Detection and Isolation of New Glycosides in Culture
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1 J OURNAL OF BACTERIOLOGY, Feb., 1966 Vol. 91, No. 2 Copyright 1966 American Society for Microbiology Printed In U.S.A. Detection and Isolation of New Glycosides in Culture Broths of Streptomyces hygroscopicus' A. D. ELBEIN,' J. A. HOLOWCZAK,' HENRY KOFFLER, AND H. R. GARNER Department of Biological Sciences, Purdue University, West Lafayette, Indiana Received for publication 30 August 1965 ABSTRACr ELBEIN, A. D. (Purdue University, Lafayette, Ind.) J. A. HOLOWCZAK, HENRY KOFFLER, AND H. R. GARNER. Detection and isolation of new glycosides in culture broths of Streptomyces hygroscopicus. J. Bacteriol. 91: Four new compounds not previously reported have been isolated and purified from the culture broths of Streptomyces hygroscopicus. The data presented suggest that these compounds may be structurally related to hygromycin A, having similar aglycons but differing in their sugar moieties. Two of the compounds apparently contain D- glucose or L-fucose as their sugar components. The others, like hygromycin A, form crystalline 2,4-dinitrophenylhydrazones, and may contain unusual keto sugars. Hygromycin A is a weakly acidic antibiotic produced by Streptomyces hygroscopicus (12). It consists of three components: (i) the unusual sugar 5-keto-6-deoxy-D-arabohexose, (ii) 3,4- dihydroxy-a-methylcinnamic acid, and (iii) neoinosamine-2, containing a deoxymethylene bridge attached to two of its hydroxyl groups. The 5-keto-6-deoxy-D-arabohexose is glycosidically bound to carbon atom 3 of the cinnamic acid, and the inosamine is attached to the carboxyl group through an amide linkage (13). Homomycin (15) and antibiotic B (16) have been shown to be structurally related to hygromycin A. A second glycoside antibiotic, hygromycin B, has also been isolated from culture broths of this organism (11). We would now like to report the isolation of additional glycosides related to hygromycin A from culture broths of S. hygroscopicus. Some evidence is also presented to indicate that at least two of these new glycosides have aglycons similar to those of hygromycin A, but differ in the sugar moieties. The detailed chemical compositions of these compounds will be the subject of a future communication. MATERIALS AND METHODS Culture conditions. Cultures of S. hygroscopicus (Jensen) Waksman and Henrici were obtained from 1 Preliminary reports of this work have appeared (9; Elbein, Koffler, and Garner, Federation Proc. 20:78, 1964). 2 Present address, Department of Biology, Rice University, Houston, Tex. 3 Present address, School of Aerospace Medicine, Brooks Air Force Base, San Antonio, Tex. the Eli Lilly Co., Indianapolis, Ind. Cultural conditions for the maintenance of the organism and growth conditions to give high yields of hygromycin A have been reported (Elbein, Koffler, and Gamer, Federation Proc. 20:78, 1964). Assay of antibiotics. Antibiotic levels were determined by diffusion assay as previously described (Elbein, Ph.D. Thesis, Purdue Univ., Lafayette, Ind., 1960). After removal of hygromycin B with Amberlite IRC-50 (11), hygromycin A can be assayed against Staphylococcus aureus (Lilly). Hygromycin B can be assayed in the presence of hygromycin A with Bacillus subtilis as the test organism. Chromatography. One- or two-dimensional paper chromatography was done with Whatman no. 1 or Whatman no. 3MM paper. Thin-layer chromatographic plates were prepared with aluminum oxide G. Chromatographic solvent systems were as follows: (I) isopropanol-n-butanol-water (14:2:4); (II) n- butanol-acetic acid-water (4:1:5); (III) isopropanolwater (9:1); (IV) ethyl acetate-pyridine-water (12: 5:4); (V) ethyl acetate-acetic acid-water (14:3:3); (VI) phenol-water (4:1); (VII) n-butanol-formic acid-water (7:2:1); (VIII) ethyl acetate-aceti acidwater (3:1:1); (IX) ethyl acetate-acetic acid-water (3:1:3); (X) n-propanol-pyridine-acetic acid-water (15:10:3:12); (XI) ethyl alcohol-0.3% HCI (2:1); and (XII) n-butanol-pyridine-water (3:1 :X). Reducing substances were detected with silver nitrate (17), neoinosamine with ninhydrin (14), and 6-deoxyhexose with Waldron's reagent (18). Ketoses were observed with orcinol-trichloroacetic acid (1), carbonyl compounds with 2,4-dinitrophenylhydrazine in HCl (2), and phenolic compounds with diazotized p-nitroaniline (3). Glucostat reagent was used for the detection of D-glucose. Papers were sprayed evenly with this reagent, then incubated at 37 C until the reaction was complete. 604
