Microbial Conversion of Acetanilide to 2'-Hydroxyacetanilide and
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1 APPLm MICROBIOLOGY, Nov. 1967, p Vol. 15, No. 6 Copyright 1967 American Society for Microbiology Printed in U.S.A. Microbial Conversion of Acetanilide to 2'-Hydroxyacetanilide and 4'- Hydroxyacetanilide ROBERT J. THERIAULT AND THOMAS H. LONGFIELD' Department ofmicrobial Chemistry, Abbott Laboratories, North Chicago, Illinois Received for publication 22 June 1967 Approximately 700 cultures of various types were examined for their ability to hydroxylate acetanilide. The major product formed by unidentified Streptomyces species RJTS-539 was identified as 4'-hydroxyacetanilide (N-acetyl-p-aminophenol). This culture gave a peak yield of 405 mg per liter from 1,000 mg of acetanilide per liter. Considerably lower yields of 4'-hydroxyacetanilide were isolated from S. cinnamoneus NRRLB The major conversion product of acetanilide formed by Amanita muscaria F-6 was identified as 2'-hydroxyacetanilide, with a peak yield of 433 mg per liter from 1,000 mg per liter of substrate. A small amount of 4'-hydroxyacetanilide was also formed. Six other Streptomyces cultures formed small amounts of one or two products identical or similar to 2'-hydroxyacetanilide or 4'-hydroxyacetanilide as determined by thin-layer chromatography and ultraviolet spectra. The conversion of acetanilide to 4'-hydroxyacetanilide (N-acetyl-p-aminophenol) in mammalian systems has been reported by Michel, Bernheim, and Bernheim (5) for the rat. Lester and Greenberg (4) and Brodie and Axelrod (1) have shown that in man acetanilide is converted to 4'-hydroxyacetanilide, followed by conjugation with sulfuric acid and glucuronic acid at the hydroxyl group. Brodie et al. (2) were successful in hydroxylating acetanilide in the 2' and 4' positions with their model system consisting of ascorbic acid, ferrous iron, ethylenediaminetetraacetic acid (EDTA), and oxygen. The hydroxylation of acetanilide by microorganisms, however, has not been reported. This investigation was carried out to determine whether microorganisms could likewise hydroxylate acetanilide, preferably in the 4' position. MATERIALS AND METHODS Cultures. The cultures used in this investigation included approximately 300 identified and unidentified mold, actinomycete, and basidiomycete stock cultures, plus over 400 actinomycetes isolated from soils. Screening medium. Initial screening in shaken tubes and shaken flasks was carried out in a medium con- 1Present address: Department of Organic Chemistry, Georgia Institute of Technology, Atlanta, Ga sisting of 5% glucose monohydrate (added after sterilization), 0.5% soybean flour, 0.5% yeast extract, plus variable levels of KH2PO4, K2HPO4, and NaCI. Agitation. A Gump rotary shaker (260 rev/min) was used for all fermentation studies. Method of analysis. Analysis of total phenol-positive products was done by use of a modification of the ferric chloride-ferricyanide procedure (3). Although the reagent is not completely specific under the conditions used, it is sensitive and positive for many phenolic compounds. Samples of 0.25 ml of the centrifuged fermentation beer supernatant fluids were pipetted to test tubes (13 X mm). Two drops of 2 N H2SO4 were added to each tube, followed by 0.25 ml of the phenol detection reagent [1% aqueous FeCI3-1% aqueous K3Fe(CN)6, 1:1]. A series of 4'-hydroxyacetanilide standards of, 250, 500, and 1,000 jg/ml was also treated with equal amounts of the reagents. The blue color indicative of phenolic compounds was allowed to develop in the standards and sample tubes, after proper mixing, for 15 min. A 6-ml amount of deionized water plus 0.1 ml of 10% oxalic acid was then added to each tube and thoroughly mixed. The blue color in the supernatant beer samples was then visually compared with the 4'-hydroxyacetanilide standards to obtain an approximation of the level of phenolic products. Chromatography. A 10-ml amount of the whole culture fermentation liquors was adjusted to ph 6 and extracted twice with 4 volumes of ethyl acetate. The ethyl acetate extracts were evaporated to dryness under vacuum, and the residues were dissolved in 2 ml of methanol. The methanol extracts were chromatographed (200,lAiters) on Whatman no. 1 paper by 1431
