Abstract
A biologically potent exopolysaccharide (EPS), Pestalopine was produced by Pestalotiopsis chamaeropsis CEL6, an endophytic fungal isolate of Chloranthus elatior Sw. Pestalopine is composed of glucose, arabinose, fucose, rhamnose, and galactose in a molar ratio of nearly 10:1:2:2:4 having an Mw ∼ 3.29 × 105 Da. Pestalopine exhibited a radical scavenging effect and significantly increased antioxidant parameters (malondialdehyde, superoxide dismutase, glutathione peroxidase, reduced glutathione oxidized glutathione) in peritoneal macrophage cells in a concentration-dependent manner, with a maximum effect at 500 mg mL−1. Pestalopine is hepatoprotective in nature and improves the liver function profiles—total bilirubin, direct bilirubin, hepatic enzymes: alkaline phosphatase, gamma-glutamyl transferase, aspartate aminotransferase, alanine transaminase of liver fibrosis induced (through thioacetamide) male Wistar rats in comparison to control. Pestalopine-fed rats are reported to have higher counts of beneficial Lactobacillus sp. Present findings suggest that Pestalopine, a novel compound may have promise as a non-toxic exogenous antioxidant with hepatoprotective and probiotic efficacies.
Similar content being viewed by others
Data availability
The original contributions presented in this study are included in the article/Supplementary Material.
References
Banerjee D, Jana M, Mahapatra S (2009) Production of exopolysaccharide by endophytic Stemphylium sp. Micol Aplicada Int 21(2):57–62
Bannister JV, Bannister WH, Rotilio G (1987) Aspects of the structure, function, and applications of superoxide dismutase. CRC Crit Rev Biochem 22:111–180
Barrera G, Pizzimenti S, Dianzani MU (2008) Lipid peroxidation: control of cell proliferation cell differentiation and cell death. Mol Aspects Med 29:1–8
Blois MS (1958) Antioxidant determinations by the use of a stable free radical. Nature 181:1199–1200
Chen C, Xin K, Liu H, Cheng J, Shen X, Wang Y, Zhang L (2017) Pantoea alhagi, a novel endophytic bacterium with ability to improve growth and drought tolerance in wheat. Sci Rep 7(1):1–14
Choi D, Maeng J, Ding J, Cha W (2007) Exopolysaccharide production and mycelial growth in an air-lift bioreactor using Fomitopsis pinicola. J Microbiol Biotechnol 17(8):1369
Craft BD, Kerrihard AL, Amarowicz R,Pegg RB (2012). Comprehensive reviews in food science and food safety. 11 148 173
Deng Z, Zhang J, Li J, Fan Y, Cao S, Huang R et al (2007) Effect of polysaccharides of cassia seeds on the intestinal microflora of piglets. Asia Pac J Clin Nutr 16:143–147
Ding M, Potter JJ, Liu XP, Torbenson MS, Mezey E (2010) Selenium supplementation decreases hepatic fibrosis in mice after chronic carbon tetrachloride administration. Biol Trace Elem Res 133:83–97
Dubois M, Gilles KA, Hamilton JK, Rebers PAT, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28(3):350–356
Elmastas, Mahfuz, I. Gulcin, L. Ozturk, and Isa Gokce. Investigation of antioxidant properties of spearmint (Mentha spicata L) (2005).
