Upgrading the accumulation of ginsenoside Rd in Panax notoginseng by a novel glycosidase-producing endophytic fungus G11-7

. 2023 Jun ; 68 (3) : 441-452. [epub] 20221226

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid36571675

Grantová podpora
31930076 National Natural Science Foundation of China
31922058 National Natural Science Foundation of China
3332022052,2572017AA08 Fundamental Research Funds for the Central Universities

Odkazy

PubMed 36571675
DOI 10.1007/s12223-022-01020-0
PII: 10.1007/s12223-022-01020-0
Knihovny.cz E-zdroje

A novel endophytic fungus producing beta-glucosidase was isolated and characterized from pigeon pea (Cajanus cajan [L.] Millsp.), which has excellent properties in converting ginsenoside Rb1 to ginsenoside Rd in Panax notoginseng. According to the 16S rDNA gene sequence, the G11-7 strain was identified as Fusarium proliferatum, and the accession number KY303906 was confirmed in GenBank. The G11-7 immobilized spores, in which the activity of beta-glucosidase could reach 0.95 U/mL, were co-cultured with P. notoginseng plant material to obtain a continuous beta-glucosidase supply for the biotransformation of ginsenoside Rb1 to Rd. Under the liquid-solid ratio (20:1), initial pH (6.0), and temperature (30 °C) constituents, the maximum ginsenoside Rd yield was obtained as 9.15 ± 0.65 mg/g, which was 3.67-fold higher than that without fungal spore co-culture (2.49 ± 0.98 mg/g). Furthermore, immobilized G11-7 spores showed significant beta-glucosidase producing ability which could be recovered and reused for 6 cycles. Overall, these results suggested that immobilized G11-7 offered a promising and effective approach to enhance the production of ginsenoside Rd for possible nutraceutical and pharmaceutical uses.

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Biswas T, Mathur A, Gupta V, Singh M, Mathur AK (2019) Salicylic acid and ultrasonic stress modulated gene expression and ginsenoside production in differentially affected Panax quinquefolius (L.) and Panax sikkimensis (Ban.) cell suspensions. Plant Cell. Tissue and Organ Culture (PCTOC) 136:575–588. https://doi.org/10.1007/s11240-018-01538-7 DOI

Chen G, Yang M, Song Y, Lu Z, Zhang J, Huang H, Wu L, Guo D (2008) Microbial transformation of ginsenoside Rb1 by Acremonium strictum. Appl Microbiol Biot 77:1345–1350. https://doi.org/10.1007/s00253-007-1258-4 DOI

Deshmukh SK, Verekar SA, Bhave SV (2015) Endophytic fungi: a reservoir of antibacterials. Front Microbiol. https://doi.org/10.3389/fmicb.2014.00715 PubMed DOI PMC

Fang H, Wei Y, Li Y, Zhou G (2020) One-pot process for the production of ginsenoside Rd by coupling enzyme-assisted extraction with selective enzymolysis. Biol Pharm Bull. https://doi.org/10.1248/bpb.b19-01127 PubMed DOI

Feng HW, Zhi YE, Sun YJ, Xu LR, Wang LM, Zhan XJ, Zhou P (2016) Insight into a novel β -1,4-glucosidase from streptomyces griseorubens JSD-1 DOI

Gai Q, Jiao J, Luo M, Wang W, Yao L, Fu Y (2017) Deacetylation biocatalysis and elicitation by immobilized Penicillium canescens in Astragalus membranaceus hairy root cultures: towards the enhanced and sustainable production of astragaloside IV. Plant Biotechnol J 15:297–305. https://doi.org/10.1111/pbi.12612 PubMed DOI

Gao J, Zhao X, Liu H, Fan Y, Cheng H, Liang F, Chen X, Wang N, Zhou Y, Tai G (2010) A highly selective ginsenoside Rb1-hydrolyzing β-d-glucosidase from Cladosporium fulvum. Process Biochem 45:897–903. https://doi.org/10.1016/j.procbio.2010.02.016 DOI

Gu Q, Duan G, Yu X (2019) Bioconversion of flavonoid glycosides from hippophae rhamnoides leaves into flavonoid aglycones by eurotium amstelodami. Microorganisms 7:122. https://doi.org/10.3390/microorganisms7050122 PubMed DOI PMC

