Exogenous fungal quorum sensing molecules inhibit planktonic cell growth and modulate filamentation and biofilm formation in the Sporothrix schenckii complex

References

• Alem MAS, Oteef MDY, Flowers TH, Douglas LJ. 2006. Production of tyrosol by Candida albicans biofilms and its role in quorum sensing and biofilm development. Eukaryotic Cell. 5:1770–1779. doi:10.1128/EC.00219-06
   PubMed Web of Science ®Google Scholar
• Bernardo SM, Rane HS, Chavez-Dozal A, Lee SA. 2014. Secretion and filamentation are mediated by the Candida albicans t-SNAREs Sso2p and Sec9p. FEMS Yeast Res. 14:762–775. doi:10.1111/1567-1364.12165
   PubMed Web of Science ®Google Scholar
• Berrocal A, Oviedo C, Nickerson KW, Navarrete J. 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
   PubMed Web of Science ®Google Scholar
• Borghi E, Borgo F, Morace G. 2016. Fungal biofilms: update on resistance. In: Christine Imbert, editor. Fungal biofilms related infection. Switzerland: Springer; p. 37–47.
   Google Scholar
• Brilhante RSN, Oliveira JS, Evangelista AJDJ, Serpa R, Silva AL, Aguiar FRM, Pereira VS, Castelo DDS, Pereira-Neto WA, Cordeiro RDA, et al. 2016b. Candida tropicalis from veterinary and human sources shows similar in vitro hemolytic activity, antifungal biofilm susceptibility and pathogenesis against Caenorhabditis elegans. Vet Microbiol. 192:213–219. doi:10.1016/j.vetmic.2016.07.022
   PubMed Web of Science ®Google Scholar
• Brilhante RSN, Caetano ÉP, Lima RACD, Marques FJDF, Castelo-Branco DDSCM, Melo CVSD, Guedes GMDM, Oliveira JSD, Camargo ZPD, Moreira JLB, et al. 2016a. Terpinen-4-ol, tyrosol, and β-lapachone as potential antifungals against dimorphic fungi. Brazilian J Microbiol. 47:917–924. doi:10.1016/j.bjm.2016.07.015
   PubMed Web of Science ®Google Scholar
• Brilhante RSN, de Aguiar FRM, da Silva MLQ, de Oliveira JS, de Camargo ZP, Rodrigues AM, Pereira VS, Serpa R, Castelo-Branco D. d S C M, Correia EEM, et al. 2018a. Antifungal susceptibility of Sporothrix schenckii complex biofilms. Med Mycol. 56:297–306. doi:10.1093/mmy/myx043
   PubMedGoogle Scholar
• Brilhante RSN, de Lima RAC, Caetano EP, Leite JJG, Castelo-Branco DDSCM, Ribeiro JF, Bandeira TDJPG, Cordeiro RDA, Monteiro AJ, Sidrim JJC, et al. 2013. Effect of farnesol on growth, ergosterol biosynthesis, and cell permeability in Coccidioides posadasii. Antimicrob Agents Chemother. 57:2167–2170. doi:10.1128/AAC.02457-12
   PubMed Web of Science ®Google Scholar
• Brilhante RSN, de Lima RAC, Marques FJDF, Silva NF, Caetano ÉP, Castelo-Branco DDSCM, Bandeira TDJPG, Moreira JLB, Cordeiro RDA, Monteiro AJ, et al. 2015a. Histoplasma capsulatum in planktonic and biofilm forms: in vitro susceptibility to amphotericin B, itraconazole and farnesol. J Med Microbiol. 64:394–399. doi:10.1099/jmm.0.000030
   PubMed Web of Science ®Google Scholar
• Brilhante RSN, Pereira VS, Oliveira JD, Lopes RGP, Rodrigues AM, de Camargo ZP, Pereira-Neto WDA, Castelo-Branco D, Cordeiro RDA, Sidrim JJC, et al. 2018b. Pentamidine inhibits the growth of Sporothrix schenckii complex and exhibits synergism with antifungal agents. Future Microbiol. 13:1129–1140. doi:10.2217/fmb-2018-0070
   PubMed Web of Science ®Google Scholar
• Brilhante RSN, Silva NF, Marques FJDF, Castelo-Branco DDSCM, de Lima RAC, Malaquias ADM, Caetano EP, Barbosa GR, de Camargo ZP, Rodrigues AM, et al. 2015b. In vitro inhibitory activity of terpenic derivatives against clinical and environmental strains of the Sporothrix schenkii complex. Med Mycol. 53:93–98. doi:10.1093/mmy/myu085
   PubMed Web of Science ®Google Scholar
• Chen H, Fink GR. 2006. Feedback control of morphogenesis in fungi by aromatic alcohols. Genes Dev. 20:1150–1161. doi:10.1101/gad.1411806
   PubMed Web of Science ®Google Scholar
• CLSI. 2017a. Reference method for broth dilution antifungal susceptibility testing of filamentous fungi ; approved standard. 3rd ed. CLSI document M38ed3. Wayne, PA: Clinical and Laboratory Standards Institute.