Guarner F, Malagelada JR (2003) Gut flora in health and disease. Lancet 361:512–519
Gülcin İ (2006) Antioxidant and antiradical activities of L-carnitine. Life Sci 78(8):803–811
Gülçin İ, Huyut Z, Elmastaş M, Aboul-Enein HY (2010) Radical scavenging and antioxidant activity of tannic acid. Arab J Chem 3(1):43–53
Halliwell B (1992) Reactive oxygen species and the central nervous system. J Neurochem 59(1609):1623
Hettiarachchy NS, Glenn KC, Gnanasambandam R, Johnson MG (1996) Natural antioxidant extract from fenugreek (Trigonella foenumgraecum) for ground beef patties. J Food Sci 61(516):519
Hwang HJ, Kim SW, Xu CP, Choi JW, Yun JW (2003) Production and molecular characteristics of four groups of exopolysaccharides from submerged culture of Phellinus gilvus. J Appl Microbiol 94:708–719
Joulak I, Finore I, Nicolaus B, Leone L, Moriello AS, Attia H, Poli A, Azabou S (2019) Evaluation of the production of exopolysaccharides by newly isolated Halomonas strains from Tunisian hypersaline environments. Int J Biol Macromol 138:658–666
Khatua S, Acharya K (2017) Alkaline extractive crude polysaccharide from Russula senecis possesses antioxidant potential and stimulates innate immunity response. J Pharm Pharmacol 69(12):1817–1828. https://doi.org/10.1111/jphp.12813
Khatua S, Acharya K (2022) Antioxidation and immune-stimulatory actions of cold alkali extracted polysaccharide fraction from Macrocybe lobayensis, a wild edible mushroom. Biotech 12(10):247
Kim SW, Chun Ping Xu, Hwang HJ, Choi JW, Kim CW, Yun JW (2003) Production and characterization of exopolysaccharides from an enthomopathogenic fungus Cordyceps militaris NG3.". Biotechnol Progress 19:428–435
Kim HO, Lim JM, Joo JH, Kim SW, Hwang HJ, Choi JW, Yun JW (2005) Optimization of submerged culture condition for the production of mycelial biomass and exopolysaccharides by Agrocybe cylindracea. Biores Technol 96(10):1175–1182
Lee WY, Park Y, Ahn JK, Ka KH, Park SY (2007) Factors influencing the production of endopolysaccharide and exopolysaccharide from Ganoderma applanatum. Enzyme Microb Technol 40:249–254
Li D, Friedman SL (1999) Liver fibrogenesis and the role of hepatic stellate cells: new insights and prospects for therapy. J Gastroenterol Hepatol 14:618–633
Liang TJ, Yuan JH, Tan YR, Ren WH, Han GQ, Zhang J, Wang LC, Qin CY (2009) Effect of ursodeoxycholic acid on TGFbetal/Smadsignaling pathway in rat hepatic stellate cells. Chin Med J 122:1209–1213
Lidbeck A, Allinger UG, Orrhage KM, Ottova L, Brismar B, Gustafsson JA et al (1991) Impact of Lactobacillus acidophilus supplements on the faecal microflora and soluble faecal bile acids in colon cancer patients. Microb Ecol Health Dis 4:81–88
Mahapatra S, Banerjee D (2012) Structural elucidation and bioactivity of a novel exopolysaccharide from endophytic Fusarium solani SD5. Carbohyd Polym 90(1):683–689
Mahapatra S, Banerjee D (2013a) Evaluation of in vitro antioxidant potency of exopolysaccharide from endophytic Fusarium solani SD5. Int J Biol Macromol 53:62–66
Mahapatra S, Banerjee D (2013b) Fungal exopolysaccharide: production, composition and applications. Microbiol Insights 6:0957
Mahapatra S, Banerjee D (2016) Production and structural elucidation of exopolysaccharide from endophytic Pestalotiopsis sp. BC55. Int J Biol Macromol 82:182–191
Mahapatra SK, Chakraborty SP, Das S, Roy S (2009) Methanol extract of Ocimum gratissimum protects murine peritoneal macrophages from nicotine toxicity by decreasing free radical generation, lipid and protein damage and enhances antioxidant protection. Oxidative Med Cell Longevity 2(4):222–230
Maity P, Nandi AK, Pattanayak M, Manna DK, Sen IK, Chakraborty I, Bhanja SK, Sahoo AK, Gupta N, Islam SS (2020) Structural characterization of a heteroglycan from an edible mushroom Termitomyces heimii. Int J Biol Macromol 151:305–311
Muzzarelli RAA, Boudrant J, Meyer D, Manno N, DeMarchis M, Paoletti MG (2012) Current views on fungal chitin/chitosan, human chitinases, food preservation, glucans, pectins and inulin atribute to Henri Braconnot precursor of the carbohydrate polymers science on the chitin bicentennial. Carbohyd Polym 87(2):995–1012
Nehad EA, El-Shamy AR (2010) Physiological studies on the production of exopolysaccharide by fungi. Agric Biol J N Am 1:1303–1308
Pietrangelo A, Gualdi R, Casalgrandi G, Montosi G, Ventura E (2007) Molecular and cellular aspects of iron induced hepatic cirrhosis in rodents. J Clin Invest 95:1824–1831
Prieto P, Pineda M, Aguilar M (1999) Spectrophotometric quantitation of antioxidant capacity through the formation of phosphomolybdenum complex: specific application to the determination of vitamin E. Anal Biochem 269(2):337–344
Roukas T, Biliaderis CG (1995) Evaluation of carob pod as a substrate for pullulan production by Aureobasidium pullulans. Appl Biochem Biotechnol 55:27–44
Ruch RJ, Cheng S-J, Klaunig JE (1989) Prevention of cytotoxicity and inhibition of intercellular communication by antioxidant catechins isolated from Chinese green tea. Carcinogenesis 10(6):1003–1008
Sajna, Kuttuvan Valappil, Swati Sharma, and Ashok Kumar Nadda. (2021). Microbial exopolysaccharides an introduction. Microbial Exopol Novel Significant Biomater: 1–18.