Guan Y, Zhou J, Zhang Z, Wang G, Cai B, Hong L, Qiu Q, He H (2006) Ginsenoside-Rd from Panax notoginseng blocks Ca2+ influx through receptor- and store-operated Ca2+ channels in vascular smooth muscle cells. Eur J Pharmacol 548:129–136. https://doi.org/10.1016/j.ejphar.2006.08.001 PubMed DOI

Guo HB, Cui XM, An N, Cai GP (2010) Sanchi ginseng (Panax notoginseng (Burkill) F. H. Chen) in China: distribution, cultivation and variations. Genet Resour Crop Ev 57:453–460. https://doi.org/10.1007/s10722-010-9531-2 DOI

Han Y, Rhew KY (2013) Ginsenoside Rd induces protective anti-Candida albicans antibody through immunological adjuvant activity. Int Immunopharmacol 17:651–657. https://doi.org/10.1016/j.intimp.2013.08.003 PubMed DOI

Hu F, Zhong J (2008) Jasmonic acid mediates gene transcription of ginsenoside biosynthesis in cell cultures of Panax notoginseng treated with chemically synthesized 2-hydroxyethyl jasmonate. Process Biochem 43:113–118. https://doi.org/10.1016/j.procbio.2007.10.010 DOI

Jeong E, Kim S, Shin K, Oh D (2020) Biotransformation of protopanaxadiol-type ginsenosides in Korean ginseng extract into food-available compound k by an extracellular enzyme fromaspergillus niger. J Microbiol Biotechn 30:1560–1567. https://doi.org/10.4014/jmb.2007.07003 DOI

Jhun JY, Na HS, Shin JW, Jung KA, Seo HB, Ryu JY, Choi JW, Moon S, Park H, Oh S, Cho M, Min JK (2018) Notoginseng radix and rehmanniae radix preparata extract combination (YH23537) reduces pain and cartilage degeneration in rats with monosodium iodoacetate-induced osteoarthritis. J Med Food 21:745–754. https://doi.org/10.1089/jmf.2017.4041 PubMed DOI

Jiao J, Gai Q, Fu Y, Ma W, Peng X, Tan S, Efferth T (2014) Efficient production of isoflavonoids byastragalus membranaceus hairy root cultures and evaluation of antioxidant activities of extracts. J Agr Food Chem 62:12649–12658. https://doi.org/10.1021/jf503839m DOI

Jin S, Yang B, Cheng Y, Tan J, Kuang H, Fu Y, Bai X, Xie H, Gao Y, Lv C, Efferth T (2017) Improvement of resveratrol production from waste residue of grape seed by biotransformation of edible immobilized Aspergillus oryzae cells and negative pressure cavitation bioreactor using biphasic ionic liquid aqueous system pretreatment. Food Bioprod Process 102:177–185. https://doi.org/10.1016/j.fbp.2016.11.009 DOI

Kong Y, Wei Z, Fu Y, Gu C, Zhao C, Yao X, Efferth T (2011) Negative-pressure cavitation extraction of cajaninstilbene acid and pinostrobin from pigeon pea [Cajanus cajan (L.) Millsp.] leaves and evaluation of antioxidant activity. Food Chem 128:596–605. https://doi.org/10.1016/j.foodchem.2011.02.079 DOI

Lee D, Lee S, Jang E, Shin H, Moon B, Lee C (2016) Metabolomic profiles of aspergillus oryzae and bacillus amyloliquefaciens during rice koji fermentation. Molecules 21:773. https://doi.org/10.3390/molecules21060773 PubMed DOI PMC

Li SP, Qiao CF, Chen YW, Zhao J, Cui XM, Zhang QW, Liu XM, Hu DJ (2013) A novel strategy with standardized reference extract qualification and single compound quantitative evaluation for quality control of Panax notoginseng used as a functional food. J Chromatogr A. https://doi.org/10.1016/j.chroma.2013.07.025 PubMed DOI PMC

Li W, Fan D (2020) Biocatalytic strategies for the production of ginsenosides using glycosidase: current state and perspectives. Appl Microbiol Biot 104:3807–3823. https://doi.org/10.1007/s00253-020-10455-9 DOI