2 14 THERIAULT AND LONGFIELD APPL. MICROBIOL. the ascending technique in a solvent system consisting of benzene-glacial acetic acid-water-n-butanol (38: 38:17:7). After development, the chromatograms were scanned with ultraviolet light and sprayed with the phenol detection reagent [1% aqueous FeCl3-1% aqueous K3Fe(CN)6, 1 :1]. Thin-layer chromatography was the preferred method used in this study. The previously described methanol solutions of the ethyl acetate extracts were spotted on glass plates (20 X 20 cm) coated with Merck Silica Gel GF, 500 IA in thickness. The plates were developed in a solvent system consisting of chloroform-95% aqueous methanol-nh40h (85:15:1). After 30 to 45 min of developing time, the plates were air-dried and scanned with ultraviolet (UV) light. The plates were then photographed with UV light (2,537 A) by use of a Polaroid Land Camera with no. 107 film. The Silica Gel GF plates were then sprayed with 2 N H2SO4, followed by an aqueous solution of 1% FeClr1% K3Fe(CN)6 (1:1). Phenolic products were revealed as intense blue spots on a pale yellow background, changing to pale blue with age. Product isolation. Selected cultures that formed major conversion products similar or identical to 2'-hydroxyacetanilide or 4'-hydroxyacetanilide by thinlayer chromatography RF or UV spectra were grown in shaken flasks ( ml/500-ml flask) in 5-liter quantities to permit isolation and identification of the products. The fermentations were sampled regularly for solvent extraction and thin-layer chromatography, and were harvested at the optimal age. The pooled harvested beer was adjusted to ph 7 and extracted twice with 4 volumes of ethyl acetate. The ethyl acetate extract was then evaporated to dryness under vacuum. For the isolation of 4'-hydroxyacetanilide, the residue was reconstituted in chloroform-methanol (99:1). This solution was added to a glass column packed withph 4 activity no. 1 (Brockmann) alumina. The product was developed and eluted with increasing amounts of methanol in the chlorofonn developing solution. The 4'-hydroxyacetanilide fractions were pooled, evaporated to dryness, and dissolved in methanol. This solution was decolorized with Darco G-60 carbon and filtered. The product was finally cystallized by the addition of chloroform. For the isolation of 2'-hydroxyacetanilide along with small amounts of 4'-hydroxyacetanilide, the residue from the ethyl acetate extract was dissolved in methanol. The products were then isolated by preparative thin-layer chromatography. The entire methanol solution was streaked on a series of Silica Gel GF thin-layer plates (20 X 20 cm). The plates were developed in the previously described system, and the products were eluted from the silica gel with methanol. The methanol solutions were filtered, and the products were crystallized; this was followed by recrystallization from hot acetone. Instrwnentation. UV spectra were determined with a Cary model 11 recording spectrophotometer. Infrared (IR) spectra were obtained with a Perkin-Elmer model 421 spectrophotometer. Nuclear magnetic resonance (NMR) spectra were determined with a Varian A-60 high-resolution spectrometer. Melting points were determined with a Kofler Micro Hot Stage melting-point apparatus. Synthetic standards. 2'-Hydroxyacetanilide was obtained from Eastman Organic Chemicals, Rochester, N.Y. The 4'-hydroxyacetanilide was prepared by the reduction of p-nitrophenol in 20% acetic acid with hydrogen followed by acetylation with acetic anhydride. The product was then crystallized from deionized water. RESULTS AND DISCUSSION Approximately 300 identified and unidentified mold, actinomycete, and basidiomycete stock cultures, plus over 400 additional actinomycetes isolated from soils for this investigation, were screened in shaken tubes and shaken flasks for their ability to hydroxylate acetanilide. The medium consisted of 5% glucose monohydrate, 0.5% soybean flour, 0.5% yeast extract, plus variable amounts of KH2PO4, K2HP04, and, depending on the desired initial ph. All cultures were inoculated from agar slants and then placed on the Gump rotary shaker for 48 hr. At that time, acetanilide was added at