Skip to main content

Advertisement

SpringerLink
Log in

Phylogenetic Analysis and Biological Evaluation of Marine Endophytic Fungi Derived from Red Sea Sponge Hyrtios erectus

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Forty-four endophytic fungal isolates obtained from marine sponge, Hyrtios erectus, were evaluated and screened for their hydrolase activities. Most of the isolates were found to be prolific producers of hydrolytic enzymes. Only 11 isolates exhibited maximum cellular contents of lipids, rhamnolipids, and protein in the fungal isolates under the isolation numbers MERVA5, MERVA22, MERVA25, MERVA29, MERVA32, MERVA34, MERV36, MERVA39, MERVA42, MERVA43, and MERVA44. These isolate extracts exhibit the highest reducing activities against carbohydrate-metabolizing enzymes including α-amylase, α-glucosidase, β-glucosidase, β-glucuronidase, and tyrosinase. Consequently, based on morphological and cultural criteria, as well as sequence information and phylogenetic analysis, these isolates could be identified and designated as Penicillium brevicombactum MERVA5, Arthrinium arundinis MERVA22, Diaporthe rudis MERVA25, Aspergillus versicolor MERVA29, Auxarthron alboluteum MERVA32, Dothiorella sarmentorum MERVA34, Lophiostoma sp. MERVA36, Fusarium oxysporum MERVA39, Penicillium chrysogenum MERVA42, Penicillium polonicum MERVA43, and Trichoderma harzianum MERVA44. The endophytic fungal species, D. rudis MERVA25, P. polonicum MERVA43, Lophiostoma sp. MERVA36, A. alboluteum MERVA32, T. harzianum MERVA44, F. oxysporum MERVA39, A. versicolor MERVA29, and P. chrysogenum MERVA42 extracts, showed significant hepatitis C virus (HCV) inhibition. Moreover, D. sarmentorum MERVA34, P. polonicum MERVA43, and T. harzianum MERVA44 extracts have the highest antitumor activity against human hepatocellular carcinoma cells (HepG2).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Chen, L., Zhang, Q. Y., Jia, M., Ming, Q. L., Yue, W., Rahman, K., Qin, L. P., & Han, T. (2016). Endophytic fungi with antitumor activities: their occurrence and anticancer compounds. Critical Reviews in Microbiology, 42(3), 454–473. https://doi.org/10.3109/1040841X.2014.959892.

    CAS  PubMed  Google Scholar 

  2. Xu, L., Meng, W., Cao, C., Wang, J., Shan, W., & Wang, Q. (2015). Antibacterial and antifungal compounds from marine fungi. Marine Drugs, 13(6), 3479–3513. https://doi.org/10.3390/md13063479.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Moghadamtousi, S. Z., Nikzad, S., Abdul Kadir, H., Abubakar, S., & Zandi, K. (2015). Potential antiviral agents from marine fungi: an overview. Marine Drugs, 13(7), 4520–4538. https://doi.org/10.3390/md13074520.

    Article  CAS  PubMed  Google Scholar 

  4. Anitha, T. S., & Palanivelu, P. (2013). Purification and characterization of an extracellular keratinolytic protease from a new isolate of Aspergillus parasiticus. Protein Expression and Purification, 88(2), 214–220. https://doi.org/10.1016/j.pep.2013.01.007.

    Article  CAS  PubMed  Google Scholar 

  5. El-Bondkly, A. M. A., & El-Gendy, M. M. A. A. (2012). Cellulase production from agricultural residues by recombinant fusant strain of a fungal endophyte of the marine sponge Latrunculia corticata for production of ethanol. Antonie Van Leeuwenhoek, 101(2), 331–346. https://doi.org/10.1007/s10482-011-9639-1.

