Abstract
Iridoids are widely found from species of Bignoniaceae family and exhibit several biological activities, such as anti-inflammatory, antimicrobial, antioxidant, and antitumor. Specioside is an iridoid found from Tabebuia species, mainly in Tabebuia aurea. Thus, here fungus-mediated biotransformation of the iridoid specioside was investigated by seven fungi. The fungus-mediated biotransformation reactions resulted in a total of nineteen different analogs by fungus Aspergillus niger, Aspergillus flavus, Aspergillus japonicus, Aspergillus terreus, Aspergillus niveus, Penicillium crustosum, and Thermoascus aurantiacus. Non-glycosylated specioside was the main metabolite observed. The other analogs were yielded from ester hydrolysis, hydroxylation, methylation, and hydrogenation reactions. The non-glycosylated specioside and coumaric acid were yielded by all fungi-mediated biotransformation. Thus, fungus applied in this study showed the ability to perform hydroxylation and glycosidic, as well as ester hydrolysis reactions from glycosylated iridoid.
Key points
• The biotransformation of specioside by seven fungi yielded nineteen analogs.
• The non-glycosylated specioside was the main analog obtained.
• Ester hydrolysis, hydroxylation, methylation, and hydrogenation reactions were observe
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The strains are deposited in the library URM (University Recife Mycology) of Federal University of Pernambuco (UFPE) and MMBF (Micoteca Mario Barreto Figueiredo). The data can be found at http://www3.ufpe.br/micoteca/nova/fazerBusca.php and http://www.biologico.sp.gov.br/page/colecoes/fungos-fitopatogenicos.All MS/MS data obtained in this study is summarized in Table 1, and the spectra are illustrated in the Supplementary Information.
References
Agarwala R, Barrett T, Beck J, Benson DA, Bollin C, Bolton E, Bourexis D, Brister JR, Bryant S, Canese K, Cavanaugh M, Charowhas C, Clark K, Dondoshansky I, Feolo M, Fitzpatrick L, Funk K, Geer WL, Gorelenkov V, Graeff A, Hlavina W, Holmes B, Johnson M, Kattman B, Khotomlianski V, Kimchi A, Kimelman M, Kimura M, Kitts P, Klimke W, Kotliarov A, Krasnov S, Kuznetsov A, Landrum MJ, Landsman D, Lathrop S, Lee JM, Leubsdorf C, Lu Z, Madden TL, Marchler-Bauer A, Malheiro A, Meric P, Karsch-Mizrachi I, Mnev A, Murphy T, Orris R, Ostell J, O’Sullivan C, Palanigobu V, Panchenko A, Phan L, Pierov B, Pruitt K, Rodarmer K, Sayers EW, Schneider V, Schoch CL, Schuler GD, Sherry ST, Siyan K, Soboleva A, Soussov V, Starchenko G, Tatusova TA, Thibaud-Nissen F, Todorov K, Trawick BW, Vakatov P, Ward M, Yaschenko M, Zasypkin M, Zbiczet K (2018) Database resources of the (NCBI) National Center for Biotechnology Information. Nucleic Acids Res 46(D1):D8–D13. https://doi.org/10.1093/nar/gkx1095
Arni SA, Drake AF, Borghi MD, Converti A (2010) Study of aromatic compounds derived from sugarcane bagasse. Part I: Effect of pH. Chem Eng Technol 33:895–901. https://doi.org/10.1002/ceat.200900557
Ashtana J, Yadav AK, Pant A, Pandey S, Gupta MM, Pandey R (2015) Specioside ameliorates oxidative stress and promotes longevity in Caenorhabditis elegans. Comp Biochem Physiol C 169:25–34. https://doi.org/10.1016/j.cbpc.2015.01.002
Bharti N, Singh S, Naqvi F, Azam A (2006) Isolation and in vitro antiamoebic activity of iridiods isolated from Kigelia pinnata. ARKIVOC 2006:69–76. https://doi.org/10.3998/ark.5550190.0007.a09