Lu C, Yin Y (2018) Optimum conversion of major ginsenoside Rb1 to minor ginsenoside Rg3(S) by pulsed electric field-assisted acid hydrolysis treatment. Open Chem 16:283–290. https://doi.org/10.1515/chem-2018-0031 DOI

Maran JP, Priya B (2015) Ultrasound-assisted extraction of pectin from sisal waste. Carbohyd Polym 115:732–738. https://doi.org/10.1016/j.carbpol.2014.07.058 DOI

Mei R, Shi Y, Duan W, Ding H, Zhang X, Cai L, Ding Z (2020) Biotransformation of α-terpineol byalternaria alternata. Rsc Adv 10:6491–6496. https://doi.org/10.1039/C9RA08042B PubMed DOI PMC

Neri DFM, Balcão VM, Costa RS, Rocha ICAP, Ferreira EMFC, Torres DPM, Rodrigues LRM, Carvalho LB, Teixeira JA (2009) Galacto-oligosaccharides production during lactose hydrolysis by free Aspergillus oryzae β-galactosidase and immobilized on magnetic polysiloxane-polyvinyl alcohol. Food Chem 115:92–99. https://doi.org/10.1016/j.foodchem.2008.11.068 DOI

Qian Y, Zhong L, Hou Y, Qu Y, Zhong Y (2016) Characterization and strain improvement of a hypercellulytic variant, trichoderma reesei SN1, by genetic engineering for optimized cellulase production in biomass conversion improvement. Front Microbiol. https://doi.org/10.3389/fmicb.2016.01349 PubMed DOI PMC

Quan L, Piao J, Min J, Kim H, Kim S, Yang D, Yang D (2011) Biotransformation of ginsenoside Rb1 to prosapogenins, gypenoside XVII, ginsenoside Rd, ginsenoside F2, and compound K by leuconostoc mesenteroides DC102. J Ginseng Res 35:344–351. https://doi.org/10.5142/jgr.2011.35.3.344 PubMed DOI PMC

Rai N, Kumari KP, Verma A, Kamble SC, Mishra P, Barik S, Kumar SS, Gautam V (2021) Plant associated fungal endophytes as a source of natural bioactive compounds. Mycology 12:139–159. https://doi.org/10.1080/21501203.2020.1870579 PubMed DOI PMC

Rao HKSJC (2020) Fascinating fungal endophytes associated with medicinal plants: recent advances and beneficial applications. Microbial Endophytes. https://doi.org/10.1016/B978-0-12-818734-0.00011-5 DOI

Razgonova M, Zakharenko A, Shin TS, Chung G, Golokhvast K (2020) Supercritical CO2 extraction and identification of ginsenosides in Russian and North Korean ginseng by HPLC with tandem mass spectrometry. Molecules. https://doi.org/10.3390/molecules25061407 PubMed DOI PMC

Riou C, Salmon JM, Vallier MJ, Gunata Z, Barre P (1998) Purification, characterization, and substrate specificity of a novel highly glucose-tolerant beta-glucosidase from Aspergillus oryzae. Appl Environ Microb 64:3607–3614. https://doi.org/10.1128/AEM.64.10.3607-3614.1998 DOI

Robl D, Delabona PS, Mergel CM, Rojas JD, Costa PS, Pimentel IC, Vicente VA, Da CPJ, Padilla G (2013) The capability of endophytic fungi for production of hemicellulases and related enzymes. Bmc Biotechnol 13:94. https://doi.org/10.1186/1472-6750-13-94 PubMed DOI PMC

Rusanova M, Rusanov K, Butterweck V, Atanassov I (2019) Exploring the capacity of endophytic fungi isolated from medicinal plants for fermentation and phenolics biotransformation of rose oil distillation wastewater. Biotechnol Biotechnol Equip 33:651–663. https://doi.org/10.1080/13102818.2019.1607778 DOI

Son J, Kim H, Oh D (2008) Ginsenoside Rd production from the major ginsenoside Rb1 by β-glucosidase from Thermus caldophilus. Biotechnol Lett 30:713–716. https://doi.org/10.1007/s10529-007-9590-4 PubMed DOI

