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A Non-Polyene Antifungal Antibiotic from Streptomyces Albidoflavus PU 23

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A Non-Polyene Antifungal Antibiotic from Streptomyces Albidoflavus PU 23 A non-polyene antifungal antibiotic from Streptomyces albidoflavus PU 23 † † S K AUGUSTINE*, S P BHAVSAR and B P KAPADNIS PG Department of Microbiology, Abeda Inamdar Senior College, 2390-B, KB Hidayatullah Road, Azam Campus, Camp, Pune 411 001, India †Department of Microbiology, University of Pune, Pune 411 007, India *Corresponding author (Fax, 91-20-26434286; Email, [email protected]) In all 312 actinomycete strains were isolated from water and soil samples from different regions. All these iso- lates were purified and screened for their antifungal activity against pathogenic fungi. Out of these, 22% of the isolates exhibited activity against fungi. One promising strain, Streptomyces albidoflavus PU 23 with strong anti- fungal activity against pathogenic fungi was selected for further studies. Antibiotic was extracted and purified from the isolate. Aspergillus spp. was most sensitive to the antibiotic followed by other molds and yeasts. The antibiotic was stable at different temperatures and pH tested and there was no significant loss of the antifungal activity after treatment with various detergents and enzymes. Synergistic effect was observed when the antibi- otic was used in combination with hamycin. The antibiotic was fairly stable for a period of 12 months at 4°C. The mode of action of the antibiotic seems to be by binding to the ergosterol present in the fungal cell mem- brane resulting in the leakage of intracellular material and eventually death of the cell. The structure of the anti- biotic was determined by elemental analysis and by ultraviolet (UV), Fourier transform infrared (FTIR), nuclear magnetic resonance (NMR) and liquid chromatography mass spectra (LCMS). The antibiotic was found to be a straight chain polyhydroxy, polyether, non-proteinic compound with a single double bond, indicating a non- polyene antifungal antibiotic. [Augustine S K, Bhavsar S P and Kapadnis B P 2005 A non-polyene antifungal antibiotic from Streptomyces albidoflavus PU 23; J. Biosci. 30 201–211] 1. Introduction The history of new drug discovery processes shows that novel skeletons have, in the majority of cases, come from Among the different types of drugs prevailing in the natural sources (Bevan et al 1995). This involves the scre- market, antifungal antibiotics are a very small but signi- ening of microorganisms and plant extracts (Shadomy ficant group of drugs and have an important role in the 1987). The search for new, safer, broad-spectrum anti- control of mycotic diseases. The need for new, safe and more fungal antibiotics with greater potency has been progress- effective antifungals is a major challenge to the pharma- ing slowly (Gupte et al 2002). One reason for the slow ceutical industry today, especially with the increase in progress compared to antibacterials is that, like mammalian opportunistic infections in the immunocompromised host. cells, fungi are eukaryotes and therefore agents that in- Keywords. Antibiotic; antifungal; non-polyene; Streptomyces albidoflavus ________________ Abbreviations used: BJMC, Byramjee Jeejeebhoy Medical College; DEPT, distortionless enhancement by polarization transfer; DSS, dimethyl silapentane sulfonate; FTIR, Fourier transform infrared; LCMS, liquid chromatography mass spectrum; MFC, mini- mum fungicidal concentration; MIC, minimum inhibitory concentration; MTCC, microbial type culture collection; NCCLS, National Committee for Clinical Laboratory Standards; NCIM, National Collection of Industrial Microorganisms; NMR, nuclear magnetic resonance; NRRL, Northern Regional Research Laboratory; SDA, Sabouraud dextrose agar; SDS, sodium dodecyl sul- phate; TLC, thin-layer chromatography; UV, ultraviolet. http://www.ias.ac.in/jbiosci J. Biosci. 30(2), March 2005, 201–211, © Indian Academy of Sciences 201 202 S K Augustine, S P Bhavsar and B P Kapadnis hibit protein, RNA or DNA biosynthesis in fungi have trifuged at 10,000 rpm for 20 min to separate the mycelial greater potential for toxicity to the host as well (Georgo- biomass. Different solvents were used and tested for the papadakou and Tkacz 1994). The other reason is that, extraction of the antibiotic from the culture supernatant. until recently, the incidence of life threatening fungal The solvents used were n-butanol, n-hexane, ethyl acetate, infections was perceived as being too low to warrant petroleum ether, chloroform, benzene and xylene to de- aggressive research by the pharmaceutical companies termine the ideal solvent for extraction of the antibiotic from (Georgopapadakou and Tkacz 1996). In the course of our the culture supernatant (see table 1). The solvent was added screening programme for new antifungal