Abstract
Five filamentous fungal strains that grew in different whey-based media under submerged fermentation were investigated for antioxidant properties and phytochemicals. Phytochemical analysis revealed the presence of alkaloids, tannin, flavonoids, glycosides, phenols, saponins, and terpenes in the crude intra- and extracellular ethyl acetate extracts of different strains. All fungal extracts exhibited effective antioxidant activities in terms of TPC, TFC, DPPH, FRAP, ABTS, reducing power, and metal chelating capacity. The activities of intracellular extracts were higher than the extracellular metabolites. Fermentation media with sugar and salt supplementation significantly influenced antioxidant production. Aspergillus niger in glucose-supplemented whey medium was found to exhibit the highest antioxidant properties. The antimicrobial activity of A. niger and Penicillium expansum extracts by microtiter plate assay showed a promising result against some pathogenic bacterial strains. Chromatographic analysis of the fungal extracts revealed the presence of chlorogenic acid, trans-cinnamic acid, ferulic acid quercetin, myricetin, kaempferol, and catechin which are known for their antioxidant properties. Accumulation of nutrients in fungal biomass under constraint environment produces secondary metabolites which has demonstrated efficacy towards alleviation of several degenerative diseases. The antioxidative enriched phytochemicals present in these five different fungal strains will provide a breakthrough in the utilisation of whey as inexpensive source of substrate for the growth of these fungi. Moreover, phytochemicals could be utilized as therapeutic agents in a cost-effective and environmentally friendly manner.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and material
Not applicable.
Code availability
Not applicable.
References
Abba CC, Eze PM, Abonyi DO, Nwachukwu CU, Proksch P, Okoye FBC, Eboka CJ (2018) Phenolic compounds from endophytic Pseudofusicoccum sp. isolated from Annona muricata. Trop J Nat Prod Res 2(7):332–337. https://doi.org/10.26538/tjnpr/v2i7.6
Al-Enazi NM, Awaad AS, Al-Othman MR, Al-Anazi NK, Alqasoumi SI (2018) Isolation, identification and anti-candidal activity of filamentous fungi from Saudi Arabia soil. Saudi Pharm J 26:253–257. https://doi.org/10.1016/j.jsps.2017.12.003
Anvari M, Khayati G (2011) Submerged yeast fermentation of cheese whey for protein production and nutritional profile analysis. Adv J Food Sci Technol 3(2):122–126
AOAC (1995) Fruits and fruit products. In: Official methods of analysis of AOAC International, agricultural chemicals; contaminants; drugs. Association of Official Analytical Chemists International, Arlington
Barros L, Oliveira S, Carvalho AM, Ferreira ICFR (2010) In vitro antioxidant properties and characterization in nutrients and phytochemicals of six medicinal plants from the Portuguese folk medicine. Ind Crop Prod 32(3):572–579. https://doi.org/10.1016/j.indcrop.2010.07.012
Bhardwaj A, Sharma D, Jadon N, Agrawal PK (2015) Antimicrobial and phytochemical screening of endophytic fungi isolated from spikes of Pinus roxburghii. Arch Clin Microbiol 6(3:1):1–9
Comalada M, Ballester I, Bailon E, Sierra S, Xaus J, Ga´lvez J, et al (2006) Inhibition of pro-inflammatory markers in primary bone marrow-derived mouse macrophages by naturally occurring flavonoids, analysis of the structure-activity relationship. Biochem Pharmacol 72(8):1010–1021. https://doi.org/10.1016/j.bcp.2006.07.016
