Abstract
The antimicrobial activity of anthraquinone emodin isolated from Aspergillus awamori WAIR120 (LC032125) culture was investigated against some clinical, phytopathogenic and foodborne pathogenic microorganisms using an agar diffusion method. Among bacterial and fungal strains tested, the highest activity was obtained against Enterococcus faecalis AHR7 as well as Aspergillus niger OC20 with minimal inhibitory emodin concentration of 125 and 85 μg/mL, respectively. Emodin was found to induce morphogenic effects including swelling and elongation of bacterial cell and conidiation decrease, pigmentation loss, and cytoplasmic retraction of fungal cell, as was shown by light microscopy. Additionally, cellular effects were also resulted, in which emodin caused considerable changes in the nature of cell membrane and submicroscopic structure of bacterial and fungal cell, as was shown by transmission electron microscopy. Furthermore, there was an evidence of a disruption of lipid metabolism of fungal cell. These findings thus indicate the future possibility of exploiting emodin as an effective inhibitor of clinical, phytopathogenic and foodborne pathogenic microorganisms.
Acknowledgements
The authors thank Dr. Basma Hamdy Amin, TEM Unit, Regional Center for Mycology and Biotechnology, Al-Azhar University, Cairo, Egypt, for excellent technical assistance during the processing steps of TEM. The work employed herein was supported in part by the Department of Botany and Microbiology, Faculty of Science, Zagazig University, Egypt.
References
Abd El-Aal M.A. 2012. Opportunistic fungi associated with ocular infections in Sharkia district. Master Thesis, Zagazig University, Zagazig, Egypt.Search in Google Scholar
Agosti G., Birkinshaw J.H. & Chaplen P. 1962. Studies in the biochemistry of micro-organisms. 112. Anthraquinone pigments of strains of Cladosporium fulvum Cooke. Biochem. J. 85: 528-530.10.1042/bj0850528Search in Google Scholar
Al-Nuri M., Za’tar N.A., Abu-Eid M.A., Hannoun M.A., Al Jondi W.J., Hussein A.I. & Ali-Shtayeh M.S. 1996. Emodin, a naturally occuring anthraquinone: its isolation and spectropho-tometric determination in Rumex cyprius Plant. Spectrosc. Lett. 29: 1539-1543.10.1080/00387019608007144Search in Google Scholar
Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W. & Lipman D.J. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.10.1093/nar/25.17.3389Search in Google Scholar
Anke H., Kolthoum I. & Laatsch H. 1980. Metabolic products of microorganisms. 192. The anthraquinones of the Aspergillus glaucus group. II. Biological activity. Arch. Microbiol. 126:231-236.10.1007/BF00409925Search in Google Scholar
Auffray Y., Boutibonnes P. & Lemarinier S. 1984. Filamentous forms of Bacillus thuringiensis (Berliner) formed in the presence of genotoxic mycotoxins. Microbiol. Aliments Nutr. 2: 59-67.Search in Google Scholar
Barnard D.L., Huffman J.H., Morris J.L., Wood S.G., Hughes B.G. & Sidwell R.W. 1992. Evaluation of the antiviral activity of anthraquinones, anthrones and anthraquinone derivatives against human cytomegalovirus. Antiviral Res. 17:63—77.10.1016/0166-3542(92)90091-ISearch in Google Scholar