    Article  CAS  PubMed  Google Scholar 

  6. El-Gendy, M. M. A. A., Al-Zahrani, S. H., & El-Bondkly, A. M. A. (2017). Construction of potent recombinant strain through intergeneric protoplast fusion in endophytic fungi for anticancerous enzymes production using rice straw. Applied Biochemistry and Biotechnology, 183(1), 30–50. https://doi.org/10.1007/s12010-017-2429-0.

    Article  CAS  PubMed  Google Scholar 

  7. El-Bondkly, A. M. A. (2012). Molecular identification using ITS sequences and genome shuffling to improve 2-deoxyglucose tolerance and xylanase activity of marine-derived fungus, Aspergillus sp. NRCF5. Applied Biochemistry and Biotechnology, 167(8), 2160–2173. https://doi.org/10.1007/s12010-012-9763-z.

    Article  CAS  PubMed  Google Scholar 

  8. Parizadeh, H., & Garampalli, R. H. (2016). Evaluation of some lichen extracts for β-glucosidase inhibitory as a possible source of herbal anti-diabetic drugs. American Journal of Biochemistry, 6(2), 46–50.

    CAS  Google Scholar 

  9. Pandey, S., Sree, A., Dash, S. S., Sethi, D. P., & Chowdhury, L. (2016). Isolation, identification and screening of marine fungi for potential tyrosinase inhibitor, antibacterial and antioxidant for future cosmeceuticals. International Journal of Bioengineering and Life Sciences, 3(12), 1159.

    Google Scholar 

  10. Bugni, T. S., & Ireland, C. M. (2004). Marine-derived fungi: a chemically and biologically diverse group of microorganisms. Natural Product Reports, 21(1), 143–163. https://doi.org/10.1039/b301926h.

    Article  CAS  PubMed  Google Scholar 

  11. Barnett, H. L., & Hunter, B. B. (1998). Illustrated genera of imperfect fungi. Published by Amer Phytopathological Society, From Murray Media. North Miami Beach, FL.

  12. Kohlmeyer, J., & Kohlmeyer, E. (1979). Marine mycology. The higher fungi. San-Francisco: Academic 690 p.

    Google Scholar 

  13. Kohlmeyer, J., & Volkmann-Kohlmeyer, B. (1991). Illustrated key to the filamentous marine fungi. Botanica Marina, 34(1), 1–61. https://doi.org/10.1515/botm.1991.34.1.1.

    Article  Google Scholar 

  14. Gilman, J. C., & Joseph, C. (1998). A manual of soil fungi. Daya Publishing House, pp. 392.

  15. El-Bondkly, A. M. A. (2006). Gene transfer between different Trichoderma species and Aspergillus niger through intergeneric protoplast fusion to convert ground rice straw to citric acid and cellulases. Applied Biochemistry and Biotechnology, 135(2), 117–132. https://doi.org/10.1385/ABAB:135:2:117.

    Article  CAS  PubMed  Google Scholar 

  16. White, T. J., Bruns, T., Lee, S., & Taylor, J. W. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, & T. J. White (Eds.), PCR protocols: a guide to methods and applications (pp. 315–322). New York: Academic.

    Google Scholar 

  17. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using likelihood, distance, and parsimony methods. Molecular Biology and Evolution, 28(10), 2731–2739. https://doi.org/10.1093/molbev/msr121.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Lowry, O. H., Rosebrough, N. J., Farr, A. L., & Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. The Journal of Biological Chemistry, 193(1), 265–275.

    Article  CAS  PubMed  Google Scholar 

  19. Somashekar, D., Venkateshwaran, G., Srividya, C., Krishnanand, Sambaiah, K., & Lokesh, B. R. (2001). Efficacy of extraction methods for lipid and fatty acid composition from fungal cultures. World Journal of Microbiology and Biotechnology, 17(3), 317–320. https://doi.org/10.1023/A:1016792311744.