Davis JM, Murphy EA, Carmichael MD (2009) Effects of the dietary flavonoid quercetin upon performance and health. Curr Sports Med Rep 8(4):206–213. https://doi.org/10.1249/jsr.0b013e3181ae8959
Espinoza-Acosta JL, Torres-Chávez PI, Ramírez-Wong B, López-Saiz CM, Montaño-Leyva B (2016) Antioxidant, antimicrobial, and antimutagenic properties of technical lignins and their applications. BioResources 11(2):5452–5481
Ezeonu CS, Ejikeme CM (2016) Qualitative and quantitative determination of phytochemical contents of indigenous Nigerian softwoods. New J Sci 2016:1–10. https://doi.org/10.1155/2016/5601327
Garcia A, Rhoden SA, Bernardi-Wenzel J, Orlandelli RC, Azevedo JL, Pamphile JA (2012) Antimicrobial activity of crude extracts of endophytic fungi isolated from medicinal plant Sapindus saponaria L. J Appl Pharm Sci 2(10):35–40. https://doi.org/10.7324/JAPS.2012.21007
Govindappa M, Channabasava R, Kumar KRS, Pushpalatha KC (2013) Antioxidant activity and phytochemical screening of crude endophytes extracts of Tabebuia argentea Bur. & K. Sch. Am J Plant Sci 4:1641–1652. https://doi.org/10.4236/ajps.2013.48198
Gulcin I (2006) Antioxidant and antiradical activities of l-carnitine. Life Sci 78(8):803–811. https://doi.org/10.1016/j.lfs.2005.05.103
Haile M, Kang WH (2019) Antioxidant activity, total polyphenol, flavonoid and tannin contents of fermented green coffee beans with selected yeasts. Fermentation 5(29):1–13. https://doi.org/10.3390/fermentation5010029
Hajdú Z, Hohmann J, Forgo P, Martinek T, Dervarics M, Zupkó I (2007) Diterpenoids and flavonoids from the fruits of Vitex agnuscastus and antioxidant activity of the fruit extracts and their constituents. Phytother Res 21(4):391–394. https://doi.org/10.1002/ptr.2021
Hameed A, Hussain SA, Yang J, Ijaz MU, Liu Q, Suleria HAR, Song Y (2017) Antioxidants potential of the filamentous fungi (Mucor circinelloides). Nutrients 9(10):1–20. https://doi.org/10.3390/nu9101101
Hassett JD, Charniga L, Bean K, Oman ED, Cohen SM (1992) Response of Pseudomonas aeruginosa to pyocyanin: mechanisms of resistance antioxidant defenses, and demonstration of manganese, co factored superoxide dismutase. Infect Immun 60:328–336
Hedge JE, Hofreiter BT (1962) Methods in carbohydrate chemistry, 17th edn. Academic Press, New York, pp 380–394
Kates M (1972) Techniques of lipidology: isolation, analysis and identification of lipids, 2nd edn. North-Holland Pub. Co., Amsterdam
Kato M, Ochiai R, Kozuma K, Sato H, Katsuragi Y (2018) Effect of chlorogenic acid intake on cognitive function in the elderly, a pilot study. Evid Based Complementary Altern Med 2018:1–8. https://doi.org/10.1155/2018/8608497
Khiralla A, Mohamed I, Thomas J, Mignard B, Yagi RSS, Dominique LM (2015) A pilot study of antioxidant potential of endophytic fungi from some Sudanese medicinal plants. Asian Pac J Trop Med 8(9):701–704. https://doi.org/10.1016/j.apjtm.2015.07.032
Kiewlicz J, Szymusiak H, Zieliński R (2015) Synthesis, thermal stability and antioxidant activity of long-chain alkyl esters of ferulic acid. Zywn-Nauk Technol Ja 4:188–200. https://doi.org/10.15193/ZNTJ/2015/101/066
Kondepudi KK, Ambalam P, Nilsson I, Wadström T, Ljungh Å (2012) Prebiotic-non digestible oligosaccharides preference of probiotic bifidobacteria and antimicrobial activity against Clostridium difficile. Anaerobe 18(5):489–497. https://doi.org/10.1016/j.anaerobe.2012.08.005
Kong NN, Fang ST, Wang JH, Wang ZH, Xia CH (2014) Two new flavonoid glycosides from the halophyte Limonium franchetii. J Asian Nat Prod Res 16:370–375. https://doi.org/10.1080/10286020.2014.884081