antibiotics, a to the supernatant in 1 : 1 proportion. Solvent-supernatant Streptomyces sp. PU 23 producing a non-polyene anti- mixture was agitated for 45 min with homogenizer. The fungal antibiotic was isolated from Pune University campus solvent was separated from broth by separating funnel. soil and later on identified as Streptomyces albidoflavus Solvent was centrifuged at 5000 rpm for 15 min to re- PU 23 (Augustine 2004). The taxonomy of the antibiotic move traces of fermentation broth. All extracts were as- producing strain and its antifungal activity in detail as sayed for their antifungal activity using respective well as production optimization have been described in solvents as control by agar well diffusion method (Augu- our previous paper (Augustine et al 2004). In the present stine et al 2004). communication, we report the isolation, purification and characterization of the antifungal antibiotic from S. albi- 2.4 Separation of antibiotic from solvent doflavus PU 23. The solvent, n-hexane was evaporated by subjecting the 2. Materials and methods sample to rotating flash evaporator (Buchi, Switzerland) at 40°C (50 rpm) under vacuum. The dark brown gummy 2.1 Actinomycete isolates substance obtained was dissolved in ethanol and concen- trated, following which the crude antibiotic powder was Three hundred and twelve isolates of actinomycetes ob- obtained. The crude antibiotic was collected and dried in tained from water and soil samples in Pune (Maharashtra), vacuum oven at 40°C overnight. The residue obtained Bangalore (Karnataka) and Malapuram (Kerala) were (crude antibiotic) was subjected to purification. used during the course of our investigation. All these isolates were screened for their antifungal activity against 2.5 Purification of antibiotic pathogenic fungi. The crude antibiotic was tested for number of components 2.2 Target organisms present by using precoated thin-layer chromatography (TLC) plates (Polygramâ Sil G/UV 254, Macherey-Nagel) Aspergillus niger NCIM586, Aspergillus flavus NCIM1028, using ethanol: water: chloroform (40 : 40 : 20) solvent Aspergillus fumigatus MTCC2544, Fusarium oxysporum system. Purification of the antibiotic was carried out by NCIM1072, Candida albicans NCIM 7102, Cryptococcus column chromatography using silica gel (60–120 mesh) humicolus NRRL12944, Cryptococcus sp. NCIM3349, Cry- of column chromatography grade (SRL, Mumbai). Col- ptococcus neoformans BJMC, Penicillium sp. NCIM768, umn (35 × 10 mm) was cleaned using water and rinsed Epidermophyton floccosum MTCC613, Trichophyton men- with acetone. After drying, a small piece of cotton was tagrophytes BJMC, Trichophyton rubrum MTCC296 and placed at the bottom of the column. Silica gel was then Microsporum gypseum MTCC283 were used as target or- packed in the column by using ethanol: water (50 : 50) as ganisms. solvent system. The crude antibiotic was loaded at the top The following work deals with the characterization of of the column and eluted using ethanol: water (50 : 50) as the antibiotic from an actinomycete isolate, S. albidoflavus solvent system. Fractions were collected at 20 min inter- PU 23, which was selected on the basis of its strong anti- val. TLC of each fraction was performed using precoated fungal activity against the target organisms. TLC plates and simple glass plates to detect the antibiotic. The TLC plates were exposed to iodine vapors to develop the antibiotic, if any. The fractions having same Rf value 2.3 Extraction of the antibiotic from culture were mixed together and the solvent evaporated at 40°C supernatant using different solvents in a vacuum oven. These fractions were tested for their antifungal activity by using the agar well diffusion method. As maximum antibiotic production was observed on the The fractions showing antifungal activity were again puri- 8th day of incubation (Augustine et al 2004), fermenta- fied by using the same above mentioned column chroma- tion was terminated on the 8th day and the broth was cen- tography system and purity was confirmed using TLC J. Biosci. 30(2), March 2005 A non-polyene antifungal antibiotic 203 plates. The brown coloured powder obtained was stored lar to each other on the agar plates already spread inocu- in an ampoule at 4°C. lated with C. albicans and incubated at 28°C for two days. The inhibition was observed in the presence and absence of hamycin (Cappuccino and Sherman 1999). 2.6 Determination of minimum inhibitory concentration Similar tests were carried out in combination with nys- and minimum fungicidal concentration values of the tatin and amphotericin B. antibiotic from S. albidoflavus PU 23 against different target organisms 2.10 Effect of ergosterol on antifungal activity of the The minimum inhibitory concentration (MIC) and mini- antibiotic from S. albidoflavus PU 23 mum fungicidal concentration (MFC) values (see table 2) of
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