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Capsular Polysaccharide of Azotobacter Agilis' Gary H JOURNAL OF BACTERIOLOGY Vol. 88, No. 6, p. 1695-1699 Decemnber, 1964 Copyright © 1964 American Society for Microbiology Printed in U.S.A. CAPSULAR POLYSACCHARIDE OF AZOTOBACTER AGILIS' GARY H. COHEN2 AND DONALD B. JOHNSTONE Department of Agricultural Biochemistry, University of Vermont, Burlington, Vermont Received for publication 19 June 1964 ABSTRACT is confined to well-defined capsules. To our COHEN, GARY H. (University of Vermont, Bur- knowledge, no reports have appeared in the lington), AND DONALD B. JOHNSTONE. Capsular literature concerning the chemistry of the extra- polysaccharide of Azotobacter agilis. J. Bacteriol. cellular polysaccharide of A. agilis. 88:1695-1699. 1964.-Capsular polysaccharide from Azotobacter agilis strain 132 was recovered from MATERIALS AND METHODS washed cells by alkaline digestion. The polysac- Growth of the organisms. A. agilis (ATCC charide was purified by centrifugation, repeated 12838) used alcohol precipitation, Sevag deproteinization, and throughout this study was originally treatment with ribonuclease and charcoal-cellu- isolated in this laboratory from water (Johnstone, lose. Methods of isolation and purification ap- 1957) and designated in subsequent reports as peared to provide a polymer showing no evidence strain 132 (Johnstone, Pfeffer, and Blanchard, of heterogeneity when examined by chemical and 1959; Johnstone, 1962b). Burk's nitrogen-free physical methods. Colorimetric, paper chromato- broth (Wilson and Knight, 1952) at pH 7.0 graphic, and enzymatic analyses on both intact supplemented with 2% sucrose was inoculated and acid-hydrolyzed polysaccharide indicated with cells growing in the logarithmic phase. that the polymer contained galactose and rham- Cultures were incubated at 31 C in 7.5-liter New nose at a molar ratio of approximately 1.0:0.7. A Brunswick fermentors with sterile moist air sialic acid-like component was also present in the polysaccharide. The study shows significant dif- supplied at the rate of 4 liters per min and an ferences in the chemical composition of the extra- impeller rotation of 130 rev/min. Incubation cellular polysaceharide of A. agilis and that of A. was discontinued after 72 hr. vinelandii. This adds further biochemical evidence Isolation and purification of polysaccharide. for the right of these species to independent status. The cells were harvested by centrifugation in a Servall continuous-flow centrifuge at 10,000 X g, Recently, we have been interested in the extra- washed in 0.05 M phosphate buffer (pH 7.3), cellular polysaccharides synthesized by Azoto- treated with 1% (v/v) formaldehyde (Dudman bacter vinelandii (Cohen and Johnstone, 1964). and Wilkinson, 1956) for 15 min, and suspended It was of interest, therefore, to extend the study in 0.1 N NaOH for 1 hr on a rotary shaker at to the capsular material of A. agilis and compare room temperature to remove the capsules. The it with that of A. vinelandii. Such information digest was then centrifuged at 10,000 X g for may provide additional help in the differentiation 1 hr and neutralized with HCl; the sedimented of these frequently confused species, the distin- cell mass was discarded, and the supernatant guishing characteristics of which have been fluid was added to 4 volumes of cold ethanol. reviewed (Johnstone, 1962a). Although the The presence of electrolyte (NaCl) was required extracellular polysaccharides of A. vinelandii are for precipitation of A. agilis capsular polysac- found as both cell-free slime and capsular mate- charide. The polysaccharide was purified by rial, the extracellular polysaccharide of A. agilis three additional alcohol precipitations followed by 17 Sevag deproteinization cycles, as outlined ' From a dissertation submitted by the senior previously (Cohen and Johnstone, 1964). author in partial fulfillment of the requirements Ribonucleic acid (RNA) was indicated in the for the Ph.D. degree. Contribution from the Uni- versity of Vermont Agricultural Experiment Sta- polysaceharide preparation by strong absorption tion, Journal Article No. 142. at 260 m,u and the presence of ribose, as shown 2 Present address: Department of Veterinary by paper chromatography of acid hydrolysates. Biology, School of Veterinary Medicine, Univer- RNA was removed by incubating the preparation sity of Pennsylvania, Philadelphia. with ribonuclease (Worthington Biochemical 1695 1696 COHEN AND) JOHNSTONE J. BACTERIOI,. Corp., Freehold, N.J.) in 0.1 M acetate buffer at by the Nelson modification (1944) of Somogyi pH 5.0 for 1 hr at 37 C. The mixture was dialyzed (1952). The hydrolysate was evaporated to against 0.1 M acetate buffer, until no ultraviolet dryness under reduced pressure and redissolved; absorption at 260 m,u was observed. The poly- the