a level of 1,000 mg/liter in powdered form to all cultures, which were then again placed on the shaker. Samples were taken during the fermentation for the determination of total phenolic products. With the volumes of sample and reagents used, it was possible to screen a large number of cultures rapidly without resorting to time-consuming solvent extraction or to paper or thin-layer chromatography. Those cultures which yielded a total phenols blue color equivalent to 200 Ag or more of 4'-hydroxyacetanilide per ml were investigated further. The fermentation beers were extracted with ethyl acetate, as previously described, concentrated, and chromatographed, preferably by thinlayer chromatography. Thin-layer Silica Gel GF plates were scanned with UV light and sprayed with 2 N H2SO4 followed by the phenol detection reagent. Extracts of those cultures which showed one or more products with an RF similar to one of the hydroxylated analogues of acetanilide were streaked by the preparative thin-layer chromatography method at higher levels on Silica Gel GF plates (20 X 20 cm). After development, the products were eluted in methanol and the UV spectra were determined. Nine cultures, which gave a high level of total phenolic products and which by either paper or thin-layer chromatography showed a strong UVabsorbing and phenol-positive product with an RF similar to 2'- or 4'-hydroxyacetanilide were grown in shaken flasks. The cultures are shown in Table 2. The respective media used are listed in Table 1. Flasks were inoculated from agar slants and were incubated at 28 C on a Gump rotary shaker at 260 rev/min. The susbtrate, acetanilide, was added at a level of 500 mg/liter
3 VOL. 15, 1967 MICROBIAL CONVERSION OF ACETANILIDE 1433 TABLE 1. Media used" Ingredient Amt (g/liter) 1 2 Glucose monohydrateb Soybean grits Soybean flour..5.0 Yeast extract Malt extract KH2PO K2HP Initial ph Water... Tap Tap a Conditions were as follows: volume per flask, unless otherwise specified, ml/500-ml Erlenmeyer flask; sterilization, 35 min at 120 C and 15 psi of pressure; aeration, cotton plug. b Glucose monohydrate was added after sterilization of the media. TABLE 2. at 48 and 168 hr. Flasks were sampled at 192, 264, 336, and 4 hr for solvent extraction, concentration, and thin-layer chromatography. Figure 1 is a Polaroid Land Camera photograph of a thin-layer plate exposed with UV light (2,537 A), showingthe UV-absorbingproductsproduced by the cultures at their peak yields. The plate in this case was developed twice for 30 min. The standards (,ug each) found in position 6 are 4'-hydroxyacetanilide (RF = 0.47), 3'-hydroxyacetanilide (RF = 0.52), 2'-hydroxyacetanilide (Rp = 0.72), and acetanilide (RF = 0.82) in ascending order. Figure 2 shows the same plate after it was sprayed with 2 N H2S04 followed by 1% aqueous FeCb3-1 % aqueous K3Fe(CN)6 (1:1). The 3'-hydroxyacetanilide standard is considerably less sensitive to the spray than 2'- and 4'- hydroxyacetanilide, and is barely discernible in the photograph. All of the cultures produced a UV-absorbing product positive to the phenol detection reagent with an RF quite close to that of 4'-hydroxyacetanilide. Three cultures, Streptomyces eurocidicus NRRLB-1676, S. griseolus ATCC-35, and Amanita muscaris F-6, in addition, formed detectable amounts of a product similar to 2'-hydroxyacetanilide. As seen in Table 2, the Cary UV spectrum of the 4'-hydroxyacetanilide-like product from each culture eluted from thin-layer plates showed a maximum of approximately 248 m,u and a shoulder at 290 m,u, and was thus identical to synthetic 4'-hydroxyacetanilide. Further, the shape of the curves was identical to synthetic 4'-hydroxyacetanilide for all cultures. Amanita muscaria F-6 and S. griseolus ATCC-35, as previously stated, formed a 2'-hydroxyacetanilide-like product by thin-layer chromatography RF. The absorption maxima and shape of the UV absorption curves were essentially identical to 2'-hydroxyacetanilide. The UV spectrum of this product produced by Streptomyces eurodicus NRRLB-1676 showed only one maximum, which matched 2'-hydroxyacetanilide, the other being obscured by an impurity. On the assumption that the products actually Comparison of cultures producing major