Abstract
This study aimed to determine the antifungal and antibiofilm activities of Agelas dispar on biofilm-producing Candida species. The methanolic extract of A. dispar was obtained and the fraction Ag2 showed inhibitory activity for all 13 Candida strains tested, in concentrations ranging from 2.5 to 0.15625 mg/mL. Antifungal activity of fungicidal nature was seen between 5.0 and 0.3125 mg/mL of extract against the strains. All the strains were classified as biofilm producers. The methanolic extract Ag2 was tested at concentrations of 2.5 and 1.25 mg/mL for antibiofilm activity against the biofilm formation and maturation in all the strains of the genus Candida. Treated and untreated biofilm samples were selected for visualization using scanning electron microscopy (SEM). SEM allowed the visualization of the quantitative decrease in the microbial community, alterations of structural morphology, and destruction of both the formation and maturation of biofilms, at the cellular level. The mechanism of action of this fraction is suggested to be at the plasma membrane and/or cell wall alteration level. Therefore, the use of the methanolic extract of A. dispar may be a promising antifungal and antibiofilm therapeutic strategy against different species of the genus Candida.
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Alves CFS, Bonez PC, Souza ME, Cruz RC, Boligon AA, Piana M, et al. Antimicrobial, antirypanosomal and antibiofilm activity of Equisetum hyemale. Microb Pathog. 2016;101:119–25.
Zeng B, Li J, Wang Y, Chen P, Wang X. In vitro and in vivo effects of suloctidil on growth and biofilm formation of the opportunistic fungus Candida albicans. Oncotarget. 2017;8(41):69972–82.
Kiraz N, Oz Y. Species distribution and in vitro antifungal susceptibility of clinical Candida isolates from a university hospital in Turkey over a 5-year period. Med Mycol. 2011;49:126–31.
Khan MSA, Malik A, Ahmad I. Anti-candial activity of essencial oils alone and in combination with amphotericin B or fluconazole against multi-drug resistant isolates of Candida albicans. Med Mycol. 2012;50:33–42.
Silva S, Rodrigues CF, Araújo D, Rodrigues ME, Henriques M. Candida species biofilms antifungal resistance. J Fungi. 2017;3(1):8.
Hu F, Tu X-F, Thakur K, Hu F, Li X-L, Zhang Y-S, et al. Comparison of antifungal activity of essential oils from different plants against three fungi. Food Chem Toxicol. 2019;134:110821.
Vital Júnior AC, Diniz- Neto H, Fernandes GL, Ferreira MDL, Pereira JA, Silva DF, Oliveira HMBF, Oliveira-Filho AA, Lima EO, Silva DF. In vitro investigation of ß-citronellol biological effect in association with amphotericin B against Candida tropicalis. Lat Am J Pharm. 2019;38(9):1784–7.
Silva D, Diniz-Neto H, Cordeiro L, Silva-Neta M, Silva S, Andrade-Júnior F, et al. (R)-(+)-β-Citronellol and (S)-(−)-β-citronellol in combination with amphotericin B against Candida spp. Int J Mol Sci. 2020;21(5):1785.
Malinovská Z. Antibiofilm activity of selected plant essential oils from the Lamiaceae family against Candida albicans clinical isolates. Ann Agric Environ Med. 2021;28(2):260–6.
Abd Rashed A, Rathi D-NG, Ahmad Nasir NAH, Abd Rahman AZ. Antifungal properties of essential oils and their compounds for application in skin fungal infections: conventional and nonconventional approaches. Molecules. 2021;26(4):1093.
Blunt JW, Copp BR, Keyzers RA, Munro MHG, Prinsep MR. Marine natural products. Nat Prod Rep. 2014;31:160–258.
Harvey AL, Edrada-Ebel R, Quinn RJ. The re-emergence of natural products for drug discovery in the genomics era. Nat Rev Drug Discov. 2015;14:111–29.
Bickmeyer U, Drechsler C, Köck M, Assmann M. Brominated pyrrole alkaloids from marine Agelas sponges reduce depolarization-induced cellular calcium elevation. Toxicon. 2004;44:45–51.
