Czech J. Food Sci., 2022, 40(3):179-186 | DOI: 10.17221/234/2020-CJFS

Sea buckthorn (Hippophae rhamnoides L.) oil exhibits antifungal activity against Aspergillus flavus via disrupting mitochondrial functionOriginal Paper

Yanhua Xin*,1,2, Jie Yang1, Sanhu Zhao1, Kewen Chen1, Yaqin Zhao1, Tiedan Zhang2, Jianhua Zhang1
1 Department of Bioengineering, Xinzhou Teachers University, Xinzhou, China
2 Ones Sun Health Industry Limited Company, Guangdong, China

The present study sought to examine how sea buckthorn (SBT) oil impacts mitochondrial and overall functionality in Aspergillus flavus. In order to assess the effect of SBT oil, it was used to treat mycelia across a range of concentrations, after which mitochondrial structures were imaged via transmission electron microscopy (TEM). In order to explore the functional impact of this treatment, we additionally examined reactive oxygen species (ROS) production, malondialdehyde (MDA) levels, enzyme activity, and shifts in mitochondrial membrane potential (ΔΨm) following treatment. We found that SBT oil induced mitochondrial damage in A. flavus in a dose-dependent manner, resulting in altered succinate dehydrogenase (SDH) and adenosine triphosphatase (ATPase) activity, reduced ΔΨm levels, and markedly elevated MDA and ROS levels. Together, these findings suggest that SBT oil can mediate antifungal activity against A. flavus through a mechanism associated with its ability to disrupt the tricarboxylic acid (TCA) cycle and mitochondrial potential, leading to MDA and ROS accumulation.

Keywords: sea buckthorn oil; mould; antifungal mechanism; mitochondria

Published: June 29, 2022  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Xin Y, Yang J, Zhao S, Chen K, Zhao Y, Zhang T, Zhang J. Sea buckthorn (Hippophae rhamnoides L.) oil exhibits antifungal activity against Aspergillus flavus via disrupting mitochondrial function. Czech J. Food Sci. 2022;40(3):179-186. doi: 10.17221/234/2020-CJFS.
Download citation

