Abstract
Endophytic fungi inhabiting niche environments are novel biocatalyst resources that need to be exploited urgently. In this study, 63 endophytic fungi isolated from Dongxiang wild rice (Oryza rufipogon Griff.) were tested to assess their potentials to transform glycyrrhizin (GL) into glycyrrhetinic acid monoglucuronide (GAMG) or glycyrrhetinic acid (GA), of which 12 strains were shown to have β-d-glucuronidase activity. Based on morphological characteristics and rDNA ITS sequence analysis, the strains S59, L138, L55 and R57 with high GL molar conversion rates (55%, 45%, 65% and 89%) were further identified as Microsphaeropsis arundinis S59, Penicillium rubens L138, Aspergillus flavus L55 and Eupenicillium javanicum R57, respectively. These four strains with four different types of GL conversion processes were identified, i.e., (1) GL → GAMG in M. arundinis S59, (2) GL → GAMG and GA in A. flavus L55, (3) GL → GA in P. rubens L138, and (4) GL → GAMG → GA in E. javanicum R57, in which the bioconversion type (4) is reported for the first time. The study not only provided abundant and diverse β-d-glucuronidase resources that can be used for GL bioconversion, especially for GAMG biosynthesis from endophytic fungi, but also expanded our knowledge of potential roles of endophytes as new biocatalysts in biotransformation.
Similar content being viewed by others
References
Akao T, Kobashi K (1987) Glycyrrhizin β-d-glucuronidase of Eubacterium sp. from human intestinal flora. Chem Pharm Bull 35:705–710. https://www.jstage.jst.go.jp/article/cpb1958/35/2/35_2_705/_article
Amin HA, El-Menoufy HA, El-Mehalawy AA et al (2010) Microbial production of glycyrrhetic acid 3-O-mono-β-d-glucuronide from glycyrrhizin by Aspergillus terreus. Malays J Microbiol 6:209–216. https://doi.org/10.21161/mjm.21509
Baltina L, Tasi YT, Huang SH et al (2019) Glycyrrhizic acid derivatives as Dengue virus inhibitors. Bioorg Med Chem Lett 29:126645. https://doi.org/10.1016/j.bmcl.2019.126645
Batiha ES, Beshbishy AM, Daim MA (2020) Traditional uses, bioactive chemical constituents, and pharmacological and toxicological activities of the miracle medicinal herb; Glycyrrhiza glabra L. (Fabaceae family). Biomolecules 10:352. https://doi.org/10.3390/biom10030352
Chen JY, Kaleem I, He DW et al (2012) Efficient production of glycyrrhetic acid 3-O-mono-β-d-glucuronide by whole-cell biocatalysis in an ionic liquid/buffer biphasic system. Process Biochem 47:908–913. https://doi.org/10.1016/j.procbio.2011.10.024
Chen K, Yang R, Shen F, Zhu H (2020) Advances in pharmacological activities and mechanisms of glycyrrhizic acid. Curr Med Chem 27:6219. https://doi.org/10.2174/0929867325666191011115407
Cheng L, Zhang H, Cui H et al (2021) Efficient enzyme-catalyzed production of diosgenin: inspired by the biotransformation mechanisms of steroid saponins in Talaromyces stollii CLY-6. Green Chem 23:5896–5910. https://doi.org/10.1039/D0GC04152A
Choudhary M, Gupta S, Dhar MK, Kaul S (2021) Endophytic fungi-mediated biocatalysis and biotransformations paving the way toward green chemistry. Front Bioeng Biotechnol 9:664705. https://doi.org/10.3389/fbioe.2021.664705
Corrêa RCG, Rhoden SA, Mota TR et al (2014) Endophytic fungi: expanding the arsenal of industrial enzyme producers. J Ind Microbiol Biotechnol 41:1467–1478. https://doi.org/10.1007/s10295-014-1496-2
Du LQ, Gao BL, Liang JF et al (2020) Microparticle-enhanced Chaetomium globosum DX-THS3 β-d-glucuronidase production by controlled fungal morphology in submerged fermentation. 3 Biotech 10:100. https://doi.org/10.1007/s13205-020-2068-y
Dubey A, Malla A, Kumar A et al (2020) Plants endophytes: unveiling hidden agenda for bioprospecting toward sustainable agriculture. Crit Rev Biotechnol 40:1210–1231. https://doi.org/10.1080/07388551.2020.1808584
