Login Register Cart 0
Generic placeholder image

Current Bioactive Compounds

Editor-in-Chief

ISSN (Print): 1573-4072
ISSN (Online): 1875-6646

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

Chemical Profiles and Bio-Activities of Different Extracts of Terfezia Species and their Other Associated Fungi

Author(s): Mosad A. Ghareeb*, Omar M. Khalaf, Mohamed S. Abdel-Aziz, Amal M. Saad, Hassan M.F. Madkour, Ahmed K. El-Ziaty and Laila A. Refahy

Volume 16, Issue 3, 2020

Page: [308 - 319] Pages: 12

DOI: 10.2174/1573407214666181009110805

Price: $65

Abstract

Background: Desert truffles (Terfezia species) are known by their vital nutritional benefits as they are considered as rich sources of vitamins, fatty acid, minerals and proteins.

Methods: The chemical constituents of the different solvent extracts of Terfezia species were isolated and identified by column chromatography, spectroscopic and GC-MS analyses. Also, the ethyl acetate and acetone extracts of different fungal isolates, associated Terfezia, after grown on rice medium were screened for their antimicrobial, anticancer and antioxidant activities via disc agar plate, micro culture tetrazolium (MTT) and 2,2-azino-di-[3-ethylbenzo-thiazolin-sulphonate] (ABTS) assays, respectively. The promising fugal strains were molecularly identified by 18SrRNA tool.

Results: Bio-guided separation of methylene chloride, ethyl acetate and n-butanol fractions of Terfezia species led to identification of nine compounds namely; (R)-4,8-dihydroxy-7-hydroxymethyl-6- methoxy isochroman-1-one (1), 4-deoxy-4α-phorbal-12-(2,3-dimethyl)butyrate-13-isobutyrate (2), oxyphylline B (3), terfezien A (4), latilagascene D (5), amaiouine (6), senbusine acetate (7), terfezien B (8) and marinoquinoline D (9). Moreover, sixteen compounds were identified in the n-hexane extract via GC-MS analysis, accounting for 93.69% of the total detected components in the extract. While, twenty five components were detected in the methylene chloride extract, representing 43.86% from total detected components in the extract. Eight fungal strains were isolated from Terfezia sp., powder by serial dilution methods and these fungi were cultivated on solid rice medium. Also, their ethyl acetate and acetone extracts were subjected to biological studies including antimicrobial, antioxidant and anticancer activities. The three potent fungal strains (1M, 4M and 8M) were identified by the molecular technique 18SrRNA as Aspergillus niger 1M-EGY-IQ, Penicillium crustosum 4M-EGY-IQ, and Fusarium proliferatum 8M-EGY-IQ for 1M, 4M and 8M, respectively.

Conclusion: Terfezia sp., comprise a rich source of bioactive compounds and could be considered as an interesting candidate for the treatment of infectious diseases.

Keywords: Terfezia species, secondary metabolites, GC-MS, fungal isolation, molecular identification, bio-activities.

