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Characterization of bioactive compounds produced by endophytic fungi isolated from Gynura procumbens (Sambung Nyawa)

Abstract

This research evaluates the bioactivity of twelve endophytic fungi successfully isolated and characterised from Gynura procumbens. The fungal extracts displayed inhibitory activity against Staphylococcus aureus, Pseudomonas aeruginosa, Methicillin-resistant Staphylococcus aureus (MRSA), Escherichia coli and Salmonella typhi with the MIC and MBC of 5000 µg/mL. High antioxidant activity using DPPH free radical scavenging assay with inhibition of 86.6% and IC50 value of 104.25 ± 18.51 µg/mL were exhibited by ethyl acetate extract of Macrophomina phaseolina SN6. In contrast, the highest scavenging activity percentage of methanolic extract was exhibited by Mycoleptodiscus indicus SN4 (50.0%). Besides that, the highest ferric reducing antioxidant power (FRAP) value of ethyl acetate and methanolic extract was recorded from M. phaseolina SN6 (239.9 mg Fe (II)/g) and M. indicus SN4 (44.7 mg Fe (II)/g), respectively. Total phenolic content (TPC) and total flavonoid content (TFC) of ethyl acetate and methanolic fungal extracts were determined using Folin-Ciocalteu and aluminium chloride, respectively. The highest TPC for ethyl acetate and methanolic extracts were exhibited by Colletotrichum gloeosporioides SN11 (87.0 mg GAE/g) and M. indicus SN4 (35.0 mg GAE/g), whereas the highest TFC of ethyl acetate and methanolic extracts were showed by M. phaseolina SN6 (122.8 mg QCE/g) and M. indicus SN4 (60.4 mg QCE/g), respectively. Bioactive metabolites of isoelemicin (50.8%), terpinen-4-ol (21.5%), eucalyptol (24.3%), oleic acid (19.8%) and β-pinene (10.9%) were detected. Owing to the higher content of phytochemicals represented in the ethyl acetate extract of M. phaseolina, SN6 is therefore identified to be a superior candidate in exhibiting strong antioxidant and antimicrobial properties be fit for further pharmaceutical studies.

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All data generated or analysed during this study are included in this published article.

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References

  1. Bhardwaj A, Agrawal P (2014) A review of fungal endophytes: as a store house of bioactive compound. World J Pharmacy and Pharm Sci 3(9):228–237

    Google Scholar 

  2. Venieraki A, Dimou M, Katinakis P (2017) Endophytic fungi residing in medicinal plants have the ability to produce the same or similar pharmacologically active secondary metabolites as their host. Hellenic Plant Protection J 10:51–56

    Article  Google Scholar 

  3. Chen L, Zhang QY, Jia M, Ming QL, Yue W, Rahman K, Qin LP, Han T (2016) Endophytic fungi with antitumor activities: their occurrence and anticancer compounds. Crit Rev Microbiol 42(3):454–473

    CAS  PubMed  Google Scholar 

  4. Yap LS, Lee WL, Ting ASY (2017) Endophytes from Malaysian medicinal plants as sources for discovering anticancer agents. Medicinal Plants and Fungi: Recent Advances in Research and Development, Medicinal and Aromatic Plants of the World Volume 4, Singapore: Springer Nature Singapore Pte Ltd.

  5. Bhagobaty RK, Joshi SR (2012) Enzymatic activity of fungi endophytic on five medicinal plant species of the pristine sacred forests of Meghalaya, India. Biotech Bioprocess Eng 17:33–40

    CAS  Article  Google Scholar 

  6. Kuralarasi R, Lingakumar K (2018) Isolation and antibacterial activity of endophytic fungi from Madhuca longifolia bark. J Medicinal Plants Stud 6(1):36–39

    Google Scholar 

  7. Manganyi MC, Regnier T, Tchatchouang CDK, Bezuidenhout CC, Ateba CN (2019) Antibacterial activity of endophytic fungi isolated from Sceletium tortuosum L (Kougoed). Annals of Microbiology 69(6):659–663