Espinosa K, Chávez MA, Duarte-Escalante E et al (2021) Phylogenetic identification, diversity, and richness of Aspergillus from homes in Havana. Cuba Microorg. 9:115. https://doi.org/10.3390/microorganisms9010115
Feng SJ, Li C, Xu XL et al (2006) Screening strains for directed biosynthesis of β-D-mono-glucuronide-glycyrrhizin and kinetics of enzyme production. J Mole Catal B-Enzym 43:63–67. https://doi.org/10.1016/j.molcatb.2006.06.016
Feng X, Liu X, Jia J et al (2019) Enhancing the thermostability of β-glucuronidase from T. pinophilum enables the biotransformation of glycyrrhizin at elevated temperature. Chem Eng Sci 204:91–98. https://doi.org/10.1016/j.ces.2019.04.020
Fu Y (2019) Biotransformation of ginsenoside Rb1 to Gyp-XVII and minor ginsenoside Rg3 by endophytic bacterium Flavobacterium sp. GE 32 isolated from panax ginseng. Lett Appl Microbiol 68:134–141. https://doi.org/10.1111/lam.13090
Guo LC, Zhao W (2017) Screening strains for biosynthesis of glycyrrhetinic acid monoglucuronide and the optimization of fermentation process. Chin J Food Sci Technol 38:88–94. https://kns.cnki.net/kcms/detail/detail.aspx?dbcode=CJFD&dbname=CJFDLAST2017&filename=SPKJ201716018&v=GkoJtOdFv7f4oqeZKzHY%25mmd2BobX9KS2rVA%25mmd2Fj7sJPHNez6yeO8mpCOnpNbXsldMIYR8s
Guo L, Katiyo W, Lu L et al (2018) Glycyrrhetic acid 3-O-mono-β-d-glucuronide (GAMG): An innovative high-potency sweetener with improved biological activities. Compr Rev Food Sci Food Saf 17:905–919. https://doi.org/10.1111/1541-4337.12353
Kim DH, Lee SW, Han MJ (1999) Biotransformation of glycyrrhizin to 18Beta-glycyrrhetinic acid-3-O-beta-D-glucuronide by Streptococcus LJ-22, a human intestinal bacterium. Biol Pharm Bull 22:320–322. https://doi.org/10.1248/bpb.22.320
Kim SW, Jin Y, Shin JH et al (2012) Glycyrrhizic acid affords robust neuroprotection in the postischemic brain via anti-inflammatory effect by inhibiting hmgb1 phosphorylation and secretion. Neurobiol Dis 46:147–156. https://doi.org/10.1016/j.nbd.2011.12.056
Kong HZ (2007) Chinese fungi. Penicillium and related sexual types, vol 35. Science Press, Beijing (in Chinese)
Kuramoto T, Ito Y, Oda M et al (1994) Microbial production of glycyrrhetic acid 3-O-mono-β-d-glucuronide from glycyrrhizin by Cryptococcus magnus Mg-27. Biosci Biotechnol Biochem 58:455–458. https://doi.org/10.1271/bbb.58.455
Luo J, Liu X, Li E et al (2013) Arundinols A–C and arundinones A and B from the plant endophytic fungus Microsphaeropsis arundinis. J Nat Prod 76:107–112. https://doi.org/10.1021/np300806a
Pastorino G, Cornara L, Soares S et al (2018) Liquorice (Glycyrrhiza glabra): a phytochemical and pharmacological review. Phytother Res 32:2323–2339. https://doi.org/10.1002/ptr.6178
Paula NMD, Silva K, Brugnari T et al (2021) Biotechnological potential of fungi from a mangrove ecosystem: Enzymes, salt tolerance and decolorization of a real textile effluent. Microbiol Res 254:126899. https://doi.org/10.1016/j.micres.2021.126899
Qi Z (1997) Chinese fungi, vol 5. Aspergillus and related sexual types. Science Press, Beijing (in Chinese)
Qi F, Dai DZ, Liu YL et al (2011) Effects of low-shear modeled microgravity on the characterization of recombinant β-d-glucuronidases expressed in Picha pastors. Appl Biochem Biotechnol 163:162–172. https://doi.org/10.1007/s12010-010-9025-x
Qin S, Zhao L, Yang Y et al (2017) A new isochroman derivative from the endophytic Microsphaeropsisarundinis. Chem Nat Compd 53:877–879. https://doi.org/10.1007/s10600-017-2145-6
Shi X, Yu L, Zhang Y et al (2020) Glycyrrhetinic acid alleviates hepatic inflammation injury in viral hepatitis disease via a hmgb1-tlr4 signaling pathway. Int Immunopharmacol 84:106578. https://doi.org/10.1016/j.intimp.2020.106578
Strobel G, Yang XS, Sears J et al (1996) Taxol from Pestalotiopsis microspora, an endophytic fungus of Taxus wallachiana. Microbiology 142:435–440
Suryanarayanan TS, Thirunavukkarasu N, Govindarajulu MB et al (2012) Fungal endophytes: an untapped source of biocatalysts. Fungal Divers 54:19–30. https://doi.org/10.1007/s13225-012-0168-7
