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

https://doi.org/10.17221/234/2020-CJFSCitation:

Xin Y.H., Yang J., Zhao S.H., Chen K.W., Zhao Y.Q., Zhang T.D., Zhang J.H. (2022): Sea buckthorn (Hippophae rhamnoides L.) oil exhibits antifungal activity against Aspergillus flavus via disrupting mitochondrial function. Czech J. Food Sci., 40: 179–186.

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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.

References:
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. https://doi.org/10.1016/j.phymed.2007.03.018
 
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. https://doi.org/10.18632/oncotarget.18460
 
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. https://doi.org/10.1007/s11130-017-0610-9
 
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. https://doi.org/10.1016/S0955-2863(02)00179-1
 
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. https://doi.org/10.1016/j.pbi.2004.03.007
 
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. https://doi.org/10.3390/molecules21060770
 
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. https://doi.org/10.1016/S0378-8741(03)00154-5
 
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.
 
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. https://doi.org/10.1007/s12550-018-0313-6
 
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. https://doi.org/10.1016/S0925-4439(02)00222-3
 
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. https://doi.org/10.1016/j.burns.2013.08.011
 
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.
 
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.
 
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.
 
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. https://doi.org/10.1016/j.seppur.2011.06.008
 
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. https://doi.org/10.1134/S1021443710060142
 
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. https://doi.org/10.1007/s12257-011-0548-y
 
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.
 
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. https://doi.org/10.1021/jf0354038
 
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. https://doi.org/10.1016/j.foodchem.2017.04.172
 
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. https://doi.org/10.1016/j.crci.2013.10.020
 
Nakayama H., Otsu K. (2018): Mitochondrial DNA as an inflammatory mediator in cardiovascular diseases. Biochemical Journal, 475: 839–852. https://doi.org/10.1042/BCJ20170714
 
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. https://doi.org/10.1016/j.jtbi.2008.09.037
 
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. https://doi.org/10.1016/j.foodchem.2004.07.009
 
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. https://doi.org/10.1083/jcb.200408145
 
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. https://doi.org/10.1007/s11746-006-1213-z
 
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.
 
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. https://doi.org/10.3390/ijms11041842
 
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.
 
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.
 
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.
 
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. https://doi.org/10.1016/j.foodchem.2010.09.057
 
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. https://doi.org/10.1016/j.fct.2009.02.002
 
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. https://doi.org/10.1016/j.bbagen.2009.05.002
 
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. https://doi.org/10.1007/s12011-015-0273-z
 
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.
 
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.
 
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. https://doi.org/10.1007/s11814-011-0279-y
 
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. https://doi.org/10.1021/jf001059s
 
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.
 
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. https://doi.org/10.1016/j.foodchem.2015.01.077
 
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