    CAS  Article  Google Scholar 

  8. Jia M, Chen L, Xin HL, Zheng CJ, Rahman K, Han T, Qin LP (2016) A friendly relationship between endophytic fungi and medicinal plants. Front Microbiol 7:1–14

    Article  Google Scholar 

  9. Tan X, Zhou Y, Zhou X, Xia X, Wei Y, He L, Tang H, Yu L (2018) Diversity and bioactive potential of culturable fungal endophytes of Dysosma versipellis; a rare medicinal plant endemic to China. Sci Rep 8(5929):1–9

    Google Scholar 

  10. Nongkhlaw FMW, Joshi SR (2015) Investigation on the bioactivity of culturable endophytic and epiphytic bacteria associated with ethnomedicinal plants. The Journal of Infection in Developing Countries 9(9):954–961

    CAS  PubMed  Article  Google Scholar 

  11. Tan HL, Chan KG, Pusparajah P, Lee LH, Goh BH (2016) Gynura procumbens: an overview of the biological activities. Front Pharmacol 7(52):1–14

    Google Scholar 

  12. Mou KM, Dash PR (2016) A comprehensive review on Gynura procumbens leaves. Int J Pharmacogn 3(4):167–174

    CAS  Google Scholar 

  13. Rahman AFMM, Asad MSA (2013) Chemical and biological investigations of the leaves of Gynura procumbens. Int J Biosci 3(4):36–43

    Google Scholar 

  14. Afandi A, Zulkiffli MH, Sadikun A, Ismail S (2014) Antioxidant properties of Gynura procumbens extracts and their inhibitory effects on two major human recombinant cytochrome P450s using a high throughput luminescence assay. Asian J Pharm Clin Res 7(5):36–41

    Google Scholar 

  15. Kaewseejan N, Puangpronpitag D, Nakornriab M (2012) Evaluation of phytochemical composition and antibacterial property of Gynura procumbens extract. Asian J Plant Sci 11(2):77–82

    Article  Google Scholar 

  16. Yadav R, Singh AV, Joshi S, Kumar M (2015) Antifungal and enzyme activity of endophytic fungi isolated from Ocimum sanctum and Aloe Vera. African J Microbiol Res 9(29):1783–1788

    Article  Google Scholar 

  17. Bezerra JDP, Nascimento CCF, Barbosa RN, Silva DCV, Svedese VM, Silva-Nogueira EB, Gomes BS, Paiva LM, Souza-Motta CM (2015) Endophytic fungi from medicinal plant Bauhinia forficata: diversity and biotechnological potential. Braz J Microbiol 46(1):49–57

    PubMed  PubMed Central  Article  Google Scholar 

  18. Tolulope RA, Adeyemi AI, Erute MA, Abiodun TS (2015) Isolation and screening of endophytic fungi from three plants used in traditional medicine in Nigeria for antimicrobial activity. International Journal of Green Pharmacy 9(1):58–62

    CAS  Article  Google Scholar 

  19. 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):1–9

    Google Scholar 

  20. Deepthi VC, Sumathi S, Faisal M, Elyas KK (2018) Isolation and identification of endophytic fungi with antimicrobial activities from the leaves of Elaeocarpus sphaericus (Gaertn) K Schum and Myristica fragrans Houtt. Int J Pharma Sci and Res 9(7):2783–2791

    CAS  Google Scholar 

  21. Cubero OF, Crespo A, Fatehi J, Bridge PD (1999) DNA extraction and PCR amplification method suitable for fresh, herbarium-stored, lichenized and other fungi. Plant Syst Evol 216:243–249

    CAS  Article  Google Scholar 

  22. Yenn TW, Ngim AS, Ibrahim D, Zakaria L (2014) Antimicrobial activity of Penicillium minioluteum ED24, an endophytic fungus residing in Orthosiphon stamineus Benth. World J Pharm Pharmaceutical Sci 3(3):121–132