2 VOL. 91, 1966 GLYCOSIDES OF STREPTOMYCES HYGROSCOPICUS Anialytical method. Total hexose was determined by the anthrone method (5), 6-deoxyhexose by the method of Dische and Shettles (4), D-glucose with Glucostat reagent (Worthington Biochemical Corp., Freehold, N.J.), L-fuCose with the L-fucose isomerase of Escherichia coli (8), neoinosamine and amino acids with ninhydrin (14), and 3,4-dihydroxy-amethylcinnamic acid with the Folin-Ciocalteu reagent (7), and also spectrophotometrically by its absorption at 272 mj1. Infrared spectra were determined as mulls in Nujol. Melting points were measured with a Fisher- Johns apparatus. Isolation of glycosides. Hygromycin A and related glycosides were extracted from culture broths as described by Mann et al. (12). Material which precipitated from anhydrous n-butanol upon addition of petroleum ether is referred to as crude preparation. Free carbohydrates or amino acids were not detected in these preparations. Hygromycin A could be isolated and purified from these crude preparations by chromatography on a column containing equal weights of Darco G-60 and Dicalite-4200 (12). Initial fractionation of glycosides. Initial observations indicated that crude preparations were composed of glycosides containing glucose and fucose as well as 5-keto-6-deoxy-D-arabohexose. Therefore, these preparations were fractionated as follows to determine the nature of these new glycosides. Preparations were treated with 2,4-dinitrophenylhydrazine in HCI according to the method of Mann and Woolf (13). By this procedure, the insoluble 2,4-dinitrophenylhydrazone of hygromycin A was formed and could be removed by centrifugation. The supematant liquid, which is referred to as fraction 1, was then neutralized with Ag2CO3, and excess 2, 4-dinitrophenyihydrazine was removed by extraction with ethyl acetate. Glycosides in the supernatant liquid (fraction 1) were then purified by charcoal-dicalite column chromatography (12). Column fractions containing hexose were pooled, and the compounds were recovered by extraction into n-butanol and precipitation from the butanol with petroleum ether. Since the glycosides were hygroscopic, the amorphous material was then lyophilized. The infrared spectra of this material showed a slight absorption at 5.8 IM, indicating that not all of the carbonyl compound(s) (hygromycin A) had been precipitated. Therefore, the above procedure was repeated until all of the carbonyl absorption band had disappeared (Fig. 2). The isolated material at this stage is referred to as fraction 2. Glycosides (fraction 2) were hydrolyzed in 1.5 N H2SO4 under reflux for 2 hr, after which they were cooled and neutralized with solid BaCO3. The precipitate was removed by filtration, and the filtrate was used for direct analysis. Filtrates were also deionized by passage through Amberlite IR-120 (H+) and Dowex-1 (HCO3-), concentrated in vacuo, and then subjected to paper chromatography. Purificationi of hygromycin A and related glycosides. After initial studie indicated that other glycosides were present in culture broths in addition to hygromycin A, the following methods were developed to isolate and purify these new compounds (Fig. 1). It was observed that the various glycosides could be Culture Concentrate to one-half original volume Saturate with (NH4)2SO4 Extract with n-butanol Discard aqueous layer Concentrate butanol phase until all water is removed Precipitate compounds with petroleum ether Lyophilize precipitated compounds after collection by centrifugation Chromatograph on charcoal-dicalite column 605 Collect fractions, concentrate into n-butanol and precipitate with petrolium ether Chromatograph fractions on Whatman no. 3MM paper to separate components in ethyl acetateacetic acid-water (3:1:3) Recover separated fractions by precipitation from n-butanol Rechromatograph with n-butanol-acetic acidwater (4:1:5) on Whatman no. 3MM paper and reisolate as above FIG. 1. Separation anid purification of glycosides obtained from culture broths of Streptomyces hygroscopicus. partially