Abstract
The purpose of this study was to isolate tea saponin from defatted C. oleifera cake and explore its potential antifungal activity and mechanism. UHPLC–MS/MS identified the compounds, and the antibacterial activity of tea saponin was determined by the inhibition zone method and double dilution method. In addition, the influence of tea saponin on the cell membrane, hyphae, and biofilm was studied to explore the antifungal mechanism of tea saponin. The results showed that the purity of tea saponin was 90.61%, and the main components of C. oleifera saponins were oleiferasaponin D3. Tea saponin has an apparent inhibitory effect on fungus. The minimum inhibitory concentrations (MIC) of the tea saponin against C. albicans, S. cerevisiae, and Penicillium were 0.078, 0.156, and 0.156 mg/mL, while the minimum fungicidal concentrations (MFC) were 0.312, 0.625, and 0.625 mg/mL, respectively. Tea saponin could destroy the cell membrane structure, which led to the leakage of cell contents and inhibited the growth of mycelium, reduced cell adhesion and aggregation, and effectively inhibited the formation of biofilm of C. albicans. Transcriptomic analyses indicated that tea saponin could down-regulate the expression of several hyphae- and biofilm-related genes (ALS3, ECE1, HWP1, EFG1, and UME6). This study confirmed that tea saponin from C. oleifera cake can be used as an effective source of natural antifungal agents and provide guidance on their utilization in the field of food safety.
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Abbreviations
- C. oleifera :
-
Camellia oleifera Abel
- C. albicans :
-
Candida albicans
- S. cerevisiae :
-
Saccharomyces cerevisiae
- AO/EB:
-
Acridine orange/ethidium bromide
- SEM:
-
Scanning electron microscope
- MIC:
-
Minimum inhibitory concentrations
- MFC:
-
Minimum fungicidal concentrations
- UHPLC–MS/MS:
-
Ultrahigh pressure liquid chromatography–high-resolution mass spectrometer
References
Dong S, Yang X, Zhao L, Zhang F, Hou Z, Xue P (2020) Antibacterial activity and mechanism of action saponins from Chenopodium quinoa Willd. husks against foodborne pathogenic bacteria. Ind Crops Prod. https://doi.org/10.1016/j.indcrop.2020.112350
Riesute R, Salomskiene J, Moreno DS, Gustiene S (2021) Effect of yeasts on food quality and safety and possibilities of their inhibition. Trends Food Sci Technol 108:1–10. https://doi.org/10.1016/j.tifs.2020.11.022
Perfect JR (2017) The antifungal pipeline: a reality check. Nat Rev Drug Discov 16(9):603–616. https://doi.org/10.1038/nrd.2017.46
Papoutsis K, Mathioudakis MM, Hasperué JH, Ziogas V (2019) Non-chemical treatments for preventing the postharvest fungal rotting of citrus caused by Penicillium digitatum (green mold) and Penicillium italicum (blue mold). Trends Food Sci Technol 86:479–491. https://doi.org/10.1016/j.tifs.2019.02.053
Rajasekar V, Darne P, Prabhune A, Kao RYT, Solomon AP, Ramage G, Samaranayake L, Neelakantan P (2021) A curcumin-sophorolipid nanocomplex inhibits Candida albicans filamentation and biofilm development. Colloids Surf B Biointerfaces 200:111617. https://doi.org/10.1016/j.colsurfb.2021.111617
Chen L, Wang Z, Liu L, Qu S, Mao Y, Peng X, Li YX, Tian J (2019) Cinnamaldehyde inhibits Candida albicans growth by causing apoptosis and its treatment on vulvovaginal candidiasis and oropharyngeal candidiasis. Appl Microbiol Biotechnol 103(21–22):9037–9055. https://doi.org/10.1007/s00253-019-10119-3
Kadosh D (2019) Regulatory mechanisms controlling morphology and pathogenesis in Candida albicans. Curr Opin Microbiol 52:27–34. https://doi.org/10.1016/j.mib.2019.04.005