    Google Scholar 

  23. Selvi K, Balagengatharathilagam P (2014) Isolation and screening of endophytic fungi from medicinal plants of Virudhunagar district for antimicrobial activity. Int J Sci Nature 5(1):147–155

    Google Scholar 

  24. Balouiri M, Sadiki M, Ibnsouda SK (2016) Methods for in vitro evaluating antimicrobial activity: a review. J Pharm Analysis 6:71–79

    Article  Google Scholar 

  25. Bastos EGP, Aguiar AA, Oliveira AIT, Silva JFM, Pimenta RS (2017) Antimicrobial evaluation of endophytic fungi extracts isolated from Casearia sylvestris. J Med Plants Res 11(43):683–689

    Article  Google Scholar 

  26. Rahim KK, Almey AAA, Khan AJ, Zahir SI, Suleiman MK, Aisyah MR (2010) Total phenolic content and antioxidant activity of methanolic and ethanolic extracts of aromatic plants’ leaves. Int Food Res J 17:1077–1084

    Google Scholar 

  27. Benzie IFF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Chem 239(292):70–76

    CAS  Google Scholar 

  28. Rebaya A, Belghith SI, Baghdikian B, Leddet VM, Mabrouki M, Olivier E, Cherif JK, Ayadi MT (2014) Total phenolic, total flavonoid, tannin content, and antioxidant activity of Halimium halimifolium (Cistaceae). J Appl Pharma Sci 5(1):52–57

    Google Scholar 

  29. 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 Biotech 6(210):1–14

    Google Scholar 

  30. Chaithra M, Vanitha S, Ramanathan A, Jegadeeshwari V, Rajesh V, Hegde V, Apshara E (2020) Morphological and molecular characterization of endophytic fungi associated with cocoa (Theobroma cacao L) in India. Current J Appl Sci Tech 38(6):1–8

    Article  CAS  Google Scholar 

  31. Alsohaili SA, Bani-Hasan BM (2018) Morphological and molecular identification of fungi isolated from different environmental sources in the northern eastern desert of Jordan. Jordan Journal of Biological Sciences 11(3).

  32. Jariwala M, Desai B (2018) Isolation and identification of endophytic fungi from various medicinal plants. BMR Microbiology 4(1):1–7

    Google Scholar 

  33. Chagas MBDO, Santos IPD, Silva LCND, Correia MTDS, Araújo JMD, Cavalcanti MDS, Lima VLDM (2017) Antimicrobial activity of cultivable endophytic fungi associated with Hancornia speciosa Gomes Bark. The Open Microbiol J 11:179–188

    CAS  PubMed  Article  Google Scholar 

  34. Yu J, Wu Y, He Z, Li M, Zhu K, Gao B (2018) Diversity and antifungal activity of endophytic fungi associated with Camellia oleifera. Microbiol 46(2):85–91

    Google Scholar 

  35. Sadrati N, Daoud H, Zerroug A, Dahamna S, Bouharati S (2013) Screening of antimicrobial and antioxidant secondary metabolites from endophytic fungi isolated from wheat (Triticum durum). J Plant Protection Res 53(2):128–136

    Article  Google Scholar 

  36. Liu X, Jia J, Jing X, Li G (2018) Antioxidant activities of extracts from sarcocarp of Cotoneaster multiflorus. J Chem 2018:1–7

    Google Scholar 

  37. Shekhar TC, Anju G (2014) Antioxidant activity by DPPH radical scavenging method of Ageratum conyzoides Linn leaves. American J Ethnomedicine 1(4):244–249

    Google Scholar 

  38. Sofiane I, Ratiba S, Miguel CMD, Nuria C (2018) Phytochemical composition and evaluation of the antioxidant activity of the ethanolic extract of Calendula suffruticosa subsp suffruticosa Vahl. Pharmacognosy Journal 10(1):64–70