separated on charcoal-dicalite columns. Thus, 25 g of the crude preparation in 300 ml of N H2SO4 was applied to a column (7 by 70 cm). The column then was washed with 3 liters of acetonewater (3:7) and developed with n-butanol-acetonewater (1: 3: 6). Fractions (20 ml) were collected, assayed for antibiotic activity, and divided as follows: (i) no activity, (ii) zone of inhibition less than 15 mm, (iii) zone of 15 to 20 mm, (iv) zone of 20 to 25 mm, and (v) zone of 25 to 30 mm (peak fractions). Fractions following the peak tube were divided similarly. Fractions also were analyzed by paper chromatography and by their absorbance at 272 mg. The absorbancy at 272 m,u is characteristic of the aglycon portion and was useful for detecting compounds with similar structures that lacked antibiotic activity. Fractions then were pooled and the glycosides were recovered as previously described. The pooled samples then were further purified by paper chromatography on Whatman no. 3MM paper, first in solvent IX, then in solvent II (Fig. 1). Chromatography on active alumina or silica gel (10), as well as paper and thin-layer chromatography of the purified materials, indicated that they were homogenous. Like hygromycin A, all of the compounds failed to crys-
3 606 ELBEIN ET AL. J. BACrEI-FOL. tallize. Two of these materials, however, formed crystalline derivatives with 2, 4-dinitrophenylhydrazine. RESULTS Growth was terminated between the 175 and 230 hr after its initiation, when assays indicated that antibiotic production had reached the maximal level. Crude preparations then were prepared from filtered culture broths as described. When these crude preparations of antibiotic were treated with 2,4-dinitrophenylhydrazine in concentrated HCl at 5 C, hygromycin A and other compounds having a free carbonyl group were precipitated as the insoluble 2,4-dinitrophenylhydrazone derivative. The removal of these carbonyl compounds could be followed by observing the disappearance of the infrared absorption band at 5.8 m,u, which is indicative of a free carbonyl group. These results are shown in Fig. 2. After two or three such treatments, all of the carbonyl compounds had been removed from the solutions. Glycosides were then isolated from the supematant fluid as described (fraction 2). Fraction 2 accounted for about 1% of the initial sample. Crude preparations that had been purified by charcoal-dicalite column chromatography contained less of these other glycosides, whereas column fractions which had been purified further by countercurrent distribution contained no detectable glycosides other than hygromycin A. Analysis of Fraction 2 gave the following analysis (molar ratios): neoinosamine, 0.92; hexose (determined by the anthrone method with an equal mixture of glucose and fucose as the standard), 1.05; 3,4-dihydroxy-a-methylcinnamic acid, When it was subjected to acid hydrolysis, two reducing sugars were detected that had the same mobility as authentic glucose and fucose as shown in Table 1. The unknown az z I.- FREQUENCY (CM-') WAVELENGTH (MICRONS) FIG. 2. Infrared absorption spectra of fractions treated with 2,4-dinitrophenylhydrazine. (A) Material before fractionation; (B) material after first 2,4-dinitrophenylhydrazine treatment (fraction 1); (C) material after third and fourth treatments with reagent (fraction 2). Arrow indicates carbonyl absorption at 5.8,u. Note how peak is reduced and then disappears with treatment. sugar with the same mobility as fucose (unknown I) reacted with L-fucose isomerase, indicating that it was L-fucose. The other unknown sugar (unknown II) reacted with glucose oxidase, and the product of this reaction chromatographed with gluconic acid, indicating that this sugar was D-glucose. The other products formed by hydrolysis of fraction 2 had the same mobilities as authentic neoinosamine and 3,4-dihydroxy-amethylcinnamic acid upon paper chromatography in several different solvent systems. These data TABLE 1. Chromatographic behavior of sugars in fraction 2 RF values in solvent svstem* Compound - I II III IV V VI VII VIII L-Fucose D-Glucose Unknownl Unknown I I D-Gluconic acid t 0.46 (0-44) Unknown II treated with glu- ( cose oxidase (0.43) * Solvent systems are described in the text. t Gluconic acid gives two spots in this solvent.