Caderby E, Baumberger E, Hoareau W, Fargues C, Decloux M, Maillard MN (2013) Sugar cane stillage: a potential source of natural antioxidants. J Agric Food Chem 61:11494–11501. https://doi.org/10.1021/jf4039474
Cao J, Yu H, Wu Y, Wang X (2019) Occurrence and biological activities of phenylpropionyl iridoids. Mini-Rev Med Chem 19:292–309. https://doi.org/10.2174/1389557518666181026091449
Chandra P, Enespa S, R, Arora PK, (2020) Microbial lipases and their industrial applications: a comprehensive review. Microb Cell Fact 19:169. https://doi.org/10.1186/s12934-020-01428-8
Elusyian CA, Ani NC, Adewunmi CO, Olugbade TA (2011) Distribution of iridoidglucosides and anti-oxidant compounds in Spathodea campanulata parts. Afr J Tradit Complement Altern Med 8:27–33. https://doi.org/10.4314/ajtcam.v8i1.60491
Flores AC, Gómez J, Torres ISE, Bejarano BV (2020) Microorganisms as biocatalysts and enzyme sources. Microorganisms. https://doi.org/10.5772/intechopen.90338
Gao J, Wang J, Cui J, Wang N, Bai Y, Yuan Y, Zhou Y (2014) Purification and characterization of two novel β-glucosidases from Penicillium oxalicum and their application in bioactive ginsenoside production. Biocatal Biotransfor 32:199–207. https://doi.org/10.3109/10242422.2014.934365
Garces HG, Hrycyk MF, Giacobino J, Machado GC, Arantes TD, Theodoro RC, Bosco SMG, Bagagli E (2016) Molecular identification and phylogenetical analysis of dermatophyte fungi from Latin America. Mycoses 59:787–797. https://doi.org/10.1111/myc.12532
Guo X, Chena X, Li L, Shena Z, Wanga X, Zhenga P, Duana F, Maa Y, Bi K (2008) LC–MS determination and pharmacokinetic study of six phenolic components in rat plasma after taking traditional Chinese medicinal-preparation: Guanxinning lyophilized powder for injection. J Chromatogr B 873:51–58. https://doi.org/10.1016/j.jchromb.2008.07.039
Guy PA, Renouf M, Barron D, Cavin C, Dionisi F, Kochhar S, Rezzi S, Williamson G, Steiling H (2009) Quantitative analysis of plasma caffeic and ferulic acid equivalents by liquid chromatography tandem mass spectrometry. J Chromatogr B 877:3965–3974. https://doi.org/10.1016/j.jchromb.2009.10.006
Harris J, Stocker H (1998) Handbook of mathematics and computational science. Springer, New York
Hegazy ME, Mohamed TA, ElShamy AI, Mohamed AEHH, Mahalel UA, Reda EH, Shaheen AM, Tawfik WA, Shahat AA, Shams KA, Abdel-Azim NS, Hammouda MF (2015) Microbial biotransformation as a tool for drug development based on natural products from mevalonic acid pathway: a review. J Adv Res 6:17–33. https://doi.org/10.1016/j.jare.2014.11.009
Izumi T, Piskula MK, Osawa S, Obata A, Tobe K, Saito M, Kataoka S, Kubota Y, Kikuchi M (2000) Soy isoflavone aglycones are absorbed faster and in higher amounts than their glucosides in humans. J Nutr 130:1695–1699. https://doi.org/10.1093/jn/130.7.1695
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz DC, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199
Kimura MA (1980) Simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120. https://doi.org/10.1007/BF01731581
Kostrzewa-Suslow E, Janeczko T (2014) Microbial transformations of 5-hydroxy- and 5-methoxyflavone in Aspergillus niger and Penicillium chermesinum cultures. J Microbiol Biotechnol Food Sci 3:448–452
Kudou S, Fleury Y, Welti D, Magnolato D, Uchida T, Kitamura K, Okubo K (1991) Malonyl isoflavone glycosides in soybean seeds (Glycine max Merrill). Agric Biol Chem 55:2227–2233. https://doi.org/10.1080/00021369.1991.10870966
