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Untargeted metabolomics to evaluate antifungal mechanism: a study of Cophinforma mamane and Candida albicans interaction |
| Asih Triastuti1,2, Marieke Vansteelandt1, Fatima Barakat1, Carlos Amasifuen3, Patricia Jargeat4, Mohamed Haddad1 |
1 UMR 152 Pharma Dev, IRD, UPS, Université de Toulouse, 31400 Toulouse, France;
2 Department of Pharmacy, Universitas Islam Indonesia, Yogyakarta 55584, Indonesia;
3 Dirección de Recursos Genéticos y Biotecnología, Instituto Nacional de Innovación Agraria, Avenida La Molina 1981, La Molina, Lima 15024, Peru;
4 Laboratoire Evolution et Diversité Biologique UMR 5174, CNRS, IRD, UPS, Université de Toulouse, 31062 Toulouse, France |
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Abstract Microbial interactions between filamentous fungi and yeast are still not fully understood. To evaluate a potential antifungal activity of a filamentous fungus while highlighting metabolomic changes, co-cultures between an endophytic strain of Cophinforma mamane (CM) and Candida albicans (CA) were performed. The liquid cultures were incubated under static conditions and metabolite alterations during the course were investigated by ultra-performance liquid chromatography-tandem mass spectrophotometry (UPLC-MS/MS). Results were analyzed using MS-DIAL, MSFINDER, METLIN, Xcalibur, SciFinder, and MetaboAnalyst metabolomics platforms. The metabolites associated with catabolic processes, including the metabolism of branched-chain amino acids, carnitine, and phospholipids were upregulated both in the mono and co-cultures, indicating fungal adaptability to environmental stress. Several metabolites, including C20 sphinganine 1-phosphate, myo-inositol, farnesol, gamma-undecalactone, folinic acid, palmitoleic acid, and MG (12:/0:0/0:0) were not produced by CA during co-culture with CM, demonstrating the antifungal mechanism of CM. Our results highlight the crucial roles of metabolomics studies to provide essential information regarding the antifungal mechanism of C. mamane against C. albicans, especially when the lost/undetected metabolites are involved in fungal survival and pathogenicity.
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| Keywords
Metabolomics
Fungal co-culture
Anti-fungal
Virulence
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Corresponding Authors:
Asih Triastuti,E-mail:asih.triastuti@uii.ac.id;Mohamed Haddad,E-mail:mohamed.haddad@ird.fr
E-mail: asih.triastuti@uii.ac.id;mohamed.haddad@ird.fr
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Issue Date: 08 March 2023
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1. Dadar M, Tiwari R, Karthik K, Chakraborty S, Shahali Y, Dhama K. Candida albicans-biology, molecular characterization, pathogenicity, and advances in diagnosis and control-an update. Microb Pathog. 2018;117:128-38.
2. Mayer FL, Wilson D, Hube B. Candida albicans pathogenicity mechanisms. Virulence. 2013;4:119-28.
3. Cavalheiro M, Teixeira MC. Candida biofilms:threats, challenges, and promising strategies. Front Med. 2018;5:1-15.
4. Desai J. Candida albicans hyphae:from growth initiation to invasion. J Fungi. 2018;4:10.
5. De Sordi L, Mühlschlegel FA. Quorum sensing and fungal-bacterial interactions in Candida albicans:a communicative network regulating microbial coexistence and virulence. FEMS Yeast Res. 2009;9:990-9.
6. Verbeke F, De Craemer S, Debunne N, Janssens Y, Wynendaele E, Van de Wiele C, De Spiegeleer B. Peptides as quorum sensing molecules:measurement techniques and obtained levels in vitro and in vivo. Front Neurosci. 2017;11:1-18.
7. Černakova L, Dižova S, Gaškova D, Jancíkova I, Bujdakova H. Impact of farnesol as a modulator of efflux pumps in a fluconazole-resistant strain of Candida albicans. Microb Drug Res. 2019;25:805-12.
8. Barakat F, Vansteelandt M, Triastuti A, Jargeat P, Jacquemin D, Graton J, Mejia K, Cabanillas B, Vendier L, Stigliani J-L, et al. Thiodiketopiperazines with two spirocyclic centers extracted from Botryosphaeria mamane, an endophytic fungus isolated from Bixa orellana L. Phytochemistry. 2019;158:1-7.
9. Pongcharoen W, Rukachaisirikul V, Phongpaichit S, Sakayaroj J. A new dihydrobenzofuran derivative from the endophytic fungus Botryosphaeria mamane PSU-M76. Chem Pharm Bull. 2007;55:1404-5.
10. Hussain H, Jabeen F, Krohn K, Al-Harrasi A, Ahmad M, Mabood F, Shah A, Badshah A, Rehman NU, Green IR, et al. Antimicrobial activity of two mellein derivatives isolated from an endophytic fungus. Med Chem Res. 2015;24:2111-4.
11. Mitaka Y, Mori N, Matsuura K. A termite fungistatic compound, mellein, inhibits entomopathogenic fungi but not egg-mimicking termite ball fungi. Appl Entomol Zool. 2019;54:39-46.
12. Berkow EL, Lockhart SR, Ostrosky-Zeichner L. Antifungal susceptibility testing:current approaches. Clin Microbiol Rev. 2020;33:1-30.
13. Elisashvili V. Submerged cultivation of medicinal mushrooms:bioprocesses and products. Int J Med Mushrooms. 2012;14:211-39.