Tamura T, Cui X, Sakaguchi N, Akashi M (2008) Ginsenoside Rd prevents and rescues rat intestinal epithelial cells from irradiation-induced apoptosis. Food Chem Toxicol 46:3080–3089. https://doi.org/10.1016/j.fct.2008.06.011 PubMed DOI

Voget S, Steele HL, Streit WR (2006) Characterization of a metagenome-derived halotolerant cellulase. J Biotechnol 126:26–36. https://doi.org/10.1016/j.jbiotec.2006.02.011 PubMed DOI

Wang C, McEntee E, Wicks S, Wu J, Yuan C (2006) Phytochemical and analytical studies of Panax notoginseng (Burk.) F.H. Chen J Nat Med-Tokyo 60:97–106. https://doi.org/10.1007/s11418-005-0027-x DOI

Wang X, Gai Z, Yu B, Feng J, Xu C, Yuan Y, Lin Z, Xu P (2007) Degradation of carbazole by microbial cells immobilized in magnetic gellan gum gel beads. Appl Environ Microb 73:6421–6428. https://doi.org/10.1128/AEM.01051-07 DOI

Wu J, Jin S, Wu S, Chen Y, Chen R (2018) Effect of filamentous fungi fermentation on the extractability and physicochemical properties of beta-glucan in oat bran. Food Chem 254:122–128. https://doi.org/10.1016/j.foodchem.2018.01.158 PubMed DOI

Xie W, Zhu T, Dong X, Nan F, Meng X, Zhou P, Sun G, Sun X (2019) HMGB1-triggered inflammation inhibition of notoginseng leaf triterpenes against cerebral ischemia and reperfusion injury via MAPK and NF-κB signaling pathways. Biomolecules (basel, Switzerland) 9:512. https://doi.org/10.3390/biom9100512 DOI

Xu L, Han T, Wu J, Zhang Q, Zhang H, Huang B, Rahman K, Qin L (2009) Comparative research of chemical constituents, antifungal and antitumor properties of ether extracts of Panax ginseng and its endophytic fungus. Phytomedicine 16:609–616. https://doi.org/10.1016/j.phymed.2009.03.014 PubMed DOI

Yan J, Jetten M, Rang J, Hu Y (2010) Comparison of the effects of different salts on aerobic ammonia oxidizers for treating ammonium-rich organic wastewater by free and sodium alginate immobilized biomass system. Chemosphere 81:669–673. https://doi.org/10.1016/j.chemosphere.2010.03.025 PubMed DOI

Yang BR, Yuen SC, Fan GY, Cong WH, Leung SW, Lee SM (2018) Identification of certain Panax species to be potential substitutes for Panax notoginseng in hemostatic treatments. Pharmacol Res 34:10–52. https://doi.org/10.1016/j.phrs.2018.05.005

Ye L, Zhou C, Zhou W, Zhou P, Chen D, Liu X, Shi X, Feng M (2010) Biotransformation of ginsenoside Rb1 to ginsenoside Rd by highly substrate-tolerant Paecilomyces bainier 229–7. Bioresource Technol 101:7872–7876. https://doi.org/10.1016/j.biortech.2010.04.102 DOI

Zhang J, Han X, Li X, Luo Y, Zhao H, Yang M, Ni B, Liao Z (2012) Core-shell hybrid liposomal vesicles loaded with Panax notoginsenoside: preparation, characterization and protective effects on global cerebral ischemia/reperfusion injury and acute myocardial ischemia in rats. Int J Nanomed 7:4299–4310. https://doi.org/10.2147/IJN.S32385 DOI

Zhang N, An X, Lang P, Wang F, Xie Y (2019) Ginsenoside Rd contributes the attenuation of cardiac hypertrophy in vivo and in vitro. Biomed Pharmacother 109:1016–1023. https://doi.org/10.1016/j.biopha.2018.10.081 PubMed DOI

Zhao J, Fu Y, Luo M, Zu Y, Wang W, Zhao C, Gu C (2012) Endophytic fungi from pigeon pea [Cajanus cajan (L.) Millsp.] produce antioxidant cajaninstilbene acid. J Agr Food Chem 60:4314–4319. https://doi.org/10.1021/jf205097y DOI

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