Zhang H, Dong M, Chen J, Wang H, Tenney K, Crews P. Bioactive secondary metabolites from the marine sponge genus Agelas. Mar Drugs. 2017;15:11–29.
Lee Y-K, Lee J-H, Lee H-K. Microbial symbiosis in marine sponges. J Microbiol. 2001;39(4):254–64.
Breckle G, Polborn K, Lindel T. Synthesis of the pyrrole-imidazole alkaloid sventrin from the marine sponge Agelas sventres. Zeitschrift fur Naturforsch – Sect B J Chem Sci. 2003;58(5):451–6.
Scala F, Fattorusso E, Menna M, Taglialatela-Scafati O, Tierney M, Kaiser M, Tasdemir D. Bromopyrrole alkaloids as lead compounds against protozoan parasites. Mar Drugs. 2010;8:2162–74.
Choi C, Son A, Lee HS, Lee YJ, Park HC. Radiosensitization by marine sponge Agelas sp. extracts in hepatocellular carcinoma cells with aautophagy induction. Sci Rep. 2018;8:1–10.
Chanas B, Pawlik JR, Lindel T, Fenical W. Chemical defense of the Caribbean sponge Agelas clathrodes (Schmidt). J Exp Mar Bio Ecol. 1997;208(1–2):185–96.
Sauleau P, Moriou C, Al MA. Metabolomics approach to chemical diversity of the Mediterranean marine sponge Agelas oroides. Nat Prod Res. 2017;31(14):1625–32.
Abdjul DB, Yamazaki H, Kanno S, Takahashi O, Kirikoshi R, Ukai K, et al. Structures and biological evaluations of agelasines isolated from the Okinawan marine sponge Agelas nakamurai. J Nat Prod. 2015;78(6):1428–33.
Cychon C, Lichte E, Köck M. The marine sponge Agelas citrina as a source of the new pyrrole–imidazole alkaloids citrinamines A-D and N-methylagelongine. Beilstein J Org Chem. 2015;11(1):2029–37.
Singh KS, Majik MS. Pyrrole-derived alkaloids of marine sponges and their biological properties. In: Studies in natural products chemistry. Elsevier; 2019. p. 377–409.
Nakamura H, Wu H, Kobayashi JI, Ohizumi Y, Hirata Y, Higashijima T, Miyazawa T. Agelasidine-A, a novel sesquiterpene possessing antispasmodic activity from the okinawa sea sponge Agelas sp. Tetrahedron Lett. 1983;24:4105–8.
Roy C, Edwina S. Evaluation of new antimicrobials in vitro and in experimental animal infection. In: Victor L, editor. Antibiotics in laboratory medicine. Baltimore: Williams and Wilkins; 1991. p. 739–86.
Hadacek F, Greger H. Testing of antifungal natural products: methodologies, comparability of results and assay choice. Phytochem Anal. 2000;11:137–47.
CLSI. Clinical and Laboratory Standards Institute. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts. Approved Standard - Fourth Edition M27-A4. 2017; Wayne, Pennsylvania, USA
Hood JR, Wilkinson JM, Cavanagh HMA. Evaluation of common antibacterial screening methods utilized in essential oil research. J Essent Oil Res. 2003;15:428–33.
Isenberg H. Clinical microbiology procedures handbook. Washington DC: American Society for Microbiology; 1992. p. 1.5.1-1.5.18.
Ncube NS, Afolayan AJ, Okoh AI. Assessment techniques of antimicrobial properties of natural compounds of plant origin: current methods and future trends. Afr J Biotechnol. 2008;7:1797–806.
Sakita KM, Conrado PCV, Faria DR, Arita GS, Capoci IR, Rodrigues-Vendramini FA, et al. Copolymeric micelles as efficient inert nanocarrier for hypericin in the photodynamic inactivation of Candida species. Future Microbiol. 2019;14:519–31.
Jin Y, Yip HK, Samaranayake YH, Yau JY, Samaranayake LP. Biofilm-forming ability of Candida albicans is unlikely to contribute to high levels of oral yeast carriage in cases of human immunodeficiency virus infection. J Clin Microbiol. 2003;41:2961–7.