    Google Scholar 

  39. Hameed J, Hussain SA, Yang J, Ijaz MU, Liu Q, Suleria HAR, Song Y (2017) Antioxidants potential of the filamentous fungi (Mucor circinelloides). Nutrients 9(1101):1–20

    CAS  Google Scholar 

  40. Sudha G, Vadivukkarasi S, Shree RBI, Lakshmanan P (2012) Antioxidant activity of various extracts from an edible mushroom Pleurotus eous. Food Sci Biotech 21(3):661–668

    CAS  Article  Google Scholar 

  41. Benzie IFF, Devaki M (2017) The ferric reducing/antioxidant power (FRAP) assay for non-enzymatic antioxidant capacity: concepts, procedures, limitations and applications. Measurement of Antioxidant Activity & Capacity: Recent Trends and Applications, 1st edn. John Wiley & Sons Ltd., West Sussex, UK

    Google Scholar 

  42. González-Palma I, Escalona-Buendía HB, Ponce-Alquicira E, Téllez-Téllez M, Gupta VK, Díaz-Godínez G, Soriano-Santos J (2016) Evaluation of the antioxidant activity of aqueous and methanol extracts of Pleurotus ostreatus in different growth stages. Front Microbiol 7(1099):1–9

    Google Scholar 

  43. Ahmed M, Hussain M, Dhar MK, Kaul S (2015) Comparative analysis of phenolics, flavonoids, and antioxidant and antibacterial potential of methanolic, hexanic, and aqueous extracts from Adiantum caudatum leaves. Antioxidants 4:394–409

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  44. Zain SNDM, Omar WAW (2018) Antioxidant activity, total phenolic content and total flavonoid content of water and methanol extracts of Phyllanthus species from Malaysia. Pharmacognosy Journal 10(4):677–681

    CAS  Article  Google Scholar 

  45. Al-Rubaye AF, Hameed IH, Kadhim MJ (2017) A review: uses of gas chromatography-mass spectrometry (GC-MS) for analysis of bioactive natural compounds of some plants. Int J Toxicological and Pharmacological Res 9(1):81–85

    Article  Google Scholar 

  46. Pan F, Su TJ, Cai SM, Wu W (2017) Fungal endophyte derived Fritillaria unibracteata var wabuensis diversity antioxidant capacities in vitro and relations to phenolic flavonoid or saponin compounds. Scientific Reports 7(42008):1–14

    Google Scholar 

  47. Chowdary K, Kaushik N (2015) Fungal endophyte diversity and bioactivity in the Indian medicinal plant Ocimum sanctum Linn. PLoS ONE 10(11):1–25

    Google Scholar 

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Acknowledgements

The authors are thankful to Universiti Malaysia Sarawak and Tun Zaidi Research Chair (TZC), Universiti Malaysia Sarawak for providing the laboratory facilities and financial support during this research investigation.

Funding

The research project was funded under the Tun Zaidi Chair Research Grant Scheme (TZC) (F07(ZRC04)/1237/2015(01)).

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Haifa Arghnia A. Jamal, Ahmad Husaini and Ngieng Ngui Sing brought up the idea, performed the literature search and data analysis and drafted the manuscript. Hairul Azman Roslan, Azham Zulkharnain and Wahab Abideen Akinkunmi proofread and critically revised the manuscript. All authors read and approved the final manuscript.

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Correspondence to Ahmad Husaini.

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Jamal, H.A.A., Husaini, A., Sing, N.N. et al. Characterization of bioactive compounds produced by endophytic fungi isolated from Gynura procumbens (Sambung Nyawa). Braz J Microbiol (2022). https://doi.org/10.1007/s42770-022-00827-w

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  • DOI: https://doi.org/10.1007/s42770-022-00827-w

Keywords

  • Antioxidant activity
  • Antibacterial activity
  • Bioactive compounds
  • Endophytic fungi
  • Gynura procumbens
  • Macrophomina phaseolina