Graphical Abstract

[1]
Ghareeb, M.A.; Mohamed, T.; Saad, A.M.; Refahy, L.A.; Sobeh, M.; Wink, M. HPLC-DAD-ESI-MS/MS analysis of fruits from Firmiana simplex (L.) and evaluation of their antioxidant and antigenotoxic properties. J. Pharm. Pharmacol., 2018, 70(1), 133-142.
[http://dx.doi.org/10.1111/jphp.12843] [PMID: 29125176]
[2]
Sobeh, M.; Mahmoud, M.F.; Hasan, R.A.; Abdelfattah, M.A.O.; Sabry, O.M.; Ghareeb, M.A.; El-Shazly, A.M.; Wink, M. Tannin-rich extracts from Lannea stuhlmannii and Lannea humilis (Anacardiaceae) exhibit hepatoprotective activities in vivo via enhancement of the anti-apoptotic protein Bcl-2. Sci. Rep., 2018, 8(1), 9343.
[http://dx.doi.org/10.1038/s41598-018-27452-8] [PMID: 29921841]
[3]
Ibeyaima, A.; Rana, J.; Dwivedi, A.K.; Saini, N.; Gupta, S. Sarethy. I.P. Pseudonocardiaceae sp. TD-015 from the thar desert, India: Antimicrobial activity and identification of antimicrobial compounds. Curr. Bioact. Compd., 2018, 14, 112-118.
[http://dx.doi.org/10.2174/1573407213666170104124315]
[4]
Dahham, S.S.; Al-Rawi, S.S.; Ibrahim, A.H.; Abdul Majid, A.S.; Abdul Majid, A.M. Antioxidant, anticancer, apoptosis properties and chemical composition of black truffle Terfezia claveryi. Saudi J. Biol. Sci., 2016.
[http://dx.doi.org/10.1016/j.sjbs.2016.01.031] [PMID: 30591773]
[5]
Patel, S. Food, health and agricultural importance of truffles: A review of current scientific literature. Curr. Trends Biotechnol. Pharm., 2012, 6, 15-27.
[6]
Al-Delaimy, K.S. Protein and amino acid composition of Iraqi truffles. Can. Inst. Food Sci. Technol. J., 1977, 10, 221-222.
[http://dx.doi.org/10.1016/S0315-5463(77)73507-2]
[7]
Bokhary, H.A.; Parvez, S. Chemical composition of desert truffles Terfezia claveryi. J. Food Compos. Anal., 1993, 6, 285-293.
[http://dx.doi.org/10.1006/jfca.1993.1031]
[8]
Al-Kaisey, M.T.; Hadwan, H.A.; Abeed, H.A.; Taher, E.J.; Dhar, B.L. Proximate analysis of Iraqi truffles. Mushroom Res., 1996, 5, 105-108.
[9]
Dahham, S.S.; Tabana, Y.M.; Iqbal, M.A.; Ahamed, M.B.; Ezzat, M.O.; Majid, A.S.; Majid, A.M. The anticancer, antioxidant and antimicrobial properties of the sesquiterpene β-caryophyllene from the essential oil of Aquilaria crassna. Molecules, 2015, 20(7), 11808-11829.
[http://dx.doi.org/10.3390/molecules200711808] [PMID: 26132906]
[10]
Kıvrak, I. Analytical methods applied to assess chemical composition, nutritional value and in vitro bioactivities of Terfezia olbiensis and Terfezia claveryi from Turkey. Food Anal. Methods, 2015, 8, 1279-1293.
[http://dx.doi.org/10.1007/s12161-014-0009-2]
[11]
Hamza, A.; Zouari, N.; Zouari, S.; Jdir, H.; Zaidi, S.; Gtari, M.; Neffati, M. Nutraceutical potential, antioxidant and antibacterial activities of Terfezia boudieri Chatin, a wild edible desert truffle from Tunisia arid zone. Arab. J. Chem., 2016, 9, 383-389.
[http://dx.doi.org/10.1016/j.arabjc.2013.06.015]
[12]
Madkour, H.M.F.; Ghareeb, M.A.; Abdel-Aziz, M.S.; Khalaf, O.M.; Saad, A.M.; El-Ziaty, A.K.; Abdel-Mogib, M. Gas chromatographymass spectrometry analysis, antimicro-bial, anticancer and antioxidant activities of n-hexane and methylene chloride extracts of Senna italica. J. Appl. Pharm. Sci, 2017, 7, 023-032.
[13]
Azaz, A.D. Isolation and identification of Soil borne fungi in fields irrigated by GAP in harran plain using two isolation methods. Turk. J. Bot., 2003, 27, 83-92.