Tsui C, Kong EF, Jabra-Rizk MA (2016) Pathogenesis of Candida albicans biofilm. Pathog Dis 74(4):ftw018. https://doi.org/10.1093/femspd/ftw018
Wall G, Montelongo-Jauregui D, Vidal Bonifacio B, Lopez-Ribot JL, Uppuluri P (2019) Candida albicans biofilm growth and dispersal: contributions to pathogenesis. Curr Opin Microbiol 52:1–6. https://doi.org/10.1016/j.mib.2019.04.001
Pisoschi AM, Pop A, Georgescu C, Turcus V, Olah NK, Mathe E (2018) An overview of natural antimicrobials role in food. Eur J Med Chem 143:922–935. https://doi.org/10.1016/j.ejmech.2017.11.095
El-Saber Batiha G, Hussein DE, Algammal AM, George TT, Jeandet P, Al-Snafi AE, Tiwari A, Pagnossa JP, Lima CM, Thorat ND, Zahoor M, El-Esawi M, Dey A, Alghamdi S, Hetta HF, Cruz-Martins N (2021) Application of natural antimicrobials in food preservation: recent views. Food Control. https://doi.org/10.1016/j.foodcont.2021.108066
Liang H, Hao B-Q, Chen G-C, Ye H, Ma J (2017) Camellia as an oilseed crop. HortScience 52(4):488–497. https://doi.org/10.21273/hortsci11570-16
Zong J, Wang R, Bao G, Ling T, Zhang L, Zhang X, Hou R (2015) Novel triterpenoid saponins from residual seed cake of Camellia oleifera Abel. show anti-proliferative activity against tumor cells. Fitoterapia 104:7–13. https://doi.org/10.1016/j.fitote.2015.05.001
Gao C, Cai C, Liu J, Wang Y, Chen Y, Wang L, Tan Z (2020) Extraction and preliminary purification of polysaccharides from Camellia oleifera Abel. seed cake using a thermoseparating aqueous two-phase system based on EOPO copolymer and deep eutectic solvents. Food Chem 313:126164. https://doi.org/10.1016/j.foodchem.2020.126164
Zhang S, Zheng L, Zheng X, Ai B, Yang Y, Pan Y, Sheng Z (2019) Effect of steam explosion treatments on the functional properties and structure of camellia (Camellia oleifera Abel.) seed cake protein. Food Hydrocolloids 93:189–197. https://doi.org/10.1016/j.foodhyd.2019.02.017
Hong C, Chang C, Zhang H, Jin Q, Wu G, Wang X (2019) Identification and characterization of polyphenols in different varieties of Camellia oleifera seed cakes by UPLC-QTOF-MS. Food Res Int 126:108614. https://doi.org/10.1016/j.foodres.2019.108614
Kuo PC, Lin TC, Yang CW, Lin CL, Chen GF, Huang JW (2010) Bioactive saponin from tea seed pomace with inhibitory effects against Rhizoctonia solani. J Agric Food Chem 58(15):8618–8622. https://doi.org/10.1021/jf1017115
Yang WS, Ko J, Kim E, Kim JH, Park JG, Sung NY, Kim HG, Yang S, Rho HS, Hong YD, Shin SS, Cho JY (2014) 21-O-angeloyltheasapogenol E3, a novel triterpenoid saponin from the seeds of tea plants, inhibits macrophage-mediated inflammatory responses in a NF-kappaB-dependent manner. Mediators Inflamm 2014:658351. https://doi.org/10.1155/2014/658351
Jia LY, Wu XJ, Gao Y, Rankin GO, Pigliacampi A, Bucur H, Li B, Tu YY, Chen YC (2017) Inhibitory effects of total triterpenoid saponins isolated from the seeds of the tea plant (Camellia sinensis) on human ovarian cancer cells. Molecules. https://doi.org/10.3390/molecules22101649
Kim JD, Khan MI, Shin JH, Lee MG, Seo HJ, Shin TS, Kim MY (2016) HPLC fractionation and pharmacological assessment of green tea seed saponins for antimicrobial, anti-angiogenic and hemolytic activities. Biotechnol Bioprocess Eng 20(6):1035–1043. https://doi.org/10.1007/s12257-015-0538-6
Hu JL, Nie SP, Huang DF, Li C, Xie MY, Wan Y (2012) Antimicrobial activity of saponin-rich fraction from Camellia oleifera cake and its effect on cell viability of mouse macrophage RAW 264.7. J Sci Food Agric 92(12):2443–2449. https://doi.org/10.1002/jsfa.5650