Torres-Mendoza D, Ortega HE, Cubilla-Rios L (2020) Patents on endophytic fungi related to secondary metabolites and biotransformation applications. J Fungi 6:58. https://doi.org/10.3390/jof6020058
Wang C, Guo X, Wang X et al (2013) Isolation and characterization of three fungi with the potential of transforming glycyrrhizin. World J Microbiol Biotechnol 29:781–788. https://doi.org/10.1007/s11274-012-1233-9
Wang Y, Gao BL, Li XX et al (2015) Phylogenetic diversity of culturable endophytic fungi in Dongxiang wild rice (Oryza rufipogon Griff), detection of polyketide synthase gene and their antagonistic activity analysis. Fungal Biol 119:1032–1045. https://doi.org/10.1016/j.funbio.2015.07.009
Wang H, Ge X, Qu H et al (2020) Glycyrrhizic acid inhibits proliferation of gastric cancer cells by inducing cell cycle arrest and apoptosis. Cancer Manag Res 12:2853–2861. https://doi.org/10.2147/CMAR.S244481
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and application. Academic Press Inc., San Diego, pp 315–322
Wu W, Davis RW, Tran-Gyamfi MB et al (2017) Characterization of four endophytic fungi as potential consolidated bioprocessing hosts for conversion of lignocellulose into advanced biofuels. Appl Microbiol Biotechnol 101:2603–2618. https://doi.org/10.1007/s00253-017-8091-1
Wu S, Wang W, Dou J et al (2020) Research progress on the protective effects of licorice-derived 18β-glycyrrhetinic acid against liver injury. Acta Pharmacol Sin 1:18–26. https://doi.org/10.1038/s41401-020-0383-9
Xiang L, Qi F, Dai DZ et al (2010) Simulated microgravity affects growth of Escherichia coli and recombinant β-d-glucuronidase production. Appl Biochem Biotechnol 162:654–661. https://doi.org/10.1007/s12010-009-8836-0
Xie J, Agrama HA, Kong D et al (2010) Genetic diversity associated with conservation of endangered Dongxiang wild rice (Oryza rufipogon). Genet Resour Crop Evol 57:597–609. https://doi.org/10.1007/s10722-009-9498-z
Xiu LX, Guo WY, Zhan PG et al (2010) Structural determination of two new triterpenoids biotransformed from glycyrrhetinic acid by Mucor polymorphosporus. Magn Reson Chem 48:164–167. https://doi.org/10.1002/mrc.2552
Xu Y, Feng X, Jia J et al (2018) A novel β-glucuronidase from Talaromyces pinophilus Li-93 precisely hydrolyzes glycyrrhizin into glycyrrhetinic acid 3-O-mono-β-d-glucuronide. Appl Environ Microbiol 84:00755-18. https://aem.asm.org/content/84/19/e00755-18.long
Zhang D, Yang Y, Castlebury LA, Cerniglia CE (1996) A method for the large scale isolation of high transformation efficiency fungal genomic DNA. FEMS Microbiol Lett 145:261–265. https://doi.org/10.1016/S0378-1097(96)00421-1
Zhang Q, Gao BL, Xiao YW et al (2020) Purification and characterization of a novel β-glucuronidase precisely converts glycyrrhizin to glycyrrhetinic acid 3-O-mono-β-d-glucuronide from plant endophytic Chaetomiumglobosum DX-THS3. Int J Biol Macromol 159:782–792. https://doi.org/10.1016/j.ijbiomac.2020.05.047
Zou S, Liu G, Kaleem I et al (2013) Purification and characterization of a highly selective glycyrrhizin-hydrolyzing β-glucuronidase from penicillium purpurogenum Li-3. Process Biochem 48:358–363. https://doi.org/10.1016/j.procbio.2012.12.008
Acknowledgements
This study was supported by the Natural Science Foundation of China (31260137), by the Foundation of Jiangxi Educational Committee (GJJ180636, GJJ190593), by Funds of Jiangxi Science and Technology Normal University (2017XJZD004), by the Natural Science Foundation of Jiangxi Province of China (20181BAB215044).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Xiao, Y., Zhang, Z., Liang, W. et al. Endophytic fungi from Dongxiang wild rice (Oryza rufipogon Griff.) show diverse catalytic potential for converting glycyrrhizin. 3 Biotech 12, 79 (2022). https://doi.org/10.1007/s13205-022-03138-x
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-022-03138-x