Basu S., Ghosh A. & Hazra B. 2005. Evaluation of the antibacterial activity of Ventilago madraspatana Gaertn., Rubia cordifolia Linn. and Lantana camara Linn.: isolation of emodin and physcion as active antibacterial agents. Phytother. Res. 19:888-894.10.1002/ptr.1752Search in Google Scholar PubMed
Boik J.C. 1995. Cancer and Natural Medicine: A Textbook of Basic Science and Clinical Research. Oregon Medical Press, Princeton, MN, USA.Search in Google Scholar
Carmo E.S., de Oliveira Lima E., de Souza E.L. & de Sousa F.B. 2008. Effect of Cinnamomum zeylancium blume essential oil on the growth and morphogenesis of some potentially pathogenic Aspergillus species. Braz. J. Microbiol. 39:91—97.10.1590/S1517-83822008000100021Search in Google Scholar
Chang C.H., Lin C.C., Yang J.J., Namba T. & Hattori M. 1996. Antiinflammatory effects of emodin from Ventilago leiocarpa. Am. J. Chin. Med. 24: 139-142.10.1142/S0192415X96000189Search in Google Scholar PubMed
Chang M., Wang J., Tian F., Zhang Q. & Ye B. 2010. Antibacterial activity of secondary metabolites from Aspergillus awamori F12 isolated from rhizospheric soil of Rhizophora stylosa Griff. Acta Microbiol. Sin. 50: 1385-1391.Search in Google Scholar
Cheng Y.W. & Kang J.J. 1998. Emodin-induced muscle contraction of mouse diaphragm and the involvement of Ca2+ influx and Ca2+ release from sarcoplasmic reticulum. Br. J. Pharmacol. 123:815-820.10.1038/sj.bjp.0701677Search in Google Scholar PubMed PubMed Central
Chukwujekwu J.C., Coombes P.H., Mulholland D.A. & van Staden J. 2006. Emodin, an antibacterial anthraquinone from the roots of Cassia occidentalis. S. Afr. J. Bot. 72:295-297.10.1016/j.sajb.2005.08.003Search in Google Scholar
de Barros I.B., de Souza-Daniel J.F., Pinto J.P., Rezendo M.I., Filho R.B. & Ferreira D.T. 2011. Phytochemical and antifun-gal activity of anthraquinones and root and leaf extracts of Coccoloba mollis on phytopathogens. Braz. Arch. Biol. Tech-nol. 54: 535-541.10.1590/S1516-89132011000300015Search in Google Scholar
Donnelly D.M.X. & Sheridan M.H. 1986. Anthraquinones from Trichoderma polysporum. Phytochem. 25:2303—2304.10.1016/S0031-9422(00)81684-2Search in Google Scholar
Ezzat S.M., El-Sayed E.A., Abou El-Hawa M.I. & Ismaiel A.A. 2007. Morphological and ultrastructural studies for the biological action of penicillic acid on some bacterial species. Res. J. Microbiol. 2: 303-314.10.3923/jm.2007.303.314Search in Google Scholar
Ghosh A.C., Manmade A. & Demain A.L. 1977. Toxins from Penicillium islandicum Sopp, pp. 625—638. In: Rodricks J.V., Hesseltine C.W. & Mehlman M.A. (eds) Mycotoxins in Human and Animal Health. Pathotox, Chicago.Search in Google Scholar
Ismaiel A.A., Ali A.E.S. & Enan G. 2014. Incidence of Listeria in Egyptian meat and dairy samples. Food Sci. Biotechnol. 23:179-185.10.1007/s10068-014-0024-5Search in Google Scholar
Ismaiel A.A., Bassyouni R.H., Kamel Z. & Gabr S.M. 2016. Detoxification of patulin by kombucha tea culture. CyTA J. Food 14: 271-279.10.1080/19476337.2015.1096828Search in Google Scholar
Ismaiel A.A. & Papenbrock J. 2014. The effects of patulin from Penicillium vulpinum on seedling growth, root tip ultrastruc-ture and glutathione content of maize. Eur. J. Plant Pathol. 139:497-509.10.1007/s10658-014-0406-9Search in Google Scholar