procedure was repeated four times to remove saccharide was passed through a charcoal-cellu- HCl. lose pad (Cifonelli and MIayeda, 1957) to remove remaining ultraviolet-absorbing material, dia- RESULTS lyzed against distilled water, and precipitated The cells of A. agilis 132 were surrounded by with ethanol and NaCl. The precipitate was a well-defined capsule, but cell-free slime, as washed successively in 80% ethanol, absolute found with A. vinelandii, was not produced. ethanol, and acetone, and dried in vacuo at room Because the slime-synthesizing capacity of some temperature. bacteria depends much upon cultural conditions Homogeneity of A. agilis polysaccharide was (Anderson and Rogers, 1963), several attempts determined in a Spinco model E ultracentrifuge were made to induce slime production in A. at 52,640 rev/min. Spectrophotometric measure- agilis. Cells were grown in Burk's broth supple- ments were performed in a Beckman model DU mented with high concentrations (1 to 20%, w/v) spectrophotometer. of glucose, fructose, or sucrose. Slime was not Hexuronic acid was determined by the carba- detected in the culture supernatant fluid by zole test (Dische, 1947), methylpentose by the acid or alcohol precipitation, nor was free slime L-cysteine-sulfuric acid test (Dische and Shettles, observed microscopically by India ink negative 1948), hexose by the primary L-cysteine-sulfuric staining (Duguid, 1951). acid method (Dische, Shettles, and Osnos, 1949), The capsular polysaccharide was isolated as a and sialic acid by the thiobarbituric acid method flocculent light-brown material. Purified poly- (Warren, 1959) and the modified Ehrlich test saccharide was white, and, although readily (Barry, Abbott, and Tsai, 1962). The standards soluble in water at high concentrations (10 mg/ were L-rhamnose, D-galactose, and N-acetyl- ml), it produced solutions of low viscosity. neuraminic acid, respectively. A purified sample The homogeneity of the highly purified poly- of N-acetylneuraminic acid isolated from bo- saccharide was examined by ultracentrifugation vine submaxillary gland was the gift of R. (Fig. 1). Although this method strongly indicated C. Woodworth, University of Vermont. the polysaccharide to be homogeneous in com- Quantitative estimation of the sugar moieties position, further studies are required for confirma- of the polysaceharide, as well as methods for tion. The sharpness of the sedimentation pattern detection of protein, were as previously described suggested a relatively narrow distribution of (Cohen and Johnstone, 1964). molecular weight species for the polymer. The Chromatography. Paper chromatography was ultraviolet spectrum of a 0.1 % (w/v) aqueous carried out by the descending technique on solution of polysaceharide revealed no maxima Whatman 3 MM paper. The following solvent in the region of 230 to 300 m,u, indicating removal systems were used: (i) n-butanol-pyridine-water of the RNA, and protein was not found by the (9:5:8, v/v); (ii) ethyl acetate-pyridine-water method of Lowry et al. (1951). (12:5:4, v/v); (iii) isopropanol-butanol-water Paper chromatography of acid hydrolysates (14:2:4, v/v); (iv) ethyl acetate-pyridine-acetic (Table 1) revealed two major components which acid-water (5:5:1:3, v/v). The sugars were were identified by the following methods as located with aniline hydrogen phthalate (Part- galactose and rhamnose. Rhamnose was indicated ridge, 1949), aniline diphenylamine (Smith, as one component of the polysaccharide on the 1958), glucose oxidase, and galactose oxidase basis of chromatographic evidence, identical reagents (Worthington Biochemical Corp., Free- color reactions with developing sprays, and a hold, N.J.) (Salton, 1960), and 0.2% (w/v) positive L-cysteine-sulfuric acid test of Dische ninhydrin in acetone for amino sugars. and Shettles (1948). The identical absorption Acid hydrolysis. Acid hydrolyses were carried spectra for unhydrolyzed polysaccharide, a out in Teflon-lined screw-capped tubes with 1 N fraction isolated from an acid hydrolysate, and an HCl at 100 C for 1 hr. A time course was run to authentic sample of L-rhamnose are illustrated obtain maximal reducing values, as determined in Fig. 2. Galactose was indicated on the basis l'OL. 88, 1964 CAPSULAR POLYSACCHARIDE OF A. AGILIS 1697 of chiromatographic evidence, identical color reactions with developing sprays, and a positive 0.5 - primary L-eysteine-sulfuric acid test. Figure 3 illustrates the identical absorption spectra for A unhydrolyzed polysaceharide, a fraction isolated from an acid hydrolysate, and an authentic H04 z 0 0.3- O.-Jm 0- 0 0.1 . 350 375 400 425 450 FIG. 2. Absorption spectrafor intact extracellular polysaccharide of Azotobacter agilis (A), rhamnose (B), and a fraction isolated front a polysaccharide hydrolysate (C), in the
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