[14]
Abdel-Aziz, M.S.; Hezma, A.M. Spectroscopic and antibacterial evaluation of a nano-hydroxapatite polyvinyl alcohol biocomposite doped with microbial-synthesized nano gold for biomedical applications. Polym. Plast. Technol. Eng., 2013, 52, 1503-1509.
[http://dx.doi.org/10.1080/03602559.2013.820754]
[15]
Martin, J.P. Use of acid rose-bengal and streptomycin in the plate method for estimating soil fungi. Soil Sci., 1950, 69, 215-232.
[http://dx.doi.org/10.1097/00010694-195003000-00006]
[16]
Ghareeb, M.A.; Refahy, L.A.; Saad, A.M.; Osman, N.S.; Abdel-Aziz, M.S.; El-Shazly, M.A.; Mohamed, A.S. In vitro antimicrobial activity of five Egyptian plant species. J. Appl. Pharm. Sci.,, 2015, 5, 045-049.
[17]
El-Neekety, A.A.; Abdel-Aziz, M.S.; Hathout, A.S.; Hamed, A.A.; Sabry, B.A.; Ghareeb, M.A.; Aly, S.E.; Abdel-Wahhab, M.A. Molecular identification of newly isolated non-toxigenic fungal strains having antiaflatoxigenic, antimicrobial and antioxidant activities. Pharma Chem., 2016, 8, 121-134.
[18]
Hathout, A.; El-Nekeety, A.; Hamed, A.; Sabry, B.; Abdel-Aziz, M.; Ghareeb, M.; Aly, S. Novel Egyptian bacterial strains exhibiting antimicrobial and antiaflatoxigenic activity. J. Appl. Pharm. Sci., 2016, 6, 001-010.
[http://dx.doi.org/10.7324/JAPS.2016.601201]
[19]
Mosmann, T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods, 1983, 65(1-2), 55-63.
[http://dx.doi.org/10.1016/0022-1759(83)90303-4] [PMID: 6606682]
[20]
Denizot, F.; Lang, R. Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J. Immunol. Methods, 1986, 89(2), 271-277.
[http://dx.doi.org/10.1016/0022-1759(86)90368-6] [PMID: 3486233]
[21]
El-Gazzar, A.B.A.; Youssef, M.M.; Youssef, A.M.S.; Abu-Hashem, A.A.; Badria, F.A. Design and synthesis of azolopyrimidoquinolines, pyrimidoquinazolines as anti-oxidant, anti-inflammatory and analgesic activities. Eur. J. Med. Chem., 2009, 44(2), 609-624.
[http://dx.doi.org/10.1016/j.ejmech.2008.03.022] [PMID: 18462840]
[22]
Liu, P.; Wang, C.; Lu, Z.; Zhu, T.; Hong, K.; Zhu, W. New isochromane derivatives from the Mangrove fungus Aspergillus wtus 094102. Nat. Prod. Commun., 2015, 10(12), 2123-2126.
[http://dx.doi.org/10.1177/1934578X1501001227] [PMID: 26882680]
[23]
Ghanadian, M.; Ayatollahi, A.M.; Mesaik, M.A.; Afsharypuor, S.; Abdalla, O.M.; Kobarfard, F. New tigliane-type diterpenoids from Euphorbia aellenii Rech. f. with immunomodulatory activity. Res. Pharm. Sci., 2011, 6(1), 35-41.
[PMID: 22049276]
[24]
Kaleem, W.A.; Nisar, M.; Qayum, M.; Zia-Ul-Haq, M.; Adhikari, A.; De Feo, V. New 14-membered cyclopeptide alkaloids from Zizyphus oxyphylla Edgew. Int. J. Mol. Sci., 2012, 13(9), 11520-11529.
[http://dx.doi.org/10.3390/ijms130911520] [PMID: 23109868]
[25]
Ragasa, C.Y.; Lim, K. Secondary metabolites from Schefflera odorata Blanco. Philipp. J. Sci., 2005, 134, 63-67.
[26]
Songca, S.P.; Sebothoma, C.; Samuel, B.B.; Eloff, J.N. A biflavonoid and a carotenoid from Rhus leptodictya: Isolation, characterization and antibacterial properties. Afr. J. Biochem. Res., 2012, 6, 172-178.
[27]
Duarte, N.; Gyémánt, N.; Abreu, P.M.; Molnár, J.; Ferreira, M.J. New macrocyclic lathyrane diterpenes, from Euphorbia lagascae, as inhibitors of multidrug resistance of tumour cells. Planta Med., 2006, 72(2), 162-168.