phenolic products when grown in the presence of acetanilide No. Culture ~~Me- Thin-layer chromatography Maximal yield No. Culture diuma Absorption max- 2'-Hydroxy 4'-Hydro products" ctnld ctnld Rpr ima of eluted Age acetydroxy- acetydroxy-ye ma hr mg/liter mg/ liter 1 Streptomyces albireticuli NRRLB , 290 (S) S. cinnamoneus NRRLB , 290(S) S. eurocidicus NRRLB , 290(S) S. griseolus ATCC , 290(S) , S. luteoverticillatus NRRLB , 290(S) S. roseochromogenes ATCC , 290(S) S. scabies ATCC , 290(S) Unidentified Streptomyces species RJTS , 290(S) Amanita muscaria F , 288(S) , a See Table 1. b The UV spectrum of synthetic 4'-hydroxyacetanilide shows a maximum at 248 m,a (S) at 290 mp. Synthetic 2'-hydroxyacetanilide shows two maxima at 243 and 284 mu. and a shoulder
4 1434 THERIAULT AND LONGFIELD APPL. MICROBIOL w:w y ww W w FiG. 1. Thin-layer plate of UV-absorbing products formed by cultures used in this investigation. (1) Streptomyces albireticuli NRRLB-1670; (2) S. cinnamoneus NRRLB-1285; (3) S. eurocidicus NRRLB-1676; (4) S. griseolus ATCC-35; (5) S. luteoverticillatus NRRLB-1995; (6) synthetic standards, in ascending order, 4'-hydroxyacetanilide (RF = 0.47), 3'-hydroxyacetanilide (Rp = 0.52), 2'-hydroxyacetanilide (RF = 0.72), and acetanilide (RF = 0.82); (7) S. roseochromogenes ATCC-3347; (8) S. scabies ATCC- 3352; (9) unidentified Streptomyces species RJTS-539; (10) Amanita muscaria F-6. were 2'-hydroxyacetanilide and 4'-hydroxyacetanilide, yields were determined at all sampling ages. The maximal yields are cited in Table 2. The unidentified Streptomyces species RJTS-539 gave the highest yield of 4'-hydroxyacetanilide of 1 mg/liter from 1,000 mg of acetanilide per liter, representing an 11.8% conversion. This culture was originally isolated from soil. Taxonomic studies indicated that this culture is a new Streptomyces species (T. J. Oliver, unpublished data). The basidiomycete A. muscaria F-6 gave the highest yield of 2'-hydroxyacetanilide of 433 mg/ liter from a total of 1,000 mg/liter of substrate, representing a 38.7% conversion. To verify structure of both 2'-hydroxyacetanilide and 4'-hydroxyacetanilide, three cultures (A. muscatia F-6, unidentified Streptomyces species RJTS-539, and S. cinnamoneus NRRLB-1285) were grown again in shaken flasks. Five-liter quantities were harvested at the optimal age. The products were then isolated, crystallized, and analyzed. The major crystalline product isolated from A. muscaria F-6 as 2'-hydroxyacetanilide was positive to the phenol detection reagent and was identical to synthetic 2'-hydroxyacetanilide by thinlayer chromatography and UV spectrum. The product gave a melting point (mp) of 207 to 209 C (cor) and the mixture with an authentic sample of 2'-hydroxyacetanilide, mp 209 C (cor), had a mp of 208 to 209 C (cor). The elemental analysis was as follows. Analysis: C8H9NO2; calculated: C, 63.56; H, 6.00; N, 9.27; 0, 21.17; found: C, 63.87; H, 6.28; N, 9.77; 0, The IR spectrum determined in a Nujol mull and the NMR spectrum determined in deuterated dimethylsulfoxide (DMSO) were identical to synthetic 2'-hydroxyacetanilide. The minor product isolated from A. muscaria F-6 was identical to synthetic 4'-hydroxyacetanilide by the phenol detection spray, thin-layer chromatography RF, UV spectrum, and by NMR spectrum as determined in deuterated acetone. The 4'-hydroxyacetanilide-like product isolated from unidentified Streptomyces species RJTS-539 was identical to synthetic 4'-hydroxyacetanilide by RF on thin-layer plates and by UV spectrum. The product gave mp 168 to 170 C (cor), and the mixture with an authentic sample of 4'-hydroxyacetanilide, mp 169 to 170 C (cor), had a mp FIG. 2. Thin-layer plate of phenol-positive products formed by cultures used in this investigation. This plate was sprayed with 2 X H2S04 followed by 1% aqueous FeCI3-1% aqueous K3Fe (CN)6 (1:1). (1) Streptomyces albireticuli NRRLB-1670; (2) S. cinnwnoneus NRRLB- 1285; (3) S. eurocidus NRRLB-1676; (4) S. griselous ATCC 35; (5) S. luteoverticillatus NRRLB-1995; (6) synthetic standards, in ascending order, 4'-hydroxyacetanilide (RF = 0.47), 3'-hydroxyacetanilide (RF = 0.52), and 2'-hydroxyacetaniide (RF = 0.72); (7) 5. roseochromogenes ATCC-3347; (8) S. scabies ATCC-3352; (9) unidentified Streptomyces species RJTS-539; (10) Amanita muscaria F-6. Am..,