    Article  CAS  Google Scholar 

  20. Abdel-Mawgoud, A. M., Lépine, F., & Déziel, E. (2010). Rhamnolipids: diversity of structures, microbial origins and roles. Applied Microbiology and Biotechnology, 86(5), 1323–1336. https://doi.org/10.1007/s00253-010-2498-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. El-Gendy, M. M. A. A., Nageh, Abo Dahab, F., Taher, Taha, M., Fareed, & Hassan, S. M. (2015). Production, purification and characterization of L-asparaginase from marine endophytic Aspergillus sp. ALAA-2000 under submerged and solid state fermentation. Journal of Microbial & Biochemical Technology, 7, 165–172.

    Google Scholar 

  22. El-Gendy, M. M. A. A., Taha, T. M., Abo-Dahab, N. F., & Hassan, F. S. M. (2016). Process optimization of L-glutaminase production; a tumour inhibitor from marine endophytic isolate Aspergillus sp. ALAA-2000. Journal of Microbial & Biochemical Technology, 8, 382–389.

    Article  Google Scholar 

  23. Ruttimann, C., Schwember, E., Salas, L., Cullen, D., & Vicuiia, R. (1992). Ligninolytic enzymes of the white-rot basidiomycetes Phlebia brevispora and Ceriporiopsis subvermispora. Biotechnology and Applied Biochemistry, 16, 64–76.

    CAS  Google Scholar 

  24. El-Bondkly, A. M. A., & Keera, A. A. (2007). UV- and EMS-induced mutations affecting synthesis of alkaloids and lipase in Penicillium roquefortii. Arab Journal of Biotechnology, 10(2), 241–248.

    Google Scholar 

  25. Collins, R. A., Ng, T. B., Fong, W. P., Wan, C. C., & Yeung, H. W. (1997). Inhibition of glycohydrolase enzymes by aqueous extracts of Chinese medicinal herbs in a microplate format. Biochemistry and Molecular Biology International, 42(6), 1163–1169.

    CAS  PubMed  Google Scholar 

  26. Suthindhiran, K. R., Jayasri, M. A., & Kannabiran, K. (2009). α-Glucosidase and α-amylase inhibitory activity of Micromonospora sp. VITSDK3 (EU551238). International Journal of Integrative Biology, 6(3), 115–120.

    CAS  Google Scholar 

  27. Verma, N., Behera, B. C., & Sharma, B. O. (2012). Glucosidase inhibitory and radical scavenging properties of lichen metabolites salazinic acid, sekikaic acid and usnic acid. Hacettepe Journal of Biology and Chemistry, 40(1), 7–21.

    Google Scholar 

  28. Vasantha, K. Y., Murugesh, C. S., & Sattur, A. P. (2014). A tyrosinase inhibitor from Aspergillus niger. Journal of Food Science and Technology, 51(10), 2877–2880. https://doi.org/10.1007/s13197-014-1395-6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Cappuccino, J., & Sherman, N. (1999). Microbiology: a laboratory manual (4th ed.pp. 1–477). Harlow: The Benjamin/Cummings Publishing Company, Inc..

    Google Scholar 

  30. Lavermicocca, P., Valerio, F., & Visconti, A. (2003). Antifungal activity of phenyllactic acid against molds isolated from bakery products. Applied Environment Microbiology, 69(1), 634–640. https://doi.org/10.1128/AEM.69.1.634-640.2003.

    Article  CAS  Google Scholar 

  31. El-Gendy, M. M. A. A., El-Bondkly, A. M. A., & Yahya, S. M. M. (2014). Production and evaluation of antimycotic and antihepatitis C virus potential of fusant MERV6270 derived from mangrove endophytic fungi using novel substrates of agroindustrial wastes. Applied Biochemistry and Biotechnology, 174(8), 2674–2701. https://doi.org/10.1007/s12010-014-1218-2.

    Article  CAS  PubMed  Google Scholar 

  32. Mosmam, T. (1983). Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. Journal of Immunological Methods, 65(1-2), 55–63. https://doi.org/10.1016/0022-1759(83)90303-4.