Ismaiel A.A., Rabie G.H., Kenawey S.E.M. & Abd El-Aal M.A. 2012. Efficacy of aqueous garlic extract on growth, afla-toxin B1 production, and cyto-morphological aberrations of Aspergillus flavus, causing human ophthalmic infection: topical treatment of A. flavus keratitis. Braz. J. Microbiol. 43: 1355-1364.Search in Google Scholar
Izhaki I. 2002. Emodin — a secondary metabolite with multiple ecological functions in higher plants. New Phytol. 155:205— 217.10.1046/j.1469-8137.2002.00459.xSearch in Google Scholar
Kögl F. & Postowsky J.J. 1925. Untersuchungen über Pilzfarbstoffe. II. Über die Farbstoffe des blutroten Hautkorpfes (Der-mocybe sanquinea Wulf.). Justus Liebigs Ann. Chem. 444:1-7.10.1002/jlac.19254440102Search in Google Scholar
Le Van T. 1984. Emodin a fungal metabolite and the effects of emodin on the growth of some soil microorganisms. Acta Agr. Silv. Ser. Agraria 23:235-242.Search in Google Scholar
Lu C., Wang H., Lv W., Xu P., Zhu J., Xie J., Liu B. & Lou Z. 2011. Antibacterial properties of anthraquinones extracted from rhubarb against Aeromonas hydrophila. Fish Sci. 77:375-384.10.1007/s12562-011-0341-zSearch in Google Scholar
Lu Y.Y., Zhang J.L. & Qian J.M. 2008. The effect of emodin on VEGF receptors in human colon cancer cells. Cancer Biother. Radiopharm. 23:222-228.10.1089/cbr.2007.0425Search in Google Scholar PubMed
Masuda T. & Ueno Y. 1984. Microsomal transformation of emodin into a direct mutagen. Mutat. Res. 125:135—144.10.1016/0027-5107(84)90065-4Search in Google Scholar
Moubasher A.H. 1993. Soil Fungi in Qatar and Other Arab Countries. The Centre for Scientific and Applied Research, Doha, Qatar.Search in Google Scholar
Mueller S.O., Schmitt M., Dekant W., Stopper H., Schlatter J., Schreier P. & Lutz W.K. 1999. Occurrence of emodin, chryso-phanol and physcion in vegetables, herbs and liquors. Geno-toxicity and antigenotoxicity of the anthraquinones and of the whole plants. Food Chem. Toxicol. 37:481-491.10.1016/S0278-6915(99)00027-7Search in Google Scholar
Natori S., Sato F. & Udagawa S. 1965. Anthraquinone metabolites of Talaromyces avellanens (Thom et Turreson), C.R. Benjamin and Preussia multispora (Saito et Minoura) Cain. Chem. Pharm. Bull. 13:385-389.10.1248/cpb.13.385Search in Google Scholar
Panichayupakaranant P., Sakunpak A. & Sakunphueak A. 2009. Quantitative HPLC determination and extraction of anthraquinones in Senna alata leaves. J. Chromatogr. Sci. 47: 197-200.10.1093/chromsci/47.3.197Search in Google Scholar
Peng J., Song Z. & Ma C. 2008. Emodin studies on pharmacokinetics and distribution in rat liver after Polygonum cuspida-tum Sieb. et Zucc. extract administration. World Sci. Technol. 10: 64-67.10.1016/S1876-3553(09)60004-1Search in Google Scholar
Shia C.S., Hou Y.C., Tsai S.Y., Huieh P.H., Leu Y.L. & Chao P.D. 2010. Differences in pharmacokinetics and ex vivo an-tioxidant activity following intravenous and oral administrations of emodin to rats. J. Pharm. Sci. 99:2185-2195.10.1002/jps.21978Search in Google Scholar PubMed