   Google Scholar
• CLSI. 2017b. Reference method for broth dilution antifungal susceptibility testing of yeasts; approved standard. 4th ed. CLSI document M27ed4. Wayne, PA: Clinical and Laboratory Standards.
   Google Scholar
• Cordeiro RA, Teixeira CEC, Brilhante RSN, Castelo-Branco DSCM, Paiva MAN, Giffoni Leite JJ, Lima DT, Monteiro AJ, Sidrim JJC, Rocha MFG. 2013. Minimum inhibitory concentrations of amphotericin B, azoles and caspofungin against Candida species are reduced by farnesol. Med Mycol. 51:53–59. doi:10.3109/13693786.2012.692489
   PubMed Web of Science ®Google Scholar
• Cordeiro RDA, Nogueira GC, Brilhante RSN, Teixeira CEC, Mourão CI, Castelo-Branco DDSCM, Paiva MDAN, Ribeiro JF, Monteiro AJ, Sidrim JJC, et al. 2012. Farnesol inhibits in vitro growth of the Cryptococcus neoformans species complex with no significant changes in virulence-related exoenzymes. Vet Microbiol. 159:375–380. doi:10.1016/j.vetmic.2012.04.008
   PubMed Web of Science ®Google Scholar
• Cordeiro RDA, Pereira LMG, de Sousa JK, Serpa R, Andrade ARC, Portela FVM, Evangelista AJDJ, Sales JA, Aguiar ALR, Mendes PBL, et al. 2019. Farnesol inhibits planktonic cells and antifungal-tolerant biofilms of Trichosporon asahii and Trichosporon inkin. Med Mycol. 57:1038–1045. doi:10.1093/mmy/myy160
   PubMed Web of Science ®Google Scholar
• Cordeiro RDA, Teixeira CEC, Brilhante RSN, Castelo-Branco DSCM, Alencar LP, de Oliveira JS, Monteiro AJ, Bandeira TJPG, Sidrim JJC, Moreira JLB, et al. 2015. Exogenous tyrosol inhibits planktonic cells and biofilms of Candida species and enhances their susceptibility to antifungals. FEMS Yeast Res. 15:fov012. doi:10.1093/femsyr/fov012
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Derengowski LS, De-Souza-Silva C, Braz SV, Mello-De-Sousa TM, Báo SN, Kyaw CM, Silva-Pereira I. 2009. Antimicrobial effect of farnesol, a Candida albicans quorum sensing molecule, on Paracoccidioides brasiliensis growth and morphogenesis. Ann Clin Microbiol Antimicrob. 8:13. doi:10.1186/1476-0711-8-13
   PubMed Web of Science ®Google Scholar
• Findri-Guštek S, Petek MJ, Sarajlija H, Mršić G, Džepina AM, Oreščanin V. 2012. The correlation of the lifestyle and medical conditions with the vaginal infections and production of 2-phenylethanol. Arch Gynecol Obstet. 286:671–682. doi:10.1007/s00404-012-2346-y
   PubMed Web of Science ®Google Scholar
• Gutierrez-Galhardo MC, Zancopé-Oliveira RM, Monzón A, Rodriguez-Tudela JL, Cuenca-Estrella M. 2010. Antifungal susceptibility profile in vitro of Sporothrix schenckii in two growth phases and by two methods: microdilution and E-test. Mycoses. 53:227–231. doi:10.1111/j.1439-0507.2009.01701.x
   PubMed Web of Science ®Google Scholar
• Hall RA, Turner KJ, Chaloupka J, Cottier F, De Sordi L, Sanglard D, Levin LR, Buck J, Mühlschlegel FA. 2011. The quorum-sensing molecules farnesol/homoserine lactone and dodecanol operate via distinct modes of action in Candida albicans. Eukaryotic Cell. 10:1034–1042. doi:10.1128/EC.05060-11
   PubMed Web of Science ®Google Scholar
• Han T-L, Tumanov S, Cannon RD, Villas-Boas SG. 2013. Metabolic response of Candida albicans to phenylethyl alcohol under hyphae-inducing conditions. PLoS One. 8:e71364. doi:10.1371/journal.pone.0071364
   PubMed Web of Science ®Google Scholar
• Harding MW, Marques LLR, Howard RJ, Olson ME. 2009. Can filamentous fungi form biofilms? Trends Microbiol. 17:475–480. doi:10.1016/j.tim.2009.08.007
