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Evaluation of Antibacterial Activity of Australian Pharmaceutical Biology Pharmaceutical Biology, 2011, 1–9, Early Online 2011 © 2011 Informa Healthcare USA, Inc. ISSN 1388-0209 print/ISSN 1744-5116 online 00 DOI: 10.3109/13880209.2010.526616 00 1 ORIGINAL ARTICLE 9 12 September 2010 Evaluation of antibacterial activity of Australian 20 September 2010 basidiomycetous macrofungi using a high-throughput 96-well plate assay 21 September 2010 1388-0209 Neeraj Bala1,2, Elizabeth A.B. Aitken2, Nigel Fechner2,3, Andrew Cusack4, and Kathryn J. Steadman1,2 1744-5116 1School of Pharmacy and 2School of Biological Sciences, The University of Queensland, Brisbane, Queensland, Australia, 3Queensland Herbarium, Brisbane, Queensland, Australia, and 4Department of Employment, Economic Development © 2011 Informa Healthcare USA, Inc. and Innovation, Brisbane, Queensland, Australia 10.3109/13880209.2010.526616 NPHB Abstract Context: The production of antimicrobial compounds by macrofungi is not unexpected because they have to compete 526616 with other organisms for survival in their natural hostile environment. Previous studies have indicated that macrofungi contain secondary metabolites with a range of pharmacological activities including antimicrobial agents. Objective: To investigate macrofungi for antimicrobial activity due to the increasing need for new antimicrobials as a result of resistance in the bacterial community to existing treatments. Materials and methods: Forty-seven different specimens of macrofungi were collected across Queensland, Australia. Freeze-dried fruiting bodies were sequentially extracted with three solvents: water, ethanol, and hexane. These extracts were tested against representative Gram+ve, Staphylococcus aureus and Gram−ve, Escherichia coli bacteria. Results and discussion: Overall water and ethanol extracts were more effective against S. aureus than E. coli, whereas For personal use only. a small number of hexane extracts showed better results for their antimicrobial potential against E. coli at higher concentrations only. Encouraging results were found for a number of macrofungi in the genera Agaricus (Agaricaceae), Amanita (Amanitaceae), Boletus (Boletaceae), Cantharellus (Cantharellaceae), Fomitopsis (Fomitopsidaceae), Hohenbuehelia (Pleurotaceae), Lentinus (Polyporaceae), Ramaria (Gomphaceae), and Strobilomyces (Boletaceae) showing good growth inhibition of the pathogens tested. Conclusion: The present study establishes the antimicrobial potential of a sample of Australian macrofungi that can serve as potential candidates for the development of new antibiotics. Keywords: Fungi, antibacterial, water extracts, 96-well plate assay, S. aureus, E. coli (Alfonso, 2005) and hence, more and better antibiot- Pharmaceutical Biology Downloaded from informahealthcare.com by University of Queensland on 03/01/11 Introduction ics are needed as indicated by the “10 × ‘20 Initiative” to The accidental discovery of penicillin from fungi develop 10 new antibiotics by 2020 by Infectious Diseases (Fleming, 1929) widely attracted scientific attention for Society of America (2010). the potential role of fungi as antimicrobial agents and Most fungi-derived pharmaceuticals have been lead to the discovery and development of other antibiot- sourced from Ascomyceteous fungi where most (but ics. However, the emergence and subsequent spread of not all) species produce microscopic fruiting bodies; antibiotic resistant bacterial strains is of increasing con- for example, those used in pharmaceuticals include cern as reviewed by Levy and Marshall (2004). Currently, Penicillium, Aspergillus, and so on, whereas perhaps this problem presents a significant challenge to medicine fewer pharmaceuticals, certainly in an industrial con- because of the therapeutic failure of life-saving drugs text, have been derived from the higher phyla of fungi, Address for Correspondence: Neeraj Bala, School of Pharmacy, The University of Queensland, Brisbane, Queensland 4072, Australia. Tel.: +61-7-33461891 (O), 0449775464 (M). Fax: +61-7-33461999. E-mail: [email protected] (Received 12 September 2010; revised 20 September 2010; accepted 21 September 2010) 1 2 N. Bala et al. the Basidiomycota. The Basidiomycota contains an of their antimicrobial potential (Ovenden et al., 2005; abundance of species that produce large fruiting bod- Beattie et al., 2010). Therefore, considering the previous ies including typical mushrooms, coral fungi, puffballs, reports on the antimicrobial potential of macrofungi and bracket fungi, and so on. Some species are frequently used in view of the continuous need for the development of as a food source such as the common field mushroom, new antimicrobials, the present study aimed to evaluate Agaricus bisporus (J. E. Lange) Imbach (Agaricaceae); a