antibiotic- and anti-quorum sensing treatment of a spatially-structured Pseudomonas aeruginosa population. J Math Biol 51(5):557–594. CrossRefPubMedGoogle Scholar
  6. Avbelj M, Zupan J, Kranjc L, Raspor P (2015) Quorum-sensing kinetics in Saccharomyces cerevisiae: a symphony of ARO genes and aromatic alcohols. J Agric Food Chem 63:8544–8550CrossRefGoogle Scholar
  7. Balagaddé FK, Song H, Ozaki J, Collins CH, Barnet M, Arnold FH, Quake SR, You L (2008) A synthetic Escherichia coli predator–prey ecosystem. Mol Syst Biol 4(1):187PubMedPubMedCentralGoogle Scholar
  8. Basu S, Gerchman Y, Collins CH, Arnold FH, Weiss R (2005) A synthetic multicellular system for programmed pattern formation. Nature 434(7037):1130–1134CrossRefGoogle Scholar
  9. Baym M, Lieberman TD, Kelsic ED, Chait R, Gross R, Yelin I, Kishony R (2016) Spatiotemporal microbial evolution on antibiotic landscapes. Science 353(6304):1147–1151CrossRefGoogle Scholar
  10. Beckmann BE, Knoester DB, Connelly BD, Waters CM, McKinley PK (2012) Evolution of resistance to quorum quenching in digital organisms. Artif Life 18(3):291–310CrossRefGoogle Scholar
  11. Brenner K, Karig DK, Weiss R, Arnold FH (2007) Engineered bidirectional communication mediates a consensus in a microbial biofilm consortium. Proc Natl Acad Sci U S A 104(44):17300–17304CrossRefGoogle Scholar
  12. Brock DA, Gomer RH (1999) A cell-counting factor regulating structure size in dictyostelium. Genes Dev 13:1960–1969CrossRefGoogle Scholar
  13. 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 49:584–589CrossRefGoogle Scholar
  14. Chen H, Fink GR (2006) Feedback control of morphogenesis in fungi by aromatic alcohols. Genes Dev 20(9):1150–1161CrossRefGoogle Scholar
  15. Chen H, Fujita M, Feng Q, Clardy J, Fink GR (2004) Tyrosol is a quorum-sensing molecule in Candida albicans. Proc Natl Acad Sci U S A 101(14):5048–5052CrossRefGoogle Scholar
  16. Chen Y, Kim JK, Hirning AJ, Josić K, Bennett MR (2015) Emergent genetic oscillations in a synthetic microbial consortium. Science 349(6251):986–989CrossRefGoogle Scholar
  17. Danino T, Mondragón-Palomino O, Tsimring L, Hasty J (2010) A synchronized quorum of genetic clocks. Nature 463(7279):326–330CrossRefGoogle Scholar
  18. Datla US, Mather WH, Chen S, Shoultz IW, Täuber UC, Jones CN, Butzin NC (2017) The spatiotemporal system dynamics of acquired resistance in an engineered microecology. Sci Rep 7(1):16071CrossRefGoogle Scholar
  19. Davis-Hanna A, Piispanen AE, Stateva LI, Hogan DA (2008) Farnesol and dodecanol effects on the Candida albicans Ras1-cAMP signalling pathway and the regulation of morphogenesis. Mol Microbiol 67:47–62CrossRefGoogle Scholar
  20. Deveau A, Piispanen AE, Jackson AA, Hogan DA (2010) Farnesol induces hydrogen peroxide resistance in Candida albicans yeast by inhibiting the Ras-cyclic AMP signaling pathway. Eukaryot Cell 9:569–577CrossRefGoogle Scholar
  21. Elowitz MB, Leibler S (2000) A synthetic oscillatory network of transcriptional regulators. Nature 403(6767):335–338CrossRefGoogle Scholar
  22. Fagerlind MG, Nilsson P, Harlén M, Karlsson S, Rice SA, Kjelleberg S (2005) Modeling the effect of acylated homoserine lactone antagonists in Pseudomonas aeruginosa. Biosystems 80(2):201–213CrossRefGoogle Scholar
  23. Figueroa M, Jarmusch AK, Raja HA, El-Elimat T, Kavanaugh JS, Horswill AR, Cooks RG, Cech NB, Oberlies NH (2014) Polyhydroxyanthraquinones as quorum sensing inhibitors from the guttates of Penicillium restrictum and their analysis by desorption electrospray ionization mass spectrometry. J Nat Prod 77(6):1351–1358CrossRefGoogle Scholar