References

  1. Basu M., Prasad R., Jayamurthy P., Pal K., Arumughan C., Sawhney R.C. (2007): Anti-atherogenic effects of seabuckthorn (Hippophaea rhamnoides) seed oil. Phytomedicine, 14: 770-777. Go to original source... Go to PubMed...
  2. Borgna V., Villegas J., Burzio V.A., Belmar S., Araya M., Jeldes E., Lobos-González L., Silva V., Villota C., Oliveira-Cruz L. (2017): Mitochondrial ASncmtRNA-1 and ASncmtRNA-2 as potent targets to inhibit tumor growth and metastasis in the RenCa murine renal adenocarcinoma model. Oncotarget, 8: 43692-43708. Go to original source... Go to PubMed...
  3. Czaplicki S., Ogrodowska D., Zadernowski R., Konopka I. (2007): Effect of sea-buckthorn (Hippophaea rhamnoides) pulp oil consumption on fatty acids and vitamin A and E accumulation in adipose tissue and liver of rats. Plant Foods for Human Nutrition, 72: 198-204. Go to original source... Go to PubMed...
  4. Eccleston C., Baoru Y., Tahvonen R., Kallio H., Rimbach G.H., Minihane A.M. (2002): Effects of an antioxidant-rich juice (sea buckthorn) on risk factors for coronary heart disease in humans. Journal of Nutritional Biochemistry, 13: 346-354. Go to original source... Go to PubMed...
  5. Fernie A.R., Carrari F., Sweetlove L.J. (2004): Respiratory metabolism: Glycolysis, the TCA cycle and mitochondrial electron transport. Current Opinion in Plant Biology, 7: 254-261. Go to original source... Go to PubMed...
  6. Gao T., Zhou H., Zhou W., Hu L., Chen J., Shi Z. (2016): The fungicidal activity of thymol against Fusarium graminearum via inducing lipid peroxidation and disrupting ergosterol biosynthesis. Molecules, 21: 770. Go to original source... Go to PubMed...
  7. Geetha S., Ram M.S., Mongia S.S., Singh V., Ilavazhagan G., Sawhney R.C. (2003): Evaluation of antioxidant activity of leaf extract of seabuckthorn (Hippophae rhamnoides L.) on chromium (VI) induced oxidative stress in albino rats. Journal of Ethnopharmacology, 87: 247-251. Go to original source... Go to PubMed...
  8. Gupta S., Gupta A., Ahmed Z., Kumar A. (2011): Antibacterial and antifungal activity in leaf, seed extract and seed oil of seabuckthorn (Hippophae salicifolia D. Don) plant. Journal of Plant Pathology & Microbiology, 2: 1-4.
  9. Hua S.S.T., Palumbo J.D., Dan E.P., Sarreal S.B.L., O'Keeffe T.L. (2018): Development of a droplet digital PCR assay for population analysis of aflatoxigenic and atoxigenic Aspergillus flavus mixtures in soil. Mycotoxin Research, 34: 1-8. Go to original source... Go to PubMed...
  10. Huang H.M., Zhang H., Xu H., Gibson G.E. (2003): Inhibition of the α-ketoglutarate dehydrogenase complex alters mitochondrial function and cellular calcium regulation. Biochimica et Biophysica Acta, 1637: 119-126. Go to original source... Go to PubMed...
  11. Ito H., Asmussen S., Traber D.L., Cox R.A., Hawkins H.K., Connelly R., Traber L.D., Walker T.W., Malgerud E., Sakurai H. (2014): Healing efficacy of sea buckthorn (Hippophae rhamnoides L.) seed oil in an ovine burn wound model. Burns, 40: 511-519. Go to original source... Go to PubMed...
  12. Kamal Y.N., Sultan A.M. (2019) Could aflatoxin B1 production by Aspergillus flavus affect the severity of keratitis: An experience in two tertiary health care centers, Egypt. European Journal of Clinical Microbiology & Infectious Diseases Official Publication of the European Society of Clinical Microbiology, 38: 2021-2027. Go to original source... Go to PubMed...
  13. Kobayashi D., Kondo K., Uehara N., Otokozawa S., Tsuji N., Yagihashi A., Watanabe N. (2002): Endogenous reactive oxygen species is an important mediator of miconazole antifungal effect. Antimicrobial Agents & Chemotherapy, 46: 3113-3117. Go to original source... Go to PubMed...
  14. Kong W., Huang C., Chen Q., Zou Y., Zhang J. (2012): Nitric oxide alleviates heat stress-induced oxidative damage in Pleurotus eryngii var. tuoliensis. Fungal Genetics & Biology, 49: 15-20. Go to original source... Go to PubMed...
  15. Kagliwal L.D., Patil S.C., Pol A.S., Singhal R.S., Patravale V.B. (2011): Separation of bioactives from seabuckthorn seeds by supercritical carbon dioxide extraction methodology through solubility parameter approach. Separation and Purification Technology, 80: 533-540. Go to original source...
  16. Kuznetsova E.I., Pchelkin V.P., Tsydendambaev V.D., Vereshchagin A.G. (2010): Distribution of unusual fatty acids in the mesocarp triacylglycerols of maturing sea buckthorn fruits. Russian Journal of Plant Physiology, 57: 852-858. Go to original source...
  17. Kim H., Cho H., Seo Y.K., Kim S., Yoon M.Y., Kang H., Park C.S., Park J.K. (2012): Inhibitory effects of sea buckthorn (Hippophae rhamnoides L.) seed on UVB-induced photoaging in human dermal fibroblasts. Biotechnology and Bioprocess Engineering, 17: 465-474. Go to original source...
  18. Lanteri C.A., Trumpower B.L., Tidwell R.R., Meshnick S.R. (2004): DB75, a novel trypanocidal agent, disrupts mitochondrial function in Saccharomyces cerevisiae. Antimicrobial Agents & Chemotherapy, 48: 3968. Go to original source... Go to PubMed...
  19. Lee N.A., Wang S., Allan R.D., Kennedy I.R. (2004): A rapid aflatoxin B1 elisa: Development and validation with reduced matrix effects for peanuts, corn, pistachio, and soybeans. Journal of Agricultural and Food Chemistry, 52: 2746-2755. Go to original source... Go to PubMed...
  20. Li Y., Shao X., Xu J., Wei Y., Xu F., Wang H. (2017): Tea tree oil exhibits antifungal activity against Botrytis cinerea by affecting mitochondria. Food Chemistry, 234: 62-67. Go to original source... Go to PubMed...