5 VOL. 15, 1967 MICROBIAL CONVERSION OF ACETANILIDE 1435 TABLE 3. Comparison of some factors affecting the conversion of acetanilide to 4'-hydroxyacetanilide by unidentified Streptomyces species RJTS-539a No Vol of basal Temp medium per 500- ml flask C ml Deletions Soybean grits Soybean grits Glucose monohydrate Medium variations Additions FeSO4-7H20, 25 mg/liter Citric acid, 500 mg/liter FeSO4-7H20, 50 mg/liter Citric acid, 500 mg/liter Soybean flour, 5 g/liter Soybean flour, 5 g/liter FeSO4 *7H20, 50 mg/liter Citric acid, 500 mg/liter Starch, 50 g/liter a Conditions were as follows: basal medium was medium 1 (Table 1); aeration, cotton plugged flasks; inoculum, agar slant culture per flask; agitation, Gump rotary shaker (260 rev/min); substrate, 0.1% acetanilide powder was added to all flasks at 48 hr. to 170 C (cor). The product analyzed as follows. Analysis: C8H9N02; calculated: C, 63.56; H, 6.00; N, 9.27; 0, 21.17; found: C, 63.50; H, 6.15; N, 9.34; 0, The Nujol mull IR spectrum and NMR spectrum in deuterated DMSO wert identical to the synthetic 4'-hydroxyacetanilide. The similar product isolated and crystallized from S. cinnamoneus NRRLB-1285 was also identical to synthetic 4'-hydroxyacetanilide by all of the above criteria. Unidentified Streptomyces species RJTS-539 was investigated in shaken flasks under a variety of conditions to increase the yield of 4'-hydroxyacetanilide. The results of some of the conditions investigated are shown in Table 3. All variables were investigated in duplicate flasks, and all analyses for 4'-hydroxyacetanilide were determined on pooled samples. All values were also corrected to 0-hr volume. As the data indicate, the yield of 4'-hydroxyacetanilide was increased from 138 mg/liter at 28 C to 272 mg/liter at C with ml of medium. Yields were further improved by the addition of FeSO4.7H20 at a level of 25 or 50 mg/liter with citric acid as the chelating agent. The highest yield of 405 mg/liter was obtained by removal of from the medium and the substitution of soybean 4' Hydroxyacetanilide yield at 234 hr mg/liter flour for soybean grits. The conversion rate was sharply reduced when starch was substituted for glucose monohydrate. A number of other conditions led to greatly reduced yields of 4'-hydroxyacetanilide by unidentified Streptomyces species RJTS-539. They included the substitution of sucrose in place of glucose monohydrate as a carbon source and the use of EDTA in place of citric acid as a chelating agent. NH4NO3 and urea were not suitable nitrogen sources. In still another experiment where the acetanilide substrate was added from a 40% DMS0 solution the maximal yield was reduced approximately 40%. 4'-Hydroxyacetanilide, then, was isolated as a major microbial conversion product of acetanilide from unidentified Streptomyces species RJTS Smaller amounts were isolated from Streptomyces cinnamoneus NRRLB-1285 and Amanita muscaria F-6. 2'-Hydroxyacetanilide was the major conversion product formed by Amanita muscaria F-6. Six other Streptomyces formed small quantities of one or two products identical or similar to 2'-hydroxyacetanilide or 4'-hydroxyacetanilide by thin-layer chromatography and UV spectra. 62
6 1436 THERIAULT AND LONGFIELD APPL. MICROBIOL. LiTERATuRE C1TED 1. BRODE, B. B., AND J. AXELROD The fate of acetanilide in man. J. Pharmacol. Exptl. Therap. 94: BRODiE, B. B., J. AXELROD, P. A. SHORE, AND S. UDENFRIEND Ascorbic acid in aromatic hydroxylation. II. Products formed by reaction of substrates with ascorbic acid, ferrous iron and oxygen. J. Biol. Chem. 208: HATHWAY, D. E Plant phenols and tannins, p. 4. In I. Smith [ed.], Chromatographic and electrophoretic techniques, vol. 1. Wm. Heinemann Medical Book Ltd, London. 4. LESTER, D., AND L. A. GREENBERG The metabolic fate of acetanilid and other aniline derivatives. IT. Major metabolites of acetanilid appearing in the blood. J. Pharnacol. Exptl. Therap. 90: MicHEL, H. O., F. BERNHEIM, AND M. L. C. BERNHEIM The hydrolysis of acetanilide by various tissues. J. Pharmacol. Exptl. Therap. 61:1-7. Downloaded from on October 13, 2018 by guest
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