Kumar RS, Sivakumar T, Sunderam RS, Gupta M, Mazumdar UK, Gomathi P, Rajeshwar Y, Saravanan S, Kumar MS, Murugesh K, Kumar KA (2005) Antioxidant and antimicrobial activities of Bauhinia racemosa L. stem bark. Braz J Med Biol 38:1015–1024. https://doi.org/10.1590/S0100-879X2005000700004
Kurhekar JV (2017) Alkaloids—the healers in medicinal plants. Int J Res Biosci 6(4):1–7
Lee J, Lee DG, Park JY, Chae S, Lee S (2015) Analysis of the trans-cinnamic acid content in Cinnamomum spp. and commercial cinnamon powder using HPLC. J Agric Food Chem 4:102–108. https://doi.org/10.4236/jacen.2015.44011
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193(1):265–275
Melappa G, Roshan A, Nithi C, Mohummed TS, Ramachandra CYL, Poojari CC (2015) Phytochemical analysis and in vitro antioxidant, antimicrobial, anti-inflammatory and cytotoxicity activities of wood rotting fungi, Trametes Ochracea. Pharmacogn J 7(2):136–146. https://doi.org/10.5530/pj.2015.2.8
Othman A, Ismail N, Ghani A, Adenan I (2007) Antioxidant capacity and phenolic content of cocoa beans. Food Chem 100(4):1523–1530. https://doi.org/10.1016/j.foodchem.2005.12.021
Palacios I, Lozano M, Moro C, D’Arrigo M, Rostagno MA, Martínez JA, García Lafuente A, Guillamón E, Villares A (2011) Antioxidant properties of phenolic compounds occurring in edible mushrooms. Food Chem 128:674–678. https://doi.org/10.1016/j.foodchem.2011.03.085
Pearson D (1981) Pearson’s chemical analysis of foods, 6th edn. J. & A. Churchill Ltd, London
Praptiwi PKD, Fathoni A, Wulansari D, Ilyas M, Agusta A (2016) Evaluation of antibacterial and antioxidant activity of extracts of endophytic fungi isolated from Indonesian Zingiberaceous plants. Nusantara Bioscie 8(2):306–311. https://doi.org/10.13057/nusbiosci/n080228
Prathyushaa AMVN, Sheelab GM, Bramhacharia PV (2018) Chemical characterization and antioxidant properties of exopolysaccharides from mangrove filamentous fungi Fusarium equiseti ANP2. Biotechnol Rep 19:1–8. https://doi.org/10.1016/j.btre.2018.e00277
Premjanu N, Jaynthy C (2014) Antioxidant activity of endophytic fungi isolated from Lannea coromendalica. Int J Res Pharm Sci 5(4):304–308
Ramesha A, Srinivas C (2014) Antimicrobial activity and phytochemical analysis of crude extracts of endophytic fungi isolated from Plumeria acuminata L. and Plumeria obtusifolia L. Eur J Exp Biol 4(2):35–43
Sadasivam S, Manickam A (1997) Biochemical methods, 2nd edn. New Age International (p) Ltd, New Delhi, pp 5–207
Saheed OK, Jamal P, Karim MdIA, Alam MdZ, Muyibi SA (2016) Utilization of fruit peels as carbon source for white rot fungi biomass production under submerged state bioconversion. J King Saud Univ Sci 28:143–151. https://doi.org/10.1016/j.jksus.2015.08.002
Satari AH, Zargar MI, Shah WA, Bansal R, Bhat MF (2018) Isolation, molecular identification. Phytochemical screening and in vitro anti-oxidant activity of endophytic fungi from Achilea millefolium Linn. J Pharmacogn Phytochem 7(4):87–92
Scharffetter-Kochanek K, Brenneisen P, Wenk J, Herrmann G, Ma W, Kuhr L (2000) Photoaging of the skin from phenotype to mechanisms. Exp Gerontol 35:307–316. https://doi.org/10.1016/s0531-5565(00)00098-x
Seal T (2016) Quantitative HPLC analysis of phenolic acids, flavonoids and ascorbic acid in four different solvent extracts of two wild edible leaves, Sonchus arvensis and Oenanthe linearis of North-Eastern region in India. J Appl Pharm Sci 6(02):157–166. https://doi.org/10.7324/JAPS.2016.60225