Shibata S., Shoji J., Ohta A. & Watanable M. 1957. Metabolic products of fungi. XI. Some observations on the occurrence of skyrin and rugulosin in mold metabolites with reference to structural relationships between penicilliopsin and skyrin. Chem. Pharm. Bull. 5: 380-383.10.1248/cpb1953.5.380Search in Google Scholar PubMed
Shibata S. & Udagawa S. 1963. Metabolic products of fungi. XIX. Isolation of rugulosin from Penicillium brunneum Udagawa. Chem. Pharm. Bull. 11:402-40310.1248/cpb.11.402Search in Google Scholar
Shieh D.E., Chen Y.Y., Yen M.H., Chiand L.C. & Lin C.C. 2004. Emodin-induced apoptosis through p53-dependent pathway in human hepatoma cells. Life Sci. 74: 2279-229010.1016/j.lfs.2003.09.060Search in Google Scholar PubMed
Singh U.P., Singh K.P., Singh S.P., Ram S.N. & Pandey V.B. 1992. Effect of emodin isolated from Rhamnus triquetra on spore germination of some fungi. Fitopatol. Bras. 17:420— 422.Search in Google Scholar
Turner W.B. & Aldridge D.C. 1983. Fungal Metabolites II. London, Academic Press.Search in Google Scholar
Ubbink-Kok T., Anderson J.A. & Konings W.N. 1986. Inhibition of electron transfer and uncoupling effects by emodin and emodinanthrone in Escherichia coli. Antimicrob. Agents Chemother. 30: 147-151.10.1128/AAC.30.1.147Search in Google Scholar PubMed PubMed Central
Wang C., Zhang D., Ma H. & Liu J. 2007. Neuroprotective effects of emodin-8-O-beta-D-glucoside in vivo and in vitro. Eur. J. Pharmacol. 577:58-63.10.1016/j.ejphar.2007.08.033Search in Google Scholar
Wang H.H. 1993. Antitrichomonal action of emodin in mice. J. Ethnopharmacol. 40: 111-116.10.1016/0378-8741(93)90055-ASearch in Google Scholar
Wang H.H. & Chung J.G. 1997. Emodin-induced inhibition of growth and DNA damage in the Helicobacter pylori. Curr. Microbiol. 35:262-266.10.1007/s002849900250Search in Google Scholar
Wang W., Zhou Q., Liu L. & Zou K. 2012. Antiallergic activity of emodin on IgE-mediated activation in RBL-2H3 cells. Pharmacol. Rep. 64: 1216-1222.10.1016/S1734-1140(12)70917-9Search in Google Scholar
Wells J.M., Cole R.J. & Kirksey J.W. 1975. Emodin, a toxic metabolite of Aspergillus wentii isolated from weevil-damaged chestnuts. Appl. Microbiol. 30: 26-28.10.1128/am.30.1.26-28.1975Search in Google Scholar PubMed PubMed Central
Xue J., Ding W. & Liu Y. 2010. Anti-diabetic effects of emodin involved in the activation of PPARgamma on high-fat dietfed and low dose of streptozotocin-induced diabetic mice. Fitoterapia 81: 173-177.10.1016/j.fitote.2009.08.020Search in Google Scholar PubMed
Yamazaki M., Maebayashi Y. & Miyaki K. 1971. The isolation of secalonic acid A from Aspergillus ochraceus cultured on rice. Chem. Pharm. Bull. 19: 199-201.10.1248/cpb.19.199Search in Google Scholar PubMed
Zhang L., Lau Y.K., Xi L., Hong R.L., Kim D.S., Chen C.F., Hortobagyi G.N., Chang C. & Hung M.C. 1998. Tyrosine kinase inhibitors, emodin and its derivative repress HER-2/neuinduced cellular transformation and metastasis-associated properties. Oncogene 16: 2855-2863.10.1038/sj.onc.1201813Search in Google Scholar PubMed
- Abbreviations
- HPLC
high performance liquid chromatography
- MIC
minimal inhibitory concentration
- TEM
transmission electron microscopy
- TLC
thin layer chromatography.