14. Cui YQ, Van Der Lans RGJM, Luyben KCAM. Effect of agitation intensities on fungal morphology of submerged fermentation. Biotechnol Bioeng. 1997;55:15-726.
15. Papagianni M. Fungal morphology and metabolite production in submerged mycelial processes. Biotechnol Adv. 2004;22:189-259.
16. Guijas C, Montenegro-Burke JR, Warth B, Spilker ME, Siuzdak G. Metabolomics activity screening for identifying metabolites that modulate phenotype. Nat Biotechnol. 2018;36:316-20.
17. Lee WNP. Characterizing phenotype with tracer based metabolomics. Metabolomics. 2006;2:31-9.
18. Gromski PS, Muhamadali H, Ellis DI, Xu Y, Correa E, Turner ML, Goodacre R. A tutorial review:metabolomics and partial least squares-discriminant analysis-a marriage of convenience or a shotgun wedding. Anal Chim Acta. 2015;879:10-23.
19. Kajula M, Ward JM, Turpeinen A, Tejesvi MV, Hokkanen J, Tolonen A, Hakkanen H, Picart P, Ihalainen J, Sahl HG, et al. Bridged epipolythiodiketopiperazines from Penicillium raciborskii, an endophytic fungus of Rhododendron tomentosum. J Nat Prod. 2016;79:685-90.
20. Iwasa E, Hamashima Y, Sodeoka M. Epipolythiodiketopiperazine Alkaloids:total syntheses and biological activities. Isr J Chem. 2011;51:420-33.
21. Evidente A, Fiore M, Bruno G, Sparapano L, Motta A. Chemical and biological characterisation of sapinopyridione, a phytotoxic 3,3,6-trisubstituted- 2,4-pyridione produced by sphaeropsis sapinea, a toxigenic pathogen of native and exotic conifers, and its derivatives. Phytochemistry. 2006;67:1019-28.
22. Cowart LA, Obeid LM. Yeast sphingolipids:recent developments in understanding biosynthesis, regulation, and function. Biochim Biophys Acta. 2007;1771:421-31.
23. Vandenbosch D, Bink A, Govaert G, Cammue BPA, Nelis HJ, Thevissen K, Coenye T. Phytosphingosine-1-phosphate is a signaling molecule involved in miconazole resistance in sessile Candida albicans Cells. Antimicrob Agents Chemother. 2012;56:2290-4.
24. Jin JH, Seyfang A. High-affinity myo-inositol transport in Candida albicans:substrate specificity and pharmacology. Microbiology. 2003;149:3371-81.
25. Michell RH. Inositol derivatives:evolution and functions. Nat Rev Mol Cell Biol. 2008;9:151-61.
26. Reynolds TB. Strategies for acquiring the phospholipid metabolite inositol in pathogenic bacteria, fungi and protozoa:making it and taking it. Microbiology. 2009;155:1386-96.
27. Polke M, Leonhardt I, Kurzai O, Jacobsen ID. Farnesol signalling in candida albicans-more than just communication. Crit Rev Microbiol. 2018;44:230-43.
28. Alem MAS, Oteef MDY, Flowers TH, Douglas LJ. Production of tyrosol by candida albicans biofilms and its role in quorum sensing and biofilm development. Eukaryot Cell. 2006;5:1770-9.
29. Han TL, Cannon RD, Villas-Bôas SG. The metabolic basis of Candida albicans morphogenesis and quorum sensing. Fungal Genet Biol. 2011;48:747-63.
30. Pereira E, Santos A, Reis F, Tavares RM, Baptista P, Lino-Neto T, Almeida- Aguiar C. A new effective assay to detect antimicrobial activity of filamentous fungi. Microbiol Res. 2013;168:1-5.
31. García-Martínez T, Peinado RA, Moreno J, García-García I, Mauricio JC. Co-culture of Penicillium chrysogenum and Saccharomyces cerevisiae leading to the immobilization of yeast. J Chem Technol Biotechnol. 2011;86:812-7.
32. White TJ, Bruns T, Lee S, Taylor J. Amplification and direct sequencing of fungal ribosomal rna genes for phylogenetics. In:PCR protocols:a guide to methods and applications; 1990; pp. 315-322.
33. Triastuti A, Vansteelandt M, Barakat F, Trinel M, Jargeat P, Fabre N, Amasifuen Guerra CA, Mejia K, Valentin A, Haddad M. How histone deacetylase inhibitors alter the secondary metabolites of Botryosphaeria mamane, an endophytic fungus isolated from Bixa orellana. Chem Biodivers. 2019;16:e1800485.
34. Tsugawa H, Cajka T, Kind T, Ma Y, Higgins B, Ikeda K, Kanazawa M, VanderGheynst J, Fiehn O, Arita M. MS-DIAL:data-independent ms/ms deconvolution for comprehensive metabolome analysis. Nat Methods. 2015;12:523-6.
35. Pang Z, Zhou G, Ewald J, Chang L, Hacariz O, Basu N, Xia J. Using metaboanalyst 5.0 for LC-HRMS spectra processing, multi-omics integration and covariate adjustment of global metabolomics Data. Nat Protoc. 2022;17:1735-61.
36. Tsugawa H, Kind T, Nakabayashi R, Yukihira D, Tanaka W, Cajka T, Saito K, Fiehn O, Arita M. Hydrogen rearrangement rules:computational ms/ms fragmentation and structure elucidation using MS-FINDER software. Anal Chem. 2016;88:7946-58. |
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