Shan S, Huang Z, Shah HM, Abbasi AM (2019) Evaluation of polyphenolics content and antioxidant activity in edible wild fruits. BioMed Res Int 2019:1–11. https://doi.org/10.1155/2019/1381989
Sharma D, Pramanik A, Agrawal PK (2016) Evaluation of bioactive secondary metabolites from endophytic fungus Pestalotiopsis neglecta BAB-5510 isolated from leaves of Cupressus torulosa D.Don. 3 Biotech 6(210):1–14. https://doi.org/10.1007/s13205-016-0518-3
Smith H, Doyle S, Murphy R (2015) Filamentous fungi as a source of natural antioxidants. Food Chem 185:389–397. https://doi.org/10.1016/j.foodchem.2015.03.134
Somaye F, Marzieh MN, Lale N (2008) Single cell protein (SCP) production from UF cheese whey by Kluyveromyces marxianus. 18 National congress of Food Industry, Mashhad. https://civilica.com/doc/140412
Srinivasan K, Jagadish LK, Shenbhagaraman R, Muthumary J (2010) Antioxidant activity of endophytic fungus Phyllosticta sp. isolated from Guazuma tomentosa. J Phytol 2(6):37–41
Sugiharto S, Yudiarti T, Isroli I (2016) Assay of antioxidant potential of two filamentous fungi isolated from the Indonesian fermented dried cassava. Antioxidants 5(1):1–6. https://doi.org/10.3390/antiox5010006
Sun Y, Hayakawa S, Chuamanochan M, Fujimoto M, Innun A, Izumori K (2006) Antioxidant effects of maillard reaction products obtained from ovalbumin and different d-aldohexoses. Biosci Biotechnol Biochem 70(3):598–605. https://doi.org/10.1271/bbb.70.598
Tiwari P, Kumar B, Kaur M, Kaur G, Kaur H (2011) Phytochemical screening and extraction, a review. Int Pharm Sci 1(1):98–106
Vindhya K, Sampath KKK, Neelambika HS, Leelavathi S (2014) Preliminary phytochemical screening of Gardenia latifolia Ait. and Gardenia gummifera Linn. Res J Pharm Biol Chem Sci 5(2):527–532
Yadav M, Yadav A, Yadav JP (2014) In vitro antioxidant activity and total phenolic content of endophytic fungi isolated from Eugenia jambolana Lam. Asian Pac J Trop Med 7:256–261. https://doi.org/10.1016/s1995-7645(14)60242-x
Zduńska K, Dana A, Kolodziejczak A, Rotsztejn H (2018) Antioxidant properties of ferulic acid and its possible application. Skin Pharmacol Physiol 31(6):332–336. https://doi.org/10.1159/000491755
Zhao GR, Xiang ZJ, Ye TX, Yaun JY, Guo XZ (2006) Antioxidant activities of Salvia miltiorrhiza and Panax notoginseng. Food Chem 99:767–774. https://doi.org/10.1016/j.foodchem.2005.09.002
Acknowledgements
The authors are thankful to MTCC, Chandigarh, India, for providing purified fungal culture and Indian Institute of Chemical Biology, West Bengal, India, for providing instrumental supports. The authors are thankful to Indian Institute of Engineering Science and Technology, Shibpur (formerly Bengal Engineering and Science University, Shibpur), West Bengal, India, for providing facilities for the completion of this research work.
Funding
This research work was supported by Indian Institute of Engineering Science and Technology, Shibpur (Formerly Bengal Engineering and Science University, Shibpur), West Bengal, India.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Erko Stackebrandt.
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
Chakraborty, A., Majumdar, S. & Bhowal, J. Phytochemical screening and antioxidant and antimicrobial activities of crude extracts of different filamentous fungi. Arch Microbiol 203, 6091–6108 (2021). https://doi.org/10.1007/s00203-021-02572-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00203-021-02572-4