4 VOL. 91, 1966 GLYCOSIDES OF STREPTOMYCES HYGROSCOPICUS 607 EI cqj N-.- 0CM E _ FRACTION NUMBER FIG. 3. Purification of a glycoside mixture on a charcoal-dicalite column. Eluant: water-acetone-nbutanol (6:3:1). Fractions were analyzedfor absorption at 272 m,u andfor biological activity by the disc method. suggested that two glycosides were present which had aglycons similar to that of hygromycin A but which differed in the carbohydrate constituents. When crude preparations were subjected to two-dimensional paper chromatography, four compounds were clearly present in addition to hygromycin A. These compounds were named hygromycin C, and compounds D, E, and F. Only hygromycin C showed antibiotic activity; the others were all inactive. Like hygromycin A, compounds D and E reacted with 2,4-dinitrophenylhydrazine spray reagent, indicating that they had free carbonyl groups. This would suggest that during the initial fractionation procedure (with 2,4-dinitrophenylhydrazine), compounds D and E would be precipitated along with hygromycin A. Thus, compound F and hygromycin C would correspond to the compounds recovered from the supernatant liquids of these reaction mixtures (fraction 2). Preliminary analyses of these two compounds suggested that the aglycon portion of the molecule was similar to that of hygromycin A, but that one contained D-glucose and the other L-fucose rather than 5- keto-6-deoxy-d-arabohexose (Table 1). When fractions from a charcoal-dicalite column were analyzed for biological activity as well as absorption at 272 m, as shown in Fig. 3, it was observed that, while biological activity eluted in a symmetrical peak, the absorbance at 272 m,u was spread over a great number of fractions. When these fractions were analyzed by paper chromatography as shown in Fig. 4, it was possible to show that fractions preceding the peak were rich in these new glycosides. By collecting such fractions and separating them by paper chromatography as shown in Fig. 1, one can isolate the four new glycosides in pure form. Table 2 compares the chromatographic behavior of these glycosides to that of hygromycin A. Like hygromycin A, they are all white amorphw ous substances. Compounds D and E yield N crystalline 2,4-dinitrophenylhydrazones which 0 have melting points of 140 to 142 C and 154 to z 156 C, respectively. Mixed melting points with the N 2,4-dinitrophenylhydrazone of hygromycin A are depressed. DIscussIoN It has been found that many antibiotic-producing organisms have the capacity of forming, in (~Q - KNOWN * HYGROMYCIN A * * * v * * 0-61 F. FIG. 4. Chromatographic analysis offractions from charcoal-dicalite columns. Column fractions were subjected to paper chromatography in solvent IX. Compounds were detected with diazotized p-nitroaniline (fractions 130 to 160 constituted the peak tubes). TABLE 2. Compound Chromatographic behavior of hygromycin A and related glycosides* Solvent systemst x Ix II XI XII Hygromycin A Hygromycin C Compound D Compound E Compound F * Results are expressed as the ratios of the indicated compounds to hygromycin A. t Compounds were detected with diazotized p- nitroaniline. Solvent systems are described in the text. 9