   PubMed Web of Science ®Google Scholar
• Heydorn A, Nielsen AT, Hentzer M, Sternberg C, Givskov M, Ersbøll BK, Molin S. 2000. Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology. 146:2395–2407. doi:10.1099/00221287-146-10-2395
   PubMed Web of Science ®Google Scholar
• 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. 67:2982–2992. doi:10.1128/AEM.67.7.2982-2992.2001
   PubMed Web of Science ®Google Scholar
• Jakab Á, Tóth Z, Nagy F, Nemes D, Bácskay I, Kardos G, Emri T, Pócsi I, Majoros L, Kovács R. 2019. Physiological and transcriptional responses of Candida parapsilosis to exogenous tyrosol. Appl Environ Microbiol. 85:e01388. doi:10.1128/AEM.01388-19
   PubMed Web of Science ®Google Scholar
• Lindsay AK, Deveau A, Piispanen AE, Hogan DA. 2012. Farnesol and cyclic AMP signaling effects on the hypha-to-yeast transition in Candida albicans. Eukaryotic Cell. 11:1219–1225. doi:10.1128/EC.00144-12
   PubMed Web of Science ®Google Scholar
• Liu P, Cheng Y, Yang M, Liu Y, Chen K, Long C, Deng X. 2014. Mechanisms of action for 2-phenylethanol isolated from Kloeckera apiculata in control of Penicillium molds of citrus fruits. BMC Microbiol. 14:242doi:10.1186/s12866-014-0242-2
   PubMed Web of Science ®Google Scholar
• Lopes-Bezerra LM, Mora-Montes HM, Zhang Y, Nino-Vega G, Rodrigues AM, De Camargo ZP, De Hoog S. 2018. Sporotrichosis between 1898 and 2017: the evolution of knowledge on a changeable disease and on emerging etiological agents. Med Mycol. 56:126–S143. doi:10.1093/mmy/myx103
   PubMed Web of Science ®Google Scholar
• Martínez-Álvarez JA, Pérez-García LA, Mellado-Mojica E, López MG, Martínez-Duncker I, Lópes-Bezerra LM, Mora-Montes HM. 2017. Sporothrix schenckii sensu stricto and Sporothrix brasiliensis are differentially recognized by human peripheral blood mononuclear cells. Front Microbiol. 8:843. doi:10.3389/fmicb.2017.00843
   PubMed Web of Science ®Google Scholar
• Mehmood A, Liu G, Wang X, Meng G, Wang C, Liu Y. 2019. Fungal quorum-sensing molecules and inhibitors with potential antifungal activity: a review. Molecules. 24:1950. doi:10.3390/molecules24101950
   PubMed Web of Science ®Google Scholar
• Mesa-Arango AC, Rueda C, Román E, Quintin J, Terrón MC, Luque D, Netea MG, Pla J, Zaragoza O. 2016. Cell wall changes in amphotericin B-resistant strains from Candida tropicalis and relationship with the immune responses elicited by the host. Antimicrob Agents Chemother. 60:2326–2335. doi:10.1128/AAC.02681-15
   PubMed Web of Science ®Google Scholar
• Nagy F, Vitális E, Jakab A, Borman AM, Forgács L, Tóth Z, Majoros L. Kovács 2020. In vitro and in vivo effect of exogenous farnesol exposure against Candida auris. Front Microbiol. 11:Article 957, 1–12. doi:10.3389/fmicb.2020.00957
   Web of Science ®Google Scholar
• Padder SA, Prasad R, Shah AH. 2018. Quorum sensing: a less known mode of communication among fungi. Microbiol Res. 210:51–58. doi:10.1016/j.micres.2018.03.007
   PubMed Web of Science ®Google Scholar
• Paluch E, Rewak-Soroczyńska J, Jędrusik I, Mazurkiewicz E, Jermakow K. 2020. Prevention of biofilm formation by quorum quenching. Appl Microbiol Biotechnol. 104:1871–1811. doi:10.1007/s00253-020-10349-w
   PubMed Web of Science ®Google Scholar
• Polke M, Leonhardt I, Kurzai O, Jacobsen ID. 2018. Farnesol signalling in Candida albicans - more than just communication. Crit Rev Microbiol. 44:230–243. doi:10.1080/1040841X.2017.1337711
   PubMed Web of Science ®Google Scholar
