, Volume 71, Issue 1, pp 245–259 | Cite as

Expanding knowledge on Russula alatoreticula, a novel mushroom from tribal cuisine, with chemical and pharmaceutical relevance

  • Somanjana Khatua
  • Swarnendu Chandra
  • Krishnendu AcharyaEmail author
Original Article


Since antiquity, numerous macrofungi are being worshiped as food and natural medicine especially in Asian tribal communities. Recent investigation has correlated these medicinal properties with bioactive components including phenols and flavonoids. However, research on mushrooms is not satisfactory; as several traditionally prized members remain undiscovered or poorly explored yet. This backdrop tempted us to unveil secondary metabolites empowered with therapeutics from an ethnic delicacy, Russula alatoreticula that was justified as a novel macrofungus in our previous publication. Accordingly, methanol extract was prepared from dried basidiocarps that was found to be enriched with phenolic compounds (pyrogallol > cinnamic acid > p-coumaric acid) and ascorbic acid. As a result, the fraction exhibited strong antioxidant activity evident by the ability of quenching free radicals, chelating Fe2+ ion and reducing components with EC50 of 263–2382 µg/ml. Besides, effective antibacterial potential against six investigated microbes was also noticed where MIC value ranged from 99 to 2673.74 µg/ml. Furthermore, the extract revealed promising anticancer property as it induced apoptosis of Hep3B cell (IC50 358.57 µg/ml) by imparting morphological changes, interfering cell cycle, depleting MMP and alleviating ROS through Bax, Bcl2, caspases 9 and 3 intrinsic mitochondrial pathway. Overall study implied that the immense bioactive potential of R. alatoreticula could possibly be utilized as a good source of natural supplement to combat against free radicals, pathogenic bacteria and hepatocellular carcinoma as well as in food safety industry.


Antibacterial potential HPLC Hep3B liver cancer Novel species Phenolics Antioxidant activity 



Authors would like to acknowledge the facilities provided by Department of Botany (UGC-CAS Phase VI, VII), University of Calcutta and DST-FIST for instrumental support.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interests.


