STUDIES OF CRYPTOCOCCUS POLYSACCHARIDES BY INFRARED SPECTROPHOTOMETRY

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1 STUDIES OF CRYPTOCOCCUS POLYSACCHARIDES BY INFRARED SPECTROPHOTOMETRY SEYMOUR LEVINE, E. EDWARD EVANS, AND PAUL W. KABLER From the St. Francis Hospital, Jersey City, New Jersey; the University of Alabama Medical Center, Birmingham, Alabama; and the Robert A. Taft Sanitary Engineering Center, U. S. Public Health Service, Cincinnati, Ohio Infrared spectrums of isolated capsular polysaccharides have been