Melo AS, Colombo AL, Arthington-Skaggs BA. Paradoxical growth effect of caspofungin observed on biofilms and planktonic cells of five different Candida species. Antimicrob Agents Chemother. 2007;51:3081–8.
Djordjevic D, Wiedmann M, Mclandsborough LA. Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation. Appl Environ Microbiol. 2002;68:2950–8.
Stepanović S, Vuković D, Hola V, Di Bonaventura G, Djukić S, Cirković I, Ruzicka F. Quantification of biofilm in microtiter plates. APMIS. 2007;115:891–9.
Barbosa JP, de Oliveira TR, Boni GC. Eucalyptus spp: Candida albicans antibiofilm activity. Ec Dental Sci. 2019;4:824–40.
Jadhav S, Shah R, Bhave M, Palombo EA. Inhibitory activity of yarrow essential oil on Listeria planktonic cells and biofilms. Food Control. 2013;29:125–30.
Blunt JW, Copp BR, Keyzers RA, Munro MHG, Prinsep MR. Marine natural products. Nat Prod Rep. 2017;34:235–94.
El-Hossary EM, Cheng C, Hamed MM, El-Sayed Hamed AN, Ohlsen K, Hentschel U, Abdelmohsen UR. Antifungal potential of marine natural products. Eur J Med Chem. 2017;126:631–51.
Tilvi S, Moriou C, Martin M-T, Gallard J-F, Sorres J, Patel K, et al. Agelastatin E, agelastatin F, and benzosceptrin C from the marine sponge Agelas dendromorpha. J Nat Prod. 2010;73(4):720–3.
Hamed ANE, Schmitz R, Bergermann A, Totzke F, Kubbutat M, Müller WEG, Youssef DTA, Bishr MM, Kamel MS, Edrada-Ebel R, Wätjen W, Proksch P. Bioactive pyrrole alkaloids isolated from the Red Sea: marine sponge Stylissa carteri. Z Naturforsch C J Biosci. 2018;73(5–6):199–210.
Nazemi M, Alidoust Salimi M, Alidoust Salimi P, Motallebi A, Tamadoni Jahromi S, Ahmadzadeh O. Antifungal and antibacterial activity of Haliclona sp. from the Persian Gulf. Iran J Mycol Med. 2014;24:220–4.
Galeano E, Martínez A. Antimicrobial activity of marine sponges from Urabá Gulf Colombian Caribbean region. J Mycol Med. 2007;17:21–4.
Dogan E, Demir O, Sertdemir M, Saracli MA, Konuklugil B. Screening of the selected marine sponges from the coasts of Turkey for antimicrobial activity. Indian J Geo-Marine Sci. 2018;47:1193–8.
Glöckner A, Cornely OA. Candida glabrata - unique features and challenges in the clinical management of invasive infections. Mycoses. 2015;58:445–50.
Zidar N, Montalvão S, Hodnik Z, Nawrot DA, Zula A, Ilas J. Antimicrobial activity of the marine alkaloids, clathrodin and oroidin, and their synthetic analogues. Mar Drugs. 2014;12:940–63.
Stout EP, Yu LC, Molinski TF. Antifungal diterpene alkaloids from the Caribbean sponge Agelas citrina: unified configurational assignments of agelasidines and agelasines. Eur J Org Chem. 2012;27:5131–5.
Hammami S, Bergaoui A, Boughalleb N, Romdhane A, Khoja I, Kamel MBH, Mighri Z. Antifungal effects of secondary metabolites isolated from marine organisms collected from the Tunisian coast. Comptes Rendus Chim. 2010;13:1397–400.
Campana R, Favi G, Baffone W, Lucarini S. Marine alkaloid 2,2-bis(6-bromo-3-indolyl) ethylamine and its synthetic derivatives inhibit microbial biofilms formation and disaggregate developed biofilms. Microorganisms. 2019;7:1–2.
Delaloye J, Calandra T. Invasive candidiasis as a cause of sepsis in the critically ill patient. Virulence. 2014;5:154–62.