5 608 ELBEIN ET AL. LJ. EtAcmmm. the same medium and at the same time, several different antibiotics or various chemical modifications of the same antibiotic. As many as five to seven different, though chemically related, antibiotics have been found in the culture medium of one organism (19). In the case of S. hygroscopicus, two distinct antibiotic types have been isolated from the culture medium. The data presented here indicate that several additional compounds, structurally related to one of these types, in this case hygromycin A, are also produced during the culture process. Studies on the structure of these four new glycosides will be the subject of a future communication. ACKNOWLEDGMENT This investigation was supported by grant G from the National Science Foundation. LITERATURE CITED 1. BIDWELL, R. G. S., G. KROTKOV, AND G. B. REED Paper chromatography of sugars in plants. Can. J. Botany 30: BLAND, D. E Separation of vanillin and syringaldehyde by paper partition chromatography. Nature 164: BRAY, H. G., W. V. THORPE, AND K. WHITE The fate of certain organic acids and amides in the rabbit. Biochem. J. 46: DISCHE, Z., AND L. B. SHETTLES A specific color reaction of methylpentoses and a spectrophotometric micromethod for their determination. J. Biol. Chem. 175: DREYWOOD, R Qualitative test for carbohydrate material. Ind. Eng. Chem. (Anal. Ed.) 18: ELBEIN, A. D., R. L. MANN, H. E. RENIS, W. M. STARK, H. KOFFLER, AND H. R. GARNER The conversion of D-glucose to 5-keto-6-deoxy- D-arabohexose. J. Biol. Chem. 236: FOLIN, O., AND V. CIOCALTEU On tyrosine and tryptophane determinations in proteins. J. Biol. Chem. 73: GREEN, M., AND S. S. COHEN Enzymaticconversion of L-fucose to L-fuculose. J. Biol. Chem. 219: HOLOWCZAK, J. A., H. KOFFLER, AND H. RV GARNER Glycosides produced by Streptomyces hygroscopicus. Plant. Physiol. 38adii. 10. ISONO, K., S. YAMASHITA, Y. TOMIYAMA, AND S. SUZUKI Studies on homomycin. J. Antibioties (Tokyo) Ser. A 10: MANN, R. L., AND W. W. BROMER The isolation of a second antibiotic from Streptomyces hygroscopicus. J. Am. Chem. Soc. 80: MANN, R. L., R. M. GALE, AND F. R. VAN ABEELE Hygromycin. II. Isolation and properties. Antibiot. Chemotherapy 3: MANN, R. L., AND D. 0. WooLF Hygromycin. III. Structure studies. J. Am. Chem. Soc. 79: MOORE, S., AND W. H. STEIN A modified ninhydrin reagent for the photometric determination of amino acids and related compounds. J. Biol. Chem NAMIKI, M., K. ISONO, ANm S. SuZUKI Studies on homomycin. V. Degradation and structure. J. Antibiot. (Tokyo) 1OA: PATRICK, J. B., R. P. WILLIAMS, C. W. WALLER, AND B. L. HuTCHINGS A new inosamine from an antibiotic. J. Am. Chem. Soc. 78: TREVELYAN, W. E., D. P. PROCTER, AND J. S. HARRISON Detection of sugars on paper chromatograms. Nature 166: WALDRON, D. M Sugar components of blood and urinary glycoproteins: confirnation of the presence of fucose by a new reaction. Nature 170 : WAKSMAN, S. A., AND H. A. LECHEVALIER The actinomycetes, vol. 3, chapter 4. The Williams & Wilkins Co., Baltimore.
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