• Pu L, Jingfan F, Kai C, Chao-An L, Yunjiang C. 2014. Phenylethanol promotes adhesion and biofilm formation of the antagonistic yeast Kloeckera apiculata for the control of blue mold on citrus. FEMS Yeast Res. 14:536–546. doi:10.1111/1567-1364.12139
   PubMed Web of Science ®Google Scholar
• Ramírez-Soto MC, Aguilar-Ancori EG, Tirado-Sánchez A, Bonifaz A. 2018. Ecological determinants of sporotrichosis etiological agents. JoF. 4:95. doi:10.3390/jof4030095
   Google Scholar
• Rodrigues CF, Černáková L. 2020. Farnesol and tyrosol: secondary metabolites with a crucial quorum-sensing role in Candida biofilm development. Genes (Basel). 11:444. doi:10.3390/genes11040444
   Web of Science ®Google Scholar
• Rodrigues AM, de Hoog S, de Camargo ZP. 2013a. Emergence of pathogenicity in the Sporothrix schenckii complex. Med Mycol. 51:405–412. doi:10.3109/13693786.2012.719648
   PubMed Web of Science ®Google Scholar
• Rodrigues AM, Teixeira M de M, de Hoog GS, Schubach TMP, Pereira SA, Fernandes GF, Bezerra LML, Felipe MS, de Camargo ZP. 2013b. Phylogenetic analysis reveals a high prevalence of Sporothrix brasiliensis in feline sporotrichosis outbreaks. PLoS Negl Trop Dis. 7:e2281doi:10.1371/journal.pntd.0002281
   PubMed Web of Science ®Google Scholar
• Sanchotene KO, Brandolt TM, Klafke GB, Poester VR, Xavier MO. 2017. In vitro susceptibility of Sporothrix brasiliensis: comparison of yeast and mycelial phases. Med Mycol. 55:869–876. doi:10.1093/mmy/myw143
   PubMed Web of Science ®Google Scholar
• Sebaa S, Boucherit ‑Otmani Z, Courtois P. 2019. Effects of tyrosol and farnesol on Candida albicans biofilm. Mol Med Rep. 19:3201–3209.
   PubMed Web of Science ®Google Scholar
• Singh MP, Singh P, Li H-B, Song Q-Q, Singh RK. 2020. Microbial biofilms: development, structure, and their social assemblage for beneficial applications. In: Mukesh Kumar Yadav, Bhim Pratap Singh, editors. New and future developments in microbial biotechnology and bioengineering: microbial biofilms. Amsterdam, Netherlands: Elsevier; p. 125–138.
   Google Scholar
• Singkum P, Muangkaew W, Suwanmanee S, Pumeesat P, Wongsuk T, Luplertlop N. 2019. Suppression of the pathogenicity of Candida albicans by the quorum-sensing molecules farnesol and tryptophol. J Gen Appl Microbiol. 65:2012–2018. doi:10.2323/jgam.2018.12.002
   PubMed Web of Science ®Google Scholar
• Wang X, Wang Y, Zhou Y, Wei X. 2014. Farnesol induces apoptosis-like cell death in the pathogenic fungus Aspergillus flavus. Mycologia. 106:881–888. doi:10.3852/13-292
   PubMed Web of Science ®Google Scholar
• Wongsuk T, Luplertlop N. 2020. Effect of quorum sensing molecules on Aspergillus fumigatus. Walailak J Sci Technol. 17:348–358.
   Google Scholar
• Wongsuk T, Pumeesat P, Luplertlop N. 2016. Fungal quorum sensing molecules: role in fungal morphogenesis and pathogenicity. J Basic Microbiol. 56:440–447. doi:10.1002/jobm.201500759
   PubMed Web of Science ®Google Scholar
• Xia J, Qian F, Xu W, Zhang Z, Wei X. 2017. In vitro inhibitory effects of farnesol and interactions between farnesol and antifungals against biofilms of Candida albicans resistant strains. Biofouling. 33:283–293. doi:10.1080/08927014.2017.1295304
   PubMed Web of Science ®Google Scholar
• Zhang J, Feng T, Wang J, Wang Y, Zhang X-H. 2019. The Mechanisms and applications of quorum sensing (QS) and quorum quenching (QQ). J Ocean Univ China. 18:1427–1442. doi:10.1007/s11802-019-4073-5
   Web of Science ®Google Scholar