  24. Gardner TS, Cantor CR, Collins JJ (2000) Construction of a genetic toggle switch in Escherichia coli. Nature 403(6767):339–342CrossRefGoogle Scholar
  25. Golé L, Rivière C, Hayakawa Y, Rieu JP (2011) A quorum-sensing factor in vegetative Dictyostelium discoideum cells revealed by quantitative migration analysis. PLoS One 6(11):e26901CrossRefGoogle Scholar
  26. Hall RA, Cottier F, Muhlschlegel FA (2009) Molecular networks in the fungal pathogen Candida albicans. Adv Appl Microbiol 67:191–212CrossRefGoogle Scholar
  27. Hornby JM, Jensen EC, 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 Microbiol 67(7):2982–2992CrossRefGoogle Scholar
  28. 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 Microbiol 70(3):1356–1359CrossRefGoogle Scholar
  29. Kebaara BW, Langford ML, Navarathna DH et al (2008) Candida albicans Tup1 is involved in farnesol-mediated inhibition of filamentous-growth induction. Eukaryot Cell 7:980–987CrossRefGoogle Scholar
  30. Kügler S, Sebghati TS, Eissenberg LG, Goldman WE (2000) Phenotypic variation and intracellular parasitism by Histoplasma capsulatum. Proc Natl Acad Sci U S A 97(16):8794–8798CrossRefGoogle Scholar
  31. Kusari P, Kusari S, Spiteller M, Kayser O (2015) Implications of endophyte-plant crosstalk in light of quorum responses for plant biotechnology. Appl Microbiol Biotechnol 99(13):5383–5390CrossRefGoogle Scholar
  32. Langford ML, Atkin AL, Nickerson KW (2009) Cellular interactions of farnesol, a quorum-sensing molecule produced by Candida albicans. Future Microbiol 4:1353–1362CrossRefGoogle Scholar
  33. Lee H, Chang YC, Nardone G, Kwon-Chung KJ (2007) TUP1 disruption in Cryptococcus neoformans uncovers a peptide-mediated density-dependent growth phenomenon that mimics quorum sensing. Mol Microbiol 64:591–601CrossRefGoogle Scholar
  34. Lohse MB, Gulati M, Johnson AD, Nobile CJ (2018) Development and regulation of single-and multi-species Candida albicans biofilms. Nat Rev Microbiol 16(1):19–31CrossRefGoogle Scholar
  35. Majumdar S, Mondal S (2016) Conversation game: talking bacteria. J Cell Commun Signal 10(4):331–335CrossRefGoogle Scholar
  36. Majumdar S, Pal S (2016) Quorum sensing: a quantum perspective. J Cell Commun Signal 10(3):173–175CrossRefGoogle Scholar
  37. Majumdar S, Pal S (2017a) Cross-species communication in bacterial world. J Cell Commun Signal 11(2):187–190CrossRefGoogle Scholar
  38. Majumdar S, Pal S (2017b) Bacterial intelligence: imitation games, time-sharing, and long-range quantum coherence. J Cell Commun Signal 11(3):281–284CrossRefGoogle Scholar
  39. Majumdar S, Pal S (2018) Information transmission in microbial and fungal communication: from classical to quantum. J Cell Commun Signal 12(2):491–502. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Majumdar S, Roy S (2017) Spatiotemporal patterns and chaos in non-equilibrium bacterial communication. In: 17th BIOMAT international symposium on mathematical and computational biology, Moscow, RussiaGoogle Scholar
  41. Majumdar S, Roy S (2018) Relevance of quantum mechanics in bacterial communication. Neuroquantology 16(3):1–6CrossRefGoogle Scholar
  42. Majumdar S, Datta S, Roy S (2012) Mathematical modelling of quorum sensing and bioluminescence in bacteria. Int J Adv Appl Sci 1(3):139–146Google Scholar