  21. Manea A.M., Ungureanu C., Meghea A. (2014): Effect of vegetable oils on obtaining lipid nanocarriers for sea buckthorn extract encapsulation. Comptes Rendus - Chimie, 17: 934-943. Go to original source...
  22. Nakayama H., Otsu K. (2018): Mitochondrial DNA as an inflammatory mediator in cardiovascular diseases. Biochemical Journal, 475: 839-852. Go to original source... Go to PubMed...
  23. Nazaret C., Heiske M., Thurley K., Mazat J.P. (2009): Mitochondrial energetic metabolism: A simplified model of TCA cycle with ATP production. Journal of Theoretical Biology, 258: 455-464. Go to original source... Go to PubMed...
  24. Negi P.S., Chauhan A.S., Sadia G.A., Rohinishree Y.S., Ramteke R.S. (2006): Antioxidant and antibacterial activities of various seabuckthorn (Hippophae rhamnoides L.) seed extracts. Food Chemistry, 92: 119-124. Go to original source...
  25. Pozniakovsky A.I., Knorre D.A., Markova O.V., Hyman A.A., Skulachev V.P., Severin F.F. (2005): Role of mitochondria in the pheromone- and amiodarone-induced programmed death of yeast. Journal of Cell Biology, 168: 257-269. Go to original source... Go to PubMed...
  26. Ranjith A., Kumar K.S., Venugopalan V.V., Arumughan C., Sawhney R.C., Singh V. (2006): Fatty acids, tocols, and carotenoids in pulp oil of three sea buckthorn species (Hippophae rhamnoides, H. salicifolia, and H. tibetana) grown in the Indian Himalayas. Journal of the American Oil Chemists Society, 83: 359-364. Go to original source...
  27. Shi X., Li B., Qin, G., Tian S. (2012): Mechanism of antifungal action of borate against Colletotrichum gloeosporioides related to mitochondrial degradation in spores. Postharvest Biology & Technology, 67: 138-143. Go to original source...
  28. Sajfrtová M., Ličková I., Wimmerová M., Sovová H., Wimmer Z. (2010): β-sitosterol: Supercritical carbon dioxide extraction from sea buckthorn (Hippophae rhamnoides L.) seeds. International Journal of Molecular Sciences, 11: 1842-1850. Go to original source... Go to PubMed...
  29. Soares N.C.P., Teodoro A.J., Lotsch P.F., Granjeiro J.M., Borojevic R., Borojevic R. (2015): Anticancer properties of carotenoids in prostate cancer: A review. Histology and Histopathology, 30: 1143-1154. Go to PubMed...
  30. Thippeswamy S., Mohana D.C., Abhishek R.U., Manjunath K. (2018): Inhibitory activity of plant extracts on aflatoxin B1 biosynthesis by Aspergillus flavus. Journal of Agricultural Science & Technology, 16: 1123-1132.
  31. Tian J., Ban X., Zeng H., He J., Chen Y., Wang Y. (2012): The mechanism of antifungal action of essential oil from dill (Anethum graveolens L.) on Aspergillus flavus. Plos One, 7: e30147. Go to original source... Go to PubMed...
  32. Ting H.C., Hsu Y.W., Tsai C.F., Lu F.J., Chou M.C., Chen W.K. (2011): The in vitro and in vivo antioxidant properties of seabuckthorn (Hippophae rhamnoides L.) seed oil. Food Chemistry, 125: 652-659. Go to original source...
  33. Upadhyay N.K., Kumar R., Mandotra S.K., Meena R.N., Siddiqui M.S., Sawhney R.C., Gupta A. (2009): Safety and healing efficacy of sea buckthorn (Hippophae rhamnoides L.) seed oil on burn wounds in rats. Food and Chemical Toxicology, 47: 1146-1153. Go to original source... Go to PubMed...
  34. Wu X.Z., Cheng A.X., Sun L.M., Sun S.J., Lou H.X. (2009): Plagiochin E, an antifungal bis(bibenzyl), exerts its antifungal activity through mitochondrial dysfunction-induced reactive oxygen species accumulation in Candida albicans. Biochimica et Biophysica Acta (BBA) - General Subjects, 1790: 770-777. Go to original source... Go to PubMed...
  35. Yan X., Yang X., Hao X., Ren Q., Gao J., Wang Y., Chang N., Qiu Y., Song G. (2015): Sodium fluoride induces apoptosis in H9c2 cardiomyocytes by altering mitochondrial membrane potential and intracellular ROS level. Biological Trace Element Research, 166: 210-215. Go to original source... Go to PubMed...
  36. Yildiz H., Şengül M., Celik F., Duralija B. (2012): Bioactive content of sea buckthorn (Hippophae rhamnoides L.) berries from Turkey. Agriculturae Conspectus Scientificus (ACS), 77: 53-55.
  37. Yuan J., Chen Z., Guo Z., Li D., Zhang F., Shen J., Zhang Y., Wang S., Zhuang Z. (2018): PbsB regulates morphogenesis, aflatoxin B1 biosynthesis, and pathogenicity of Aspergillus flavus. Frontiers in Cellular & Infection Microbiology, 8: 162. Go to original source... Go to PubMed...
  38. Yoon M.Y., Oh J.S., Kang H., Park J.K. (2012): Antioxidant and antibacterial behavior for sediment removed ethanol extract from sea buckthorn seed. Korean Journal of Chemical Engineering, 29: 1069-1073. Go to original source...
  39. Yang B., Kallio H.P. (2011): Fatty acid composition of lipids in sea buckthorn (Hippophaë rhamnoides L.) berries of different origins. Journal of Agricultural and Food Chemistry, 49: 1939-1947. Go to original source... Go to PubMed...
  40. Yen C.H., Dai Y.S., Yang Y.H., Lee J.H., Chiang B.L. (2008): Linoleic acid metabolite levels and transepidermal water loss in children with atopic dermatitis. Annals of Allergy, Asthma & Immunology, 100: 66-73. Go to original source... Go to PubMed...
  41. Zheng S., Jing G., Wang X., Ouyang Q., Jia L., Tao N. (2015): Citral exerts its antifungal activity against Penicillium digitatum by affecting the mitochondrial morphology and function. Food Chemistry, 178: 76-81. Go to original source... Go to PubMed...

This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International (CC BY NC 4.0), which permits non-comercial use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.