© 2016 Institute of Botany, Slovak Academy of Sciences
Articles in the same Issue
- Cellular and Molecular Biology
- A broad host range food-grade cloning vector for lactic acid bacteria
- Cellular and Molecular Biology
- Antimicrobial and morphogenic effects of emodin produced by A spergillus awamori WAIR120
- Cellular and Molecular Biology
- Herbal augmentation enhances malachite green bio degradation efficacy of Saccharomyces cerevisiae
- Cellular and Molecular Biology
- Efflux pump inhibitory activity of flavonoids isolated from Alpinia calcarata against methicillin-resistant Staphylococcus aureus
- Cellular and Molecular Biology
- Status of metal pollution in rivers flowing through urban settlements at Pune and its effect on resident microflora
- Cellular and Molecular Biology
- Use of N, N′-diacetylchitobiose in decreasing toxic effects of indoor air pollution by preventing oxidative DNA damage
- Botany
- The relationship between macrophyte assemblages and environmental variables in drainage and irrigation canals in Slovakia
- Botany
- Effects of ZnCl2 on ROS generation, plasma membrane properties, and changes in protein expression in grapevine root explants
- Botany
- Molecular characterization and alternative splicing of a MYB transcription factor gene in tumourous stem mustard and its response to abiotic stresses
- Zoology
- First report of Gussevia asota (Monogenea: Dactylogyridae), destructive parasite of A stronotus ocellatus (Perciformes: Cichlidae) in Europe
- Zoology
- Response of the carpet shell clam (Ruditapes decussatus) and the Manila clam (Ruditapes philippinarum) to salinity stress
- Zoology
- Biodiversity of zooplankton (Rotifera and crustacea) in water soldier (Stratiotes aloides) habitats
- Zoology
- Testing for longitudinal zonation of macroinvertebrate fauna along a small upland headwater stream in two seasons
- Zoology
- Aphids (Hemiptera: Aphididae) of different plant communities in an urban environment
- Zoology
- Seasonal activity of adult leaf beetles (Coleoptera: Chrysomelidae, Orsodacnidae) occurring in Kovada Lake and Kızıldağ National Parks in Isparta province (Turkey)
- Cellular and Molecular Biology
- Ependymal tables designated for differentiation of the ependyma based on the adjacent periventricular structures
Articles in the same Issue
- Cellular and Molecular Biology
- A broad host range food-grade cloning vector for lactic acid bacteria
- Cellular and Molecular Biology
- Antimicrobial and morphogenic effects of emodin produced by A spergillus awamori WAIR120
- Cellular and Molecular Biology
- Herbal augmentation enhances malachite green bio degradation efficacy of Saccharomyces cerevisiae
- Cellular and Molecular Biology
- Efflux pump inhibitory activity of flavonoids isolated from Alpinia calcarata against methicillin-resistant Staphylococcus aureus
- Cellular and Molecular Biology
- Status of metal pollution in rivers flowing through urban settlements at Pune and its effect on resident microflora
- Cellular and Molecular Biology
- Use of N, N′-diacetylchitobiose in decreasing toxic effects of indoor air pollution by preventing oxidative DNA damage
- Botany
- The relationship between macrophyte assemblages and environmental variables in drainage and irrigation canals in Slovakia
- Botany
- Effects of ZnCl2 on ROS generation, plasma membrane properties, and changes in protein expression in grapevine root explants
- Botany
- Molecular characterization and alternative splicing of a MYB transcription factor gene in tumourous stem mustard and its response to abiotic stresses
- Zoology
- First report of Gussevia asota (Monogenea: Dactylogyridae), destructive parasite of A stronotus ocellatus (Perciformes: Cichlidae) in Europe
- Zoology
- Response of the carpet shell clam (Ruditapes decussatus) and the Manila clam (Ruditapes philippinarum) to salinity stress
- Zoology
- Biodiversity of zooplankton (Rotifera and crustacea) in water soldier (Stratiotes aloides) habitats
- Zoology
- Testing for longitudinal zonation of macroinvertebrate fauna along a small upland headwater stream in two seasons
- Zoology
- Aphids (Hemiptera: Aphididae) of different plant communities in an urban environment
- Zoology
- Seasonal activity of adult leaf beetles (Coleoptera: Chrysomelidae, Orsodacnidae) occurring in Kovada Lake and Kızıldağ National Parks in Isparta province (Turkey)
- Cellular and Molecular Biology
- Ependymal tables designated for differentiation of the ependyma based on the adjacent periventricular structures