[http://dx.doi.org/10.1055/s-2005-873196] [PMID: 16491453]
[28]
Lomchoey, N. Cyclopeptide alkaloids from some Ziziphus plants.M.Sc. Thesis, Srinakharinwirot University, 2011.
[29]
Gao, F.; Li, Y.Y.; Wang, D.; Huang, X.; Liu, Q. Diterpenoid alkaloids from the Chinese traditional herbal “Fuzi” and their cytotoxic activity. Molecules, 2012, 17(5), 5187-5194.
[http://dx.doi.org/10.3390/molecules17055187] [PMID: 22628040]
[30]
Okanya, P.W.S. Isolation and structure elucidation of secondary metabolites from the Gliding bacteria Ohtaekwangia kribbensis and Hya-langium minutum. Dissertation, Saarlandes University, 2012.
[31]
Adams, R.P. Identification of essential oil components by gas chromatography-mass spectrometry; Allured Publishing Corporation: Carol Stream, Illinois, USA, 1995.
[32]
Baron, S. Introduction to Mycology, 4th ed; University of Texas Medical Branch: Galveston, 1996.
[33]
Feofilova, E.P. The kingdom fungi: heterogeneity of physiological and biochemical properties and relationships with plants, animals, and prokaryotes. Appl. Biochem. Microbiol., 2001, 37, 124-137.
[http://dx.doi.org/10.1023/A:1002863311534]
[34]
Singhania, M.; Ravichander, P.; Swaroop, S.; Selvakumar, J.N.; Vaithilingam, M.; Chandrasekaran, S.D. Anti-bacterial and anti-oxidant property of Streptomyces laurentii VITMPS isolated from marine soil. Curr. Bioact. Compd., 2017, 13, 78-81.
[http://dx.doi.org/10.2174/1573407212666160606130704]
[35]
Meyer, V. Genetic engineering of filamentous fungi--progress, obstacles and future trends. Biotechnol. Adv., 2008, 26(2), 177-185.
[http://dx.doi.org/10.1016/j.biotechadv.2007.12.001] [PMID: 18201856]
[36]
Janakat, S.M.; Al-Fakhiri, S.M.; Sallal, A.K.J. Evaluation of antibacterial activity of aqueous and methanolic extracts of the truffle Terfezia claveryi against Pseudomonas aeruginosa. Saudi Med. J., 2005, 26(6), 952-955.
[PMID: 15983681]
[37]
Gouzi, H.; Belyagoubi, L.; Abdelali, K.N.; Khelifi, A. In vitro antibacterial activities of aqueous extracts from Algerian desert truffles (Terfezia and Tirmania, Ascomycetes) against Pseudomonas aeruginosa and Staphylococcus aureus. Int. J. Med. Mushrooms, 2011, 13(6), 553-558.
[http://dx.doi.org/10.1615/IntJMedMushr.v13.i6.70] [PMID: 22181843]
[38]
Doğan, H.H.; Aydın, S. Determination of antimicrobial effect, antioxidant activity and phenolic contents of desert truffle in Turkey. Afr. J. Tradit. Complement. Altern. Med., 2013, 10(4), 52-58.
[PMID: 24146501]
[39]
Neggaz, S.; Fortas, Z.; Chenni, M.; El Abed, D.; Ramli, B.; Kambouche, N. In vitro evaluation of antioxidant, antibacterial and antifungal activities of Terfezia claveryi Chatin. Phytotherapie, 2015, 1-7.
[40]
Saddiq, A.A.; Danial, E.N. Assessment of phenolic content, free radical-scavenging capacity and antimicrobial activities of Truffle claveryi. Wulfenia J., 2012, 19, 403-422.
[41]
Chen, Y.-F.; Jiang, W.-W.; Zhang, S.-Q.; Kan, J.-Q.; Liang, Y. Antioxidant activity and characterization of one new polysac-charide obtained from Perigord Truffle (Tuber huidongense). Evid. Based. Complement.Altern. Med., 2016. 3537193
[42]
Sugita, T.; Nishikawa, A. Fungal identification method based on DNA sequence analysis: Reassessment of the methods of the pharmaceutical society of Japan and Japanese pharmacopoeia. J. Health Sci., 2003, 46, 531-533.