    Article  Google Scholar 

  33. Ruiza, N., Duboisb, N., Wielgosz-Collina, G., du Ponta, T. R., Bergéb, J. P., Pouchusa, Y. F., & Barnathan, G. (2007). Lipid content and fatty acid composition of a marine-derived Trichoderma longibrachiatum strain cultured by agar surface and submerged fermentations. Process Biochemistry, 42(4), 676–680. https://doi.org/10.1016/j.procbio.2006.09.017.

    Article  CAS  Google Scholar 

  34. Kiran, G. S., Thajuddin, N., Hema, T. A., Idhayadhulla, A., Kumar, R. S., & Selvin, J. (2010). Optimization and characterization of rhamnolipid biosurfactant from sponge associated marine fungi Aspergillus sp. MSF1. Desalination and Water Treatment, 24(1-3), 257–265. https://doi.org/10.5004/dwt.2010.1569.

    Article  CAS  Google Scholar 

  35. de Souza, P. M., Bittencourt, M. L. A., Caprara, C. C., de Freitas, M., de Almeida, R. P. C., Silveira, D., Fonseca, Y. M., Filho, E. X. F., Junior, A. P., & Magalhães, P. O. (2015). A biotechnology perspective of fungal proteases, review. Brazilian Journal of Microbiology, 46(2), 337–346. https://doi.org/10.1590/S1517-838246220140359.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Ellilä, S., Fonseca, L., Uchima, C., Cota, J., Goldman, G. H., Saloheimo, M., Sacon, V., & Siika-aho, M. (2017). Development of a low-cost cellulase production process using Trichoderma reesei for Brazilian biorefineries. Biotechnology for Biofuels, 10(30), 1–17.

    Google Scholar 

  37. Barriuso, J., & Martínez, M. J. (2017). Evolutionary history of versatile-lipases from Agaricales through reconstruction of ancestral structures. BMC Genomics, 18(1), 12. https://doi.org/10.1186/s12864-016-3419-2.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Pundir, R. K., Mishra, V. K., Rana, S., & Lakhani, M. (2016). Screening of laccase producing fungi from soil samples—An in vitro study. Electronic Journal of Biology, 12(3), 254–257.

    Google Scholar 

  39. Abeysekera, W. K. S. M., Chandrasekara, A., & Liyanage, P. K. (2007). Amylase and glucosidase enzyme inhibitory activity of ginger (Zingiber officinale Roscoe) an in vitro study. Tropical Agricultural Research, 19, 128–135.

    Google Scholar 

  40. Pavithra, N., Sathish, L., Babu, N., Venkatarathanamma, V., Pushpalatha, H., Reddy, G. B., & Ananda, K. (2014). Evaluation of α-amylase, α-glucosidase and aldose reductase inhibitors in ethyl acetate extracts of endophytic fungi isolated from antidiabetic medicinal plants. International Journal of Pharmaceutical Sciences and Research, 5(12), 5334–5341.

    Google Scholar 

  41. Haroon, M. H., Premaratne, S. R., Choudhry, I. M., & Dharmaratne, H. R. W. (2013). Natural product research a new β-glucuronidase inhibiting butyrolactone from the marine endophytic fungus Aspergillus. Formerly Natural Product Letters, 27(12), 1060–1066. https://doi.org/10.1080/14786419.2012.708659.

    Article  CAS  Google Scholar 

  42. Abd El-Hady, F. K., Abdel-Aziz, M. S., Souleman, A. M. A., Abd El-Shahid, Z. A., & Shaker, K. H. (2016). Potentiality of improving or suppressing tyrosinase inhibitory activity by media composition for the marine fungus Aspergillus unguis SPMD-EGY. Der Pharma Chemica, 8(19), 458–465.

    CAS  Google Scholar 

  43. Abd El-Hady, F. K., Abdel-Aziz, M. S., Souleman, A. M. A., Shaker, K. H., & Abd El-Shahid, Z. A. (2014). Tyrosinase, acetylcholinesterase inhibitory potential, antioxidant and antimicrobial activities of sponge derived fungi with correlation to their GC/MS analysis. International Journal of Pharmaceutical Sciences Review and Research, 26(2), 338–345.