Larkin M, Blackshields G, Brown N, Chenna R, Mcgettigan P, Mcwilliam H, Valentin F, Wallace I, Wilm A, Lopez R, Thompson J, Gibson T, Higgins D (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. https://doi.org/10.1093/bioinformatics/btm404
Liu J-H, Yu B-Y (2010) Biotransformation of bioactive natural products for pharmaceutical lead compounds. Curr Org Chem 14:1400–1406. https://doi.org/10.2174/138527210791616786
Li XN, Sun J, Shi H, Yu LL, Ridge CD, Mazzola EP, Okunji C, Iwu MM, Michel TK, Chen P (2017) Profiling hydroxycinnamic acid glycosides, iridoid glycosides, and phenylethanoid glycosides in baobab fruit pulp (Adansonia digitata). Food Res Int 99:755–761. https://doi.org/10.1016/j.foodres.2017.06.025
Malange KF, Santos GG, Kato NN, Parada CA, Toffoli-Kadri MC, Carollo CA, Silva DB, Portugal LC, Alves FM, Rita PHS, Rondon ES (2019) Tabebuia aurea decreases hyperalgesia and neuronal injury induced by snake venom. J Ethnopharmacol 233:131–140. https://doi.org/10.1016/j.jep.2018.12.037
Mamma D, Hatzinikolaou DG, Christakopoulos P (2004) Biochemical and catalytic properties of two intracellular beta-glucosidases from the fungus Penicillium decumbens active on flavonoid glucosides. J Mol Catal B Enzym 27:183–190. https://doi.org/10.1016/j.molcatb.2003.11.011
Mohammed WA, Alia AQ, Errayes AO (2020) Green chemistry: principles, applications, and disadvantages. Chem Methodol 4:408–423. https://doi.org/10.33945/SAMI/CHEMM.2020.4.4
Németh K, Plumb GW, Berrin JG, Juge N, Jacob R, Naim HY, Williamson G, Swallow DM, Kroon PA (2003) Deglycosylation by small intestinal epithelial cell beta-glucosidases is a critical step in the absorption and metabolism of dietary flavonoid glycosides in humans. Eur J Nutr 42:29–42. https://doi.org/10.1007/s00394-003-0397-3
Nocchi SR, Kato NN, Almeida JM, Ferreira AMT, Toffoli-Kadri MC, Meirelles LEF, Damke GMZF, Consolaro MEL, Rigo GV, Macedo AJ, Tasca T, Reis SV, Alves FM, Carollo CA, Silva DB (2020) Pharmacological properties of specioside from the stem bark of Tabebuia aurea. Rev Bras Farmacogn 30:118–122. https://doi.org/10.1007/s43450-020-00017-5
Owen RW, Haubner R, Mier W, Giacosa A, Hulld WE, Spiegelhalder B, Bartsch H (2003) Isolation, structure elucidation and antioxidant potential of the major phenolic and flavonoid compounds in brined olive drupes. Food Chem Toxicol 41:703–717. https://doi.org/10.1016/S0278-6915(03)00011-5
Parshikov IA, Sutherland B (2015) Biotransformation of steroids and flavonoids by cultures of Aspergillus niger. Appl Biochem Biotechnol 176:903–923. https://doi.org/10.1007/s12010-015-1619-x
Peart PC, Reynolds WF, Reese PB (2013) The facile bioconversion of testosterone by alginate-immobilised filamentous fungi. J Mol Catal B Enzym 95:70–81. https://doi.org/10.1016/j.molcatb.2013.05.025
Perkins C, Siddique S, Puri M, Demain AL (2015) Biotechnological applications of microbial bioconversions. Crit Rev Biotechnol 36:1050–1065. https://doi.org/10.3109/07388551.2015.1083943
Reis FP, Senna Bonfa IM, Cavalcante RB, Okoba D, de Souza Vasconcelos SB, Candeloro L, de Oliveira Filiu WF, Duenhas Monreal AC, da Silva VJ, Santa Rita PH, Carollo CA, Toffoli-Kadri MC (2014) Tabebuia aurea decreases inflammatory, myotoxic and hemorrhagic activities induced by the venom of Bothrops neuwiedi. J Ethnopharmacol 158:352–357. https://doi.org/10.1016/j.jep.2014.10.045