  1. Acharya K, Bera I, Khatua S, Rai M (2015a) Pharmacognostic standardization of Grifola frondosa: a well-studied medicinal mushroom. Pharm Lett 7(7):72–78Google Scholar
  2. Acharya K, Khatua S, Sahid S (2015b) Pharmacognostic standardization of Macrocybe crassa: an imminent medicinal mushroom. Res J Pharm Technol 8(7):860–866CrossRefGoogle Scholar
  3. Acharya K, Ghosh S, Khatua S, Mitra P (2016) Pharmacognostic standardization and antioxidant capacity of an edible mushroom Laetiporus sulphureus. J Verbrauch Lebensm 11(1):33–42. CrossRefGoogle Scholar
  4. Acharya K et al (2017a) Exploring a new edible mushroom Ramaria subalpina: chemical characterization and antioxidant activity. Pharmacogn J 9:30–34. CrossRefGoogle Scholar
  5. Acharya K, Khatua S, Ray S (2017b) Quality assessment and antioxidant study of Pleurotus djamor (Rumph. ex Fr.) Boedijn. J Appl Pharm Sci 7(6):105–110Google Scholar
  6. Alves MJ, Ferreira ICFR, Pintado M (2012) Antimicrobial activity of wild mushroom extracts against clinical isolates resistant to different antibiotics. J Appl Microbiol 113:466–475. CrossRefGoogle Scholar
  7. Alves MJ, Ferreira ICFR, Froufe HJC, Abreu RMV, Martins A, Pintado M (2013) Antimicrobial activity of phenolic compounds identified in wild mushrooms, SAR analysis and docking studies. J Appl Microbiol 115:346–357. CrossRefGoogle Scholar
  8. Barros L, Dueñas M, Ferreira IC, Baptista P, Santos-Buelga C (2009) Phenolic acids determination by HPLC-DAD-ESI/MS in sixteen different Portuguese wild mushrooms species. Food Chem Toxicol 47(6):1076–1079. CrossRefGoogle Scholar
  9. Biswal D, Pramanik NR, Chakrabarti S, Drew MGB, Acharya K, Chandra S (2017) Syntheses, crystal structures, DFT calculations, protein interaction and anticancer activities of water soluble dipicolinic acid-imidazole based oxidovanadium(IV) complexes. Dalton Trans 46:16682–16702. CrossRefGoogle Scholar
  10. Boeing JS, Barizão ÉO, Silva BC, Montanher PF, Almeida VC, Visentainer JV (2014) Evaluation of solvent effect on the extraction of phenolic compounds and antioxidant capacities from the berries: application of principal component analysis. Chem Cent J 8:48. CrossRefGoogle Scholar
  11. Chatterjee S, Chatterjee A, Chandra S, Khatua S, Saha GK, Acharya K (2016) Tricholoma giganteum ameliorates benzo[α]pyrene-induced lung cancer in mice. Int J Curr Pharm Sci Rev Res 7(5):283–290Google Scholar
  12. Dundar A et al (2015) Antioxidant, antimicrobial, cytotoxic and anticholinesterase activities of seven mushroom species with their phenolic acid composition. J Hortic 2:161. CrossRefGoogle Scholar
  13. Golbano JM, López-Aparicio P, Recio MN, Pérez-Albarsanz M (2008) Finasteride induces apoptosis via Bcl-2, Bcl-xL, Bax and caspase-3 proteins in LNCaP human prostate cancer cell line. Int J Oncol 32:919–924Google Scholar
  14. Gursoy N, Sarikurkeu C, Tepe B, Solak MH (2010) Evaluation of antioxidant activities of 3 edible mushrooms: Ramaria flava (Schaef.: Fr.) Quél., Rhizopogon roseolus (Corda) T.M. Fries., and Russula delica Fr. Food Sci Biotechnol 19(3):691–696. CrossRefGoogle Scholar
  15. Hsu S et al (2007) Crude extracts of Euchresta formosana radix induce cytotoxicity and apoptosis in human hepatocellular carcinoma cell line (Hep3B). Anticancer Res 27:2415–2426Google Scholar
  16. Ivanova TS, Krupodorova TA, Barshteyn VY, Artamonova AB, Shlyakhovenko VA (2014) Anticancer substances of mushroom origin. Exp Oncol 36(2):58–66Google Scholar
  17. Kashibhatla S, Amarante-Mendes GP, Finucane D, Brunner T, Bossy-Wetzel E, Green DR (2006) Acridine orange/ethidium bromide (AO/EB) staining to detect apoptosis. Cold Spring Harb Protoc. Google Scholar
  18. Khatua S, Paul S, Acharya K (2013) Mushroom as the potential source of new generation of antioxidant: a review. Res J Pharm Technol 6(5):496–505Google Scholar
  19. Khatua S, Dutta AK, Acharya K (2015) Russula senecis: a delicacy among the tribes of West Bengal. PeerJ 3:e810. CrossRefGoogle Scholar
  20. Khatua S, Dutta AK, Chandra S, Paloi S, Das K, Acharya K (2017a) Introducing a novel mushroom from mycophagy community with emphasis on biomedical potency. PLoS ONE 12(5):e0178050. CrossRefGoogle Scholar
  21. Khatua S, Ghosh S, Acharya K (2017b) A simplified method for microtiter based analysis of in vitro antioxidant activity. Asian J Pharm 11(2):S327–S335Google Scholar
  22. Khatua S, Ghosh S, Acharya K (2017c) Chemical composition and biological activities of methanol extract from Macrocybe lobayensis. J Appl Pharm Sci 7(10):144–151Google Scholar
  23. Kosanic M, Rankovic B, Dasic M (2013) Antioxidant and antimicrobial properties of mushrooms. Bulg J Agric Sci 19(5):1040–1046Google Scholar
  24. Kouassi KA, Kouadio EJP, Djè KM, Dué AE, Kouamé LP (2016) Edible ectomycorrhizal mushrooms Russula spp. of Côte d’Ivoire: total phenolic content, HPLC-profiles of phenolic compounds and organic acids, antioxidant activities. J Agric Chem Environ 5:73–84. Google Scholar