    CAS  Google Scholar 

  44. Wang, G., Li, Q., & Zhu, P. (2008). Phylogenetic diversity of culturable fungi associated with the Hawaiian sponges Suberites zeteki and Gelliodes fibrosa. Antonie Van Leeuwenhoek, 93(1-2), 163–174. https://doi.org/10.1007/s10482-007-9190-2.

    Article  PubMed  Google Scholar 

  45. Wiese, J., Ohlendorf, B., Blümel, M., Schmaljohann, R., & Imhoff, J. F. (2011). Phylogenetic identification of fungi isolated from the marine sponge Tethya aurantium and identification of their secondary metabolites. Marine Drugs, 9(12), 561–585. https://doi.org/10.3390/md9040561.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Abian, O., Vega, S., Sancho, J., & Velazquez-Campoy, A. (2013). Allosteric inhibitors of the NS3 protease from the hepatitis C virus. PLoS One, 8(7), 1–10.

    Article  CAS  Google Scholar 

  47. Hawas, U. W., Al-Farawati, R., Abou El-Kassem, L. T., & Turki, A. J. (2016). Different culture metabolites of the Red Sea fungus Fusarium equiseti optimize the inhibition of hepatitis C virus NS3/4A protease (HCV PR). Marine Drugs, 14(10), 190. https://doi.org/10.3390/md14100190.

    Article  PubMed Central  CAS  Google Scholar 

  48. Bladt, T. T., Frisvad, J. C., Knudsen, P. B., & Larsen, T. O. (2013). Anticancer and antifungal compounds from Aspergillus, Penicillium and other filamentous fungi. Molecules, 18(9), 11338–11376. https://doi.org/10.3390/molecules180911338.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Faculty of Science, University of Jeddah, Jeddah, 80203, Saudi Arabia

    Mervat Morsy Abbas Ahmed El-Gendy

  2. Chemistry of Natural and Microbial Products Department, National Research Centre, Dokki, Giza, 12622, Egypt

    Mervat Morsy Abbas Ahmed El-Gendy

  3. Hormones Department, Medical Research Division, National Research Centre, Dokki, Giza, 12622, Egypt

    Shaymaa M. M. Yahya

  4. Phytochemistry Department, National Research Centre, Dokki, Giza, 12622, Egypt

    Ahmed R. Hamed & Maha M. Soltan

  5. Biology Unit, Central Laboratory for Pharmaceutical and Drug Industries Research Division, National Research Centre, Dokki, Giza, 12622, Egypt

    Ahmed R. Hamed & Maha M. Soltan

  6. Genetics and Cytology Department, National Research Centre, Dokki, Giza, 12622, Egypt

    Ahmed Mohamed Ahmed El-Bondkly

Authors
  1. Mervat Morsy Abbas Ahmed El-Gendy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shaymaa M. M. Yahya
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ahmed R. Hamed
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maha M. Soltan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ahmed Mohamed Ahmed El-Bondkly
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

El-Gendy MMAA, Yahya SMM, Hamed AR, Soltan MM, and El-Bondkly AMA designed the study, performed the experiments, managed the literature searches and data analysis, and wrote the manuscript. All the authors read and approved the final manuscript.

Corresponding author

Correspondence to Mervat Morsy Abbas Ahmed El-Gendy.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

El-Gendy, M.M.A.A., Yahya, S.M.M., Hamed, A.R. et al. Phylogenetic Analysis and Biological Evaluation of Marine Endophytic Fungi Derived from Red Sea Sponge Hyrtios erectus. Appl Biochem Biotechnol 185, 755–777 (2018). https://doi.org/10.1007/s12010-017-2679-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-017-2679-x

Keywords

Search

Navigation