[http://dx.doi.org/10.1248/jhs.49.531]
[43]
Kurtzman, C.P.; Robnett, C.J. Identification of clinically important ascomycetous yeasts based on nucleotide divergence in the 5′ end of the large-subunit (26S) ribosomal DNA gene. J. Clin. Microbiol., 1997, 35(5), 1216-1223.
[http://dx.doi.org/10.1128/JCM.35.5.1216-1223.1997] [PMID: 9114410]
[44]
Kurtzman, C.P.; Robnett, C.J. Identification and phylogeny of ascomycetous yeasts from analysis of nuclear large subunit (26S) ribosomal DNA partial sequences. Antonie van Leeuwenhoek, 1998, 73(4), 331-371.
[http://dx.doi.org/10.1023/A:1001761008817] [PMID: 9850420]
[45]
Fell, J.W.; Boekhout, T.; Fonseca, A.; Scorzetti, G.; Statzell-Tallman, A. Biodiversity and systematics of basidiomycetous yeasts as determined by large-subunit rDNA D1/D2 domain sequence analysis. Int. J. Syst. Evol. Microbiol., 2000, 50(Pt 3), 1351-1371.
[http://dx.doi.org/10.1099/00207713-50-3-1351] [PMID: 10843082]
[46]
Pitt, J.I.; Hocking, A.D. Fungi and Food Spoilage; third ed.; Springer Link: Springer e-Books. , 2009.
[http://dx.doi.org/10.1007/978-0-387-92207-2]
[47]
Al-Hindi, R.R.; Al-Najada, A.R.; Mohamed, S.A. Isolation and identification of some fruit spoilage fungi: screening of plant cell wall degrading enzymes. Afr. J. Microb., 2011, 5, 443-448.
[48]
Larone, D.H. Medically important fungi: A guide to identification, 4th ed; ASM press, 1995.
[49]
Saad, D.S.; Kinsey, G.C.; Kim, S.; Gaylarde, C.C. Extraction of genomic DNA from filamentous fungi in biofilms on water-based paint coatings. Int. Biodeterior. Biodegradation, 2004, 54, 99-103.
[http://dx.doi.org/10.1016/j.ibiod.2004.05.003]
[50]
González, J.M.; Sáiz-Jiménez, C. Application of molecular nucleic acid-based techniques for the study of microbial communities in monuments and artworks. Int. Microbiol., 2005, 8(3), 189-194.
[PMID: 16200497]
[51]
Lord, N.S.; Kaplan, C.W.; Shank, P.; Kitts, C.L.; Elrod, S.L. Assessment of fungal diversity using terminal restriction fragment (TRF) pattern analysis: comparison of 18S and ITS ribosomal regions. FEMS Microbiol. Ecol., 2002, 42(3), 327-337.
[http://dx.doi.org/10.1111/j.1574-6941.2002.tb01022.x] [PMID: 19709292]
[52]
Anderson, I.C.; Campbell, C.D.; Prosser, J.I. Potential bias of fungal 18S rDNA and internal transcribed spacer polymerase chain reaction primers for estimating fungal biodiversity in soil. Environ. Microbiol., 2003, 5(1), 36-47.
[http://dx.doi.org/10.1046/j.1462-2920.2003.00383.x] [PMID: 12542711]
[53]
Rajalakshmi, S.; Mahesh, N. Production and characterization of bioactive metabolites isolated from Aspergillus terreus in rhizosphere soil of medicinal plants. Int. J. Curr. Microbiol. Appl. Sci., 2014, 3, 784-798.
[54]
Ade, A.; Yanwirasti, M.; Djamaan, A.; Handayani, D. Cytotoxic activity screening of ethyl acetate fungal extracts derived from the marine sponge Neopetrosia chaliniformisAR-01. J. Appl. Pharm. Sci., 2017, 7, 174-178.
[55]
Ghazala, I.; Haddar, A.; Ben Romdhane, M.; Ellouz-Chaanouni, S. Screening and molecular identification of new microbial strains for production of enzymes of biotechnological. Int. Braz. Arch. Biol. Technol., 2016, 59e16150152
[http://dx.doi.org/10.1590/1678-4324-2016150152]

Rights & Permissions Print Cite
Article Metrics
6
© 2024 Bentham Science Publishers | Privacy Policy