Tóth R, Nosek J, Mora-Montes HM, Gabaldon T, Bliss JM, Nosanchuk JD, Turner SA, Butler G, Vágvölgyi C, Gácser A. Candida parapsilosis: from Genes to the Bedside. Clin Microbiol Rev. 2019 Feb 27;32(2):e00111-e118.
Modrzewska B, Kurnatowski P. Adherence of Candida sp. to host tissues and cells as one of its pathogenicity features. Ann Parasitol. 2015;61:3–9.
Chaves GM, Diniz MG, Silva-Rocha WP, Souza LB, Gondim LA, Ferreira MA. Species distribution and virulence factors of Candida spp. isolated from the oral cavity of kidney transplant recipients in Brazil. Mycopathologia. 2013;175:255–63.
Tumbarello M, Posteraro B, Trecarichi EM, Fiori B, Rossi M, Porta R, et al. Biofilm production by Candida species and inadequate antifungal therapy as predictors of mortality for patients with candidemia. J Clin Microbiol. 2007;45:1843–50.
Pannanusorn S, Fernandez V, Römling U. Prevalence of biofilm formation in clinical isolates of Candida species causing bloodstream infection. Mycoses. 2013;56:264–72.
Cepas V, López Y, Gabasa Y, Martins CB, Ferreira JD, Correia MJ, et al. Inhibition of bacterial and fungal biofilm formation by 675 extracts from microalgae and cyanobacteria. Antibiotics. 2019;8:1–12.
Zore GB, Thakre AD, Jadhav S, Karuppayil SM. Terpenoids inhibit Candida albicans growth by affecting membrane integrity and arrest of cell cycle. Phytomedicine. 2011;18:1181–90.
Monteiro DR, Feresin LP, Arias LS, Barão VAR, Barbosa DB, Delbem ACB. Effect of tyrosol on adhesion of Candida albicans and Candida glabrata to acrylic surfaces. Med Mycol. 2015;53:656–65.
Cai A, Kleij AW. Regio and enantio selective preparation of chiral allylic sulfones featuring elusive quaternary stereocenters. Angew Chemie 2019;58:14944–9.
Tampieri MP, Galuppi R, MacChioni F, Carelle MS, Falcioni L, Cionim PL, Morelli I. The inhibition of Candida albicans by selected essential oils and their major components. Mycopathologia. 2005;159:339–45.
Paduch R, Kandefer-Szerszeń M, Trytek M, Fiedurek J. Terpenes: substances useful in human healthcare. Arch Immunol Ther Exp (Warsz). 2007;55:315–27.
Chandrasekhar S, Kumar TP, Haribabu K, Reddy CR. Hydroxyphthalimide allied triazole-pyrrolidine catalyst for asymmetric Michael additions in water. Tetrahedron Asymmetry. 2010;21:2372–5.
Bakulev V, Dehaen W, Beryozkina T. Thermal rearrangements and transformations of 1,2,3-triazoles. In: Dehaen W, Bakulev V, editors. Chemistry of 1,2,3-triazoles. Springer, Cham: Topics in Heterocyclic Chemistry; 2014. p. 40.
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We are grateful to Conselho Nacional de Desenvolvimento Científico e Tecnológico or the National Council for Scientific and Technological Development (CNPq) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for their structural and financial support to this work.
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MCNDP and RMA executed, analyzed, and interpreted the data for the sponge Agelas dispar extraction and fractionation, liquid chromatography, and mass spectrometry. ACVJ and VSA executed and analyzed the data for the antifungal and antibiofilm activities in the formation and maturation of biofilm among 13 strains of Candida species, designed the work, prepared the article, and translated it into English. JPB and JFH executed and analyzed the data for treated and untreated biofilm samples for visualization using scanning electron microscopy (SEM). DB and MARS identified the Candida species and participated in the preparation of the article.
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Júnior, A.C.V., de Castro Nogueira Diniz Pontes, M., Barbosa, J.P. et al. Antibiofilm and Anti-Candidal Activities of the Extract of the Marine Sponge Agelas dispar. Mycopathologia 186, 819–832 (2021). https://doi.org/10.1007/s11046-021-00591-9
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DOI: https://doi.org/10.1007/s11046-021-00591-9