  43. Majumdar S, Roy S, Llinas R (2017) Bacterial conversations and pattern formation. bioRxiv.
  44. Martin-Rodriguez AJ, Reyes F, Martin J, Perez-Yepez J, Leon-Barrios M, Couttolenc A, Espinoza C, Trigos A, Martin VS, Norte M, Fernandez JJ (2014) Inhibition of bacterial quorum sensing by extracts from aquatic fungi: first report from marine endophytes. Mar Drugs 12:5503–5526. CrossRefPubMedPubMedCentralGoogle Scholar
  45. Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55:165–199CrossRefGoogle Scholar
  46. Rajesh PS, Rai VR (2013) Hydrolytic enzymes and quorum sensing inhibitors from endophytic fungi of Ventilago madraspatana Gaertn. Biocatal Agric Biotechnol 2(2):120–124CrossRefGoogle Scholar
  47. Ramage G, Saville SP, Wickes BL, Lopez-Ribot JL (2002) Inhibition of Candida albicans biofilm formation by farnesol, a quorum-sensing molecule. Appl Environ Microbiol 68:5459–5463CrossRefGoogle Scholar
  48. Roca MG, Arlt J, Jeffree CE, Read ND (2005) Cell biology of conidial anastomosis tubes in Neurospora crassa. Eukaryot Cell 4(5):911–919CrossRefGoogle Scholar
  49. Sato T, Watanabe T, Mikami T, Matsumoto T (2004) Farnesol, a morphogenetic autoregulatory substance in the dimorphic fungus Candida albicans, inhibits hyphae growth through suppression of a mitogen-activated protein kinase cascade. Biol Pharm Bull 27:751–752CrossRefGoogle Scholar
  50. Scott SR, Hasty J (2016) Quorum sensing communication modules for microbial consortia. ACS Synth Biol 5(9):969–977CrossRefGoogle Scholar
  51. Seeley TD, Visscher PK (2004) Group decision making in nest-site selection by honey bees. Apidologie (Celle) 35:101–116CrossRefGoogle Scholar
  52. Severin FF, Meer MV, Smirnova EA, Knorre DA, Skulachev VP (2008) Natural causes of programmed death of yeast Saccharomyces cerevisiae. Biochim Biophys Acta 1783(7):1350–1353CrossRefGoogle Scholar
  53. Shapiro JA (1998) Thinking about bacterial populations as multicellular organisms. Annu Rev Microbiol 52:81–104CrossRefGoogle Scholar
  54. Sharma M, Prasad R (2011) The quorum-sensing molecule farnesol is a modulator of drug efflux mediated by ABC multidrug transporters and synergizes with drugs in Candida albicans. Antimicrob Agents Chemother 55:4834–4843CrossRefGoogle Scholar
  55. Shou W, Ram S, Vilar JM (2007) Synthetic cooperation in engineered yeast populations. Proc Natl Acad Sci U S A 104(6):1877–1882CrossRefGoogle Scholar
  56. Song H, Payne S, Gray M, You L (2009) Spatiotemporal modulation of biodiversity in a synthetic chemical-mediated ecosystem. Nat Chem Biol 5(12):929–935CrossRefGoogle Scholar
  57. Sprague GF Jr, Winans SC (2006) Eukaryotes learn how to count: quorum sensing by yeast. Genes Dev 20:1045–1049CrossRefGoogle Scholar
  58. Stricker J, Cookson S, Bennett MR, Mather WH, Tsimring LS, Hasty J (2008) A fast, robust and tunable synthetic gene oscillator. Nature 456(7221):516–519CrossRefGoogle Scholar
  59. Viretta AU, Fussenegger M (2004) Modeling the quorum sensing regulatory network of human-pathogenic Pseudomonas aeruginosa. Biotechnol Prog 20:670–678. CrossRefGoogle Scholar
  60. Ward J (2008) Mathematical modeling of quorum-sensing control in biofilms. In: Balaban N (ed) Control of biofilm infections by signal manipulation, vol. 2 of Springer Series on Biofilms. Springer, Berlin, pp 79–108Google Scholar
  61. Westwater C, Balish E, Schofield DA (2005) Candida albicans-conditioned medium protects yeast cells from oxidative stress: a possible link between quorum sensing and oxidative stress resistance. Eukaryot Cell 4:1654–1661CrossRefGoogle Scholar
  62. Williams P, Winzer K, Chan WC, Camara M (2007) Look who’s talking: communication and quorum sensing in the bacterial world. Philos Trans R Soc Lond Ser B Biol Sci 362(1483):1119–1134CrossRefGoogle Scholar
  63. You L, Cox RS III, Weiss R, Arnold FH (2004) Programmed population control by cell–cell communication and regulated killing. Nature 428(6985):868–871CrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Subhoshmita Mondal
    • 1
  • Sarangam Majumdar
    • 2
  1. 1.Department of Chemical EngineeringJadavpur UniversityKolkataIndia
  2. 2.Dipartimento di Ingegneria Scienze Informatiche e MatematicaUniversità degli Studi di L’ AquilaL’ AquilaItaly

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