Santra, Hiran Kanti, and Debdulal Banerjee. (2021) Microbial exopolysaccharides: structure and therapeutic properties microbial polymers. Appl Ecol Persp: 375–420.
Santra HK, Banerjee D (2022a) Bioactivity study and metabolic profiling of Colletotrichum alatae LCS1 an endophyte of club moss Lycopodium Clavatum L. PLoS ONE 17(4):0267302
Santra HK, Banerjee D (2022b) Production optimization, characterization and drought stress resistance by β-glucan rich heteropolysaccharide from an endophytic fungi Colletotrichum alatae LCS1 isolated from clubmoss (Lycopodium clavatum). Front. Fungal Biol 2:65
Saxena S, Strobel GA (2021) Marvellous Muscodor spp update on their biology and applications. Microb Ecol 82(1):5–20
Seki E, De Minicis S, Gwak GY, Kluwe J, Inokuchi S, Bursill CA et al (2009) CCR1 and CCR5 promote hepatic fibrosis in mice. J Clin Inves 119:1858–1870
Singha K, Hor PK, Soren JP, Mondal J, Mondal KC, Pati BR, Das PK, Mohapatra. (2021) Exploration of bioactive prospects of a polysaccharide fraction from Termitomyces heimii against colorectal cancer and broad spectrum bacteria. Bioactive Carbohydrates Dietary Fibre 25:100255
Sun L, Yang Y, Wang R, Li S, Qiu Y, Lei P, Gao J, Hong Xu, Zhang F, Lv Y (2020) Effects of exopolysaccharide derived from Pantoea alhagi NX-11 on drought resistance of rice and its efficient fermentation preparation. Int J Biol Macromol 162:946–955
Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38:3022–3027
Tiwari P, Bae H (2022) Endophytic fungi: key insights, emerging prospects, and challenges in natural product drug discovery. Microorganisms 10(2):360
Wen J, Okyere SK, Wang S, Wang J, Xie L, Ran Y, Yanchun H (2022) Endophytic fungi: an effective alternative source of plant-derived bioactive compounds for pharmacological studies. J Fungi 8(2):205
White TJ, Thomas SJWT, Lee B, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols Guide Methods Appl 18(1):315–322
Wonglumsom W, Vishnubhatla A, Fung DYC (2000) Effect of volume of liquid enrichment medium containing oxyrase@ on growth of Campylobacter jejuni. J Rapid Methods Autom Microbiol 8:111–139
Yang H, He G (2008) Influence of nutritional conditions on exopolysaccharide production by submerged cultivation of the medicinal fungus Shiraia bambusicola. World J Microbiol Biotechnol 24:2903–2907
Ye RG, Lu ZY (2006) Internal medicine, 6th edn. People’s Medical Publishing House, Beijing
Funding
The authors have not disclosed any funding.
Author information
Authors and Affiliations
Contributions
HKS performed the work and wrote the manuscript. DB supervised the planning of the project and critically reviewed the manuscript.
Corresponding author
Ethics declarations
Conflict of interests
The authors declare no conflict of interests.
Additional information
Communicated by Yusuf Akhter.
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
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Santra, H.K., Banerjee, D. Broad spectrum bioactivity of a novel β-glucan rich heteropolysaccharide, Pestalopine isolated from endophytic fungi Pestalotiopsis chamaeropsis CEL6. Arch Microbiol 205, 284 (2023). https://doi.org/10.1007/s00203-023-03620-x
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00203-023-03620-x