Schaub J, Zielesny A, Steinbeck C, Sorokina M (2020) Too sweet: cheminformatics for deglycosylation in natural products. J Cheminform 12:67. https://doi.org/10.1186/s13321-020-00467-y
Schröder P, Bauer JO, Strohmann C, Kumar K, Waldmann H (2016) Synthesis of an iridoid-inspired compound collection and discovery of autophagy inhibitors. J Org Chem 81:10242–10255. https://doi.org/10.1021/acs.joc.6b01185
Schuerg T, Gabriel R, Baecker N, Baker SE, Singer SW (2017) Thermoascus aurantiacus is an intriguing host for the industrial production of cellulases. Curr Biotechnol 6:89–97. https://doi.org/10.2174/2211550105666160520123504
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
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 applications. Academic Press, San Diego, pp 315–322
Yan FY, Xia W, Zhang XX, Chen S, Nie XZ, Qian LC (2016) Characterization of β-glucosidase from Aspergillus terreus and its application in the hydrolysis of soybean isoflavones. J Zhejiang Univ Sci 17:455–464. https://doi.org/10.1631/jzus.B1500317
Ying YM, Shan WG, Zhan ZJ (2014) Biotransformation of huperzine A by a fungal endophyte of Huperzia serrata furnished sesquiterpenoid-alkaloid hybrids. J Nat Prod 77:2054–2059. https://doi.org/10.1021/np500412f
Yousuf M, Mammadova K, Baghirova S, Rahimova R (2019) Biotransformation: a one pot method of novel pharmacological importance. Nov Appro Drug Des Dev 4:1–3. https://doi.org/10.19080/NAPDD.2019.04.555645
Zhan Y, Liu H, Wu Y, Wei P, Chen Z, Williamson JS (2015) Biotransformation of artemisinin by Aspergillus niger. Appl Microbiol Biotechnol 99:3443–3446. https://doi.org/10.1007/s00253-015-6464-x
Zhong K, Zhao S-Y, Jönsson LJ, Hong F (2008) Enzymatic conversion of epigallocatechin gallate to epigallocatechin with an inducible hydrolase from Aspergillus niger. Biocatal Biotransformation 26:306–312. https://doi.org/10.1080/10242420802090487
Zohri AN, Mostafa E (2000) Biotransformation of steroid by some thermophilic and thermotolerant fungi grown on yeast-starch and molasses media. Bull Fac Sci Assiut Univ 29:425–431
Acknowledgements
The authors thank INAU (Instituto Nacional de Áreas Úmidas), CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico), FUNDECT (Fundação de Apoio ao Desenvolvimento do Ensino, Ciência e Tecnologia do Estado de Mato Grosso do Sul), and CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior).
Funding
DBS is supported by productive fellowship from CNPq (grant number 313047/2020–0).
Author information
Authors and Affiliations
Contributions
NSC, JCPM, and DBS conceived and designed research. ESA supplied the strains of the fungi. NNK and CAC collected the plant and isolated the specioside iridoid. NSC, NNK, and LBS conducted experiments. RR analyzed the ITS sequence and identified the microorganisms. NSC, CAC, ESA, and DBS analyzed the chemical data. NSC and DBS wrote the manuscript. All authors read and approved the manuscript.
Corresponding author
Ethics declarations
Ethics approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Conflict of Interest
All authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Cassemiro, N.S., Sanches, L.B., Kato, N.N. et al. New derivatives of the iridoid specioside from fungal biotransformation. Appl Microbiol Biotechnol 105, 7731–7741 (2021). https://doi.org/10.1007/s00253-021-11504-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-021-11504-7