  25. Kozarski M et al (2015) Antioxidants of edible mushrooms. Molecules 20(10):19489–19525. CrossRefGoogle Scholar
  26. Liang C, Park AY, Guan JL (2007) In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro. Nat Protoc 2(2):329–333. CrossRefGoogle Scholar
  27. Lin J, Liu W (2006) o-Orsellinaldehyde from the submerged culture of the edible mushroom Grifola frondosa exhibits selective cytotoxic effect against Hep3B cells through apoptosis. J Agric Food Chem 54:7564–7569. CrossRefGoogle Scholar
  28. Liu K, Liu P, Liu R, Wu X (2015) Dual AO/EB staining to detect apoptosis in osteosarcoma cells compared with flow cytometry. Med Sci Monit Basic Res 21:15–20. CrossRefGoogle Scholar
  29. Munshi A, Hobbs M, Meyn RE (2005) Clonogenic cell survival assay. In: Blumenthal RD (ed) Chemosensitivity. Humana Press, New York, pp 21–28CrossRefGoogle Scholar
  30. Nedelkoska DN et al (2013) Screening of antibacterial and antifungal activities of selected Macedonian wild mushrooms. Zb Matice Srp Prir Nauk 124:333–340. CrossRefGoogle Scholar
  31. Palacios I et al (2011) Antioxidant properties of phenolic compounds occurring in edible mushrooms. Food Chem 128:674–678. CrossRefGoogle Scholar
  32. Panda MK, Tayung K (2015) Documentation and ethnomedicinal knowledge on wild edible mushrooms among ethnic tribes of northern Odisha, India. Asian J Pharm Clin Res 8(4):139–143Google Scholar
  33. Park M et al (2003) Suppression of extracellular signal-related kinase and activation of p38 MAPK are two critical events leading to caspase-8-and mitochondria-mediated cell death in phytosphingosine-treated human cancer cells. J Biol Chem 278(50):50624–50634CrossRefGoogle Scholar
  34. Pereira DM, Valentão P, Pereira JA, Andrade PB (2009) Phenolics: from chemistry to biology. Molecules 14:2202–2211. CrossRefGoogle Scholar
  35. Pontiki E, Hadjipavlou-Litina D, Litinas K, Geromichalos G (2014) Novel cinnamic acid derivatives as antioxidant and anticancer agents: design, synthesis and modeling studies. Molecules 19:9655–9674. CrossRefGoogle Scholar
  36. Preet R et al (2012) Quinacrine has anticancer activity in breast cancer cells through inhibition of topoisomerase activity. Int J Cancer 130:1660–1670. CrossRefGoogle Scholar
  37. 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 269:337–341. CrossRefGoogle Scholar
  38. Qiu GH, Xie X, Xu F, Shi X, Wang Y, Deng L (2015) Distinctive pharmacological differences between liver cancer cell lines HepG2 and Hep3B. Cytotechnol 67:1–12. CrossRefGoogle Scholar
  39. Ribble D, Goldstein NB, Norris DA, Shellman YG (2005) A simple technique for quantifying apoptosis in 96-well plates. BMC Biotechnol 5:12. CrossRefGoogle Scholar
  40. Ruan-Soto F, Ordaz-Velázquez M, García-Santiago W, Pérez-Ovando EC (2017) Traditional processing and preservation of wild edible mushrooms in Mexico. Ann Food Process Preserv 2(1):1013Google Scholar
  41. Sanchez C (2017) Reactive oxygen species and antioxidant properties from mushrooms. Synth Syst Biotechnol 2:13–22. CrossRefGoogle Scholar
  42. Shiraha H, Yamamoto K, Namba M (2013) Human hepatocyte carcinogenesis (Review). Int J Oncol 42:1133–1138. CrossRefGoogle Scholar
  43. Singdevsachan SK, Patra JK, Tayung K, Sarangi K, Thatoi H (2014) Evaluation of nutritional and nutraceutical potentials of three wild edible mushrooms from Similipal Biosphere Reserve, Odisha, India. J Verbrauch Lebensm 9:111–120. CrossRefGoogle Scholar
  44. Tiong JJL, Loo JSE, Mai C-W (2016) Global antimicrobial stewardship: a closer look at the formidable implementation challenges. Front Microbiol 7:1860. CrossRefGoogle Scholar
  45. Wang D et al (2017) A new prenylated flavonoid induces G0/G1 arrest and apoptosis through p38/JNK MAPK pathways in human hepatocellular carcinoma cells. Sci Rep 7:5736. CrossRefGoogle Scholar
  46. Wu JY et al (2011) Anti-cancer effects of protein extracts from Calvatia lilacina, Pleurotus ostreatus and Volvariella volvacea. Evid Based Complement Alternat Med. Google Scholar
  47. Xu W, Huang JJ, Cheung PCK (2012) Extract of Pleurotus pulmonarius suppresses liver cancer development and progression through inhibition of VEGF-induced PI3 K/AKT signaling pathway. PLoS ONE 7(3):e34406. CrossRefGoogle Scholar
  48. Youn M et al (2008) Chaga mushroom (Inonotus obliquus) induces G0/G1 arrest and apoptosis in human hepatoma HepG2 cells. World J Gastroenterol 14(4):511–517. CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Somanjana Khatua
    • 1
  • Swarnendu Chandra
    • 1
  • Krishnendu Acharya
    • 1
    Email author
  1. 1.Molecular and Applied Mycology and Plant Pathology Laboratory, Department of Botany, Centre of Advanced StudyUniversity of CalcuttaKolkataIndia

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