sample of Australian macrofungi for their antibacte- others have been used chiefly in medicine (Boa, 2004; rial activity against sensitive strains of Staphylococcus Molitoris, 1994), whereas some are known for their noto- aureus (Gram+ve) and Escherichia coli (Gram−ve). The riously toxic properties such as Amanitas. agar well diffusion and disc diffusion methods are com- According to Chang and Buswell (1996), the Romans monly used for antimicrobial activity testing but these perceived mushrooms as “Food of the Gods,” the Chinese methods have some limitations. For example, some treasured them as a health food, whereas Lentinula compounds may be more diffusible and can produce a edodes (Berk.) Pegler (Marasmiaceae), the shiitake greater zone of inhibition despite their lower activity in mushroom, was highly prized by Japanese emperors as comparison with less diffusible compounds that might an aphrodisiac and was cultivated at secret and heavily be more active but may produce smaller zone of inhibi- guarded locations. In accordance with their traditional tion (Janes et al., 2007; Lund et al., 2009). Therefore, in uses, macrofungi have been extensively investigated for the present study, a high-throughput 96-well microplate their therapeutic significance resulting in the discovery bioassay procedure was used. of an antibiotic pleuromutilin from Pleurotus mutilis (Fr.) Sacc. and Pleurotus passeckerianus Pilat (Pleurotaceae) Materials and methods (Kavanagh et al., 1951). A number of pleuromutilin derivatives have since been developed for veterinary use Sample collection in the treatment of Mycoplasma infections (Drews et al., Macrofungi fruiting bodies (47 different species) were 1975; Werner et al., 1978; Hannan et al., 1997; Hunt, 2000; collected from a range of natural environments across Jones et al., 2002; Xu et al., 2009). Furthermore, retapa- Queensland, Australia during May 2008 to October 2009 mulin (Altabax) has emerged as an antibiotic for human (Table 1). The fruiting bodies were identified based on use for the topical treatment of Gram+ve bacterial skin sporocarp morphology and macroscopic characters. The infections including methicillin-resistant Staphylococcus collections were freeze-dried and stored at −80°C until aureus (Jones et al., 2006; Novak & Shlaes, 2010). extraction. The therapeutic potential of mushrooms has been extensively reviewed by Wasser and Weis (1999) and Preparation of macrofungi extracts Lindequist et al. (2005). Extracts of various fungal fruit- Freeze-dried macrofungi (500 mg) were macerated in For personal use only. ing bodies such as Pleurotus ostreatus (Jacq.) P. Kumm. 25 mL distilled water and then extracted for 1 h in an ultra- (Iwalokun et al., 2007), Pholiota adiposa (Fr.) P. Kumm. sonic water bath. Following centrifugation (15,000 rpm (Strophariaceae) (Dulger, 2004), Coprinus digitalis for 15 min), the supernatant was removed. The residue (Batsch) Fr. (Agaricaceae) (Efremenkova et al., 2003), was re-extracted with 25 mL water in the sonicating Podaxis pistillaris (L.) Fr. (Agaricaceae) (Al-Fatimi et al., water bath for 30 min, centrifuged, and the supernatant 2006), Lycoperdon pusillum Batsch [now Bovista pusilla was pooled with that from the first extraction, collec- (Batsch) Pers.], and Lycoperdon giganteum Batsch [now tively forming 50 mL of water extract, which was filtered Calvatia gigantea (Batsch) Lloyd] (Lycoperdaceae) through 0.45-µm membrane filter and freeze-dried. The (Jonathan & Fasidi, 2003) have shown activity against a remaining insoluble material was extracted sequentially range of different Gram+ve and Gram−ve bacteria and with 100% ethanol and n-hexane, respectively, following also fungi. Stamets (2006) mentioned that macrofungi the same procedure as described for the water extracts. Pharmaceutical Biology Downloaded from informahealthcare.com by University of Queensland on 03/01/11 produce numerous novel pharmaceuticals. However, The ethanol extracts were evaporated to dryness under only a small proportion (10%) of the total estimated reduced pressure in a rotary evaporator at 40°C, whereas number of macrofungi species on Earth (140,000) has the hexane extracts were evaporated overnight in a fume been described (Hawksworth, 2001). It means that hood. there is an enormous inherent scope for the nutritional and medicinal value among macrofungi that still needs Preparation of mushroom extracts concentrations to be discovered. The same is true for the Australian The water extracts were each dissolved in 2 mL of distilled macrofungi. Among 10,000 estimated Australian water. The ethanol and hexane extracts were first dis- macrofungi, <4000 have been described, thus leav- solved in 400 µL absolute alcohol, sonicated for 10 min, ing behind a large proportion of macrofungi yet
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