Zhang XF, Yang SL, Han YY, Zhao L, Lu GL, Xia T, Gao LP (2014) Qualitative and quantitative analysis of triterpene saponins from tea seed pomace (Camellia oleifera Abel) and their activities against bacteria and fungi. Molecules 19(6):7568–7580. https://doi.org/10.3390/molecules19067568
Tang Y, He X, Sun J, Liu G, Li C, Li L, Sheng J, Zhou Z, Xin M, Ling D, Yi P, Zheng F, Li J, Li Z, Yang Y, Tang J, Chen X (2021) Comprehensive evaluation on tailor-made deep eutectic solvents (DESs) in extracting tea saponins from seed pomace of Camellia oleifera Abel. Food Chem 342:128243. https://doi.org/10.1016/j.foodchem.2020.128243
Zhao Y, Su R, Zhang W, Yao G-L, Chen J (2020) Antibacterial activity of tea saponin from Camellia oleifera shell by novel extraction method. Ind Crops Prod. https://doi.org/10.1016/j.indcrop.2020.112604
Cai R, Hu M, Zhang Y, Niu C, Yue T, Yuan Y, Wang Z (2019) Antifungal activity and mechanism of citral, limonene and eugenol against Zygosaccharomyces rouxii. Lwt 106:50–56. https://doi.org/10.1016/j.lwt.2019.02.059
Liang Z, Qi Y, Guo S, Hao K, Zhao M, Guo N (2019) Effect of AgWPA nanoparticles on the inhibition of Staphylococcus aureus growth in biofilms. Food Control 100:240–246. https://doi.org/10.1016/j.foodcont.2019.01.030
Yang L, Liu X, Zhong L, Sui Y, Quan G, Huang Y, Wang F, Ma T (2018) Dioscin inhibits virulence factors of Candida albicans. Biomed Res Int 2018:4651726. https://doi.org/10.1155/2018/4651726
de Souza MR, Teixeira RC, Daude MM, Augusto ANL, Sagio SA, de Almeida AF, Barreto HG (2021) Comparative assessment of three RNA extraction methods for obtaining high-quality RNA from Candida viswanathii biomass. J Microbiol Methods 184:106200. https://doi.org/10.1016/j.mimet.2021.106200
Fu HZ, Wan KH, Yan QW, Zhou GP, Feng TT, Dai M, Zhong RJ (2018) Cytotoxic triterpenoid saponins from the defatted seeds of Camellia oleifera Abel. J Asian Nat Prod Res 20(5):412–422. https://doi.org/10.1080/10286020.2017.1343822
Joshi R, Sood S, Dogra P, Mahendru M, Kumar D, Bhangalia S, Pal HC, Kumar N, Bhushan S, Gulati A, Saxena AK, Gulati A (2012) In vitro cytotoxicity, antimicrobial, and metal-chelating activity of triterpene saponins from tea seed grown in Kangra valley, India. Med Chem Res 22(8):4030–4038. https://doi.org/10.1007/s00044-012-0404-4
Lee JH, Kim YG, Khadke SK, Yamano A, Watanabe A, Lee J (2019) Inhibition of biofilm formation by Candida albicans and polymicrobial microorganisms by nepodin via hyphal-growth suppression. ACS Infect Dis 5(7):1177–1187. https://doi.org/10.1021/acsinfecdis.9b00033
Hu Q, Chen YY, Jiao QY, Khan A, Li F, Han DF, Cao GD, Lou HX (2018) Triterpenoid saponins from the pulp of Sapindus mukorossi and their antifungal activities. Phytochemistry 147:1–8. https://doi.org/10.1016/j.phytochem.2017.12.004
Shinobu-Mesquita CS, Bonfim-Mendonca PS, Moreira AL, Ferreira IC, Donatti L, Fiorini A, Svidzinski TI (2015) Cellular structural changes in Candida albicans caused by the hydroalcoholic extract from Sapindus saponaria L. Molecules 20(5):9405–9418. https://doi.org/10.3390/molecules20059405
Bi Z, Zhao Y, Morrell JJ, Lei Y, Yan L (2021) The antifungal mechanism of konjac flying powder extract and its active compounds against wood decay fungi. Ind Crops Prod. https://doi.org/10.1016/j.indcrop.2021.113406
Cho J, Choi H, Lee J, Kim MS, Sohn HY, Lee DG (2013) The antifungal activity and membrane-disruptive action of dioscin extracted from Dioscorea nipponica. Biochim Biophys Acta 3:1153–1158. https://doi.org/10.1016/j.bbamem.2012.12.010
Alcazar-Fuoli L, Mellado E (2014) Current status of antifungal resistance and its impact on clinical practice. Br J Haematol 166(4):471–484. https://doi.org/10.1111/bjh.12896
Sadowska B, Budzynska A, Wieckowska-Szakiel M, Paszkiewicz M, Stochmal A, Moniuszko-Szajwaj B, Kowalczyk M, Rozalska B (2014) New pharmacological properties of Medicago sativa and Saponaria officinalis saponin-rich fractions addressed to Candida albicans. J Med Microbiol 63(Pt 8):1076–1086. https://doi.org/10.1099/jmm.0.075291-0
Budzynska A, Sadowska B, Wieckowska-Szakiel M, Micota B, Stochmal A, Jedrejek D, Pecio L, Rozalska B (2014) Saponins of Trifolium spp. aerial parts as modulators of Candida albicans virulence attributes. Molecules 19(7):10601–10617. https://doi.org/10.3390/molecules190710601
Banti CN, Raptopoulou CP, Psycharis V, Hadjikakou SK (2021) Novel silver glycinate conjugate with 3D polymeric intermolecular self-assembly architecture; an antiproliferative agent which induces apoptosis on human breast cancer cells. J Inorg Biochem 216:111351. https://doi.org/10.1016/j.jinorgbio.2020.111351
Orsi CF, Borghi E, Colombari B, Neglia RG, Quaglino D, Ardizzoni A, Morace G, Blasi E (2014) Impact of Candida albicans hyphal wall protein 1 (HWP1) genotype on biofilm production and fungal susceptibility to microglial cells. Microb Pathog 69–70:20–27. https://doi.org/10.1016/j.micpath.2014.03.003
Nobile CJ, Schneider HA, Nett JE, Sheppard DC, Filler SG, Andes DR, Mitchell AP (2008) Complementary adhesin function in C. albicans biofilm formation. Curr Biol 18(14):1017–1024. https://doi.org/10.1016/j.cub.2008.06.034
Nobile CJ, Andes DR, Nett JE, Smith FJ, Yue F, Phan QT, Edwards JE, Filler SG, Mitchell AP (2006) Critical role of Bcr1-dependent adhesins in C. albicans biofilm formation in vitro and in vivo. PLoS Pathog 2(7):e63. https://doi.org/10.1371/journal.ppat.0020063
Phan QT, Myers CL, Fu Y, Sheppard DC, Yeaman MR, Welch WH, Ibrahim AS, Edwards JE Jr, Filler SG (2007) Als3 is a Candida albicans invasin that binds to cadherins and induces endocytosis by host cells. PLoS Biol 5(3):e64. https://doi.org/10.1371/journal.pbio.0050064
Banerjee M, Thompson DS, Lazzell A, Carlisle PL, Pierce C, Monteagudo C, Lopez-Ribot JL, Kadosh D (2008) UME6, a novel filament-specific regulator of Candida albicans hyphal extension and virulence. Mol Biol Cell 19(4):1354–1365. https://doi.org/10.1091/mbc.E07-11-1110
Lassak T, Schneider E, Bussmann M, Kurtz D, Manak JR, Srikantha T, Soll DR, Ernst JF (2011) Target specificity of the Candida albicans Efg1 regulator. Mol Microbiol 82(3):602–618. https://doi.org/10.1111/j.1365-2958.2011.07837.x
Acknowledgements
This work was supported by the Forestry Science and Technology Innovation Project of Guangdong Province (2017KJCX005).
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This work was supported by the Forestry Science and Technology Innovation Project of Guangdong Province (2017KJCX005).
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ZY: writing—original draft, data curation, writing—review and editing, software. XW: conceptualization, formal analysis, methodology, resources, writing—review and editing, project administration, fund applicant. JH: investigation, instrumental analysis, data collection.
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Yu, Z., Wu, X. & He, J. Study on the antifungal activity and mechanism of tea saponin from Camellia oleifera cake. Eur Food Res Technol 248, 783–795 (2022). https://doi.org/10.1007/s00217-021-03929-1
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DOI: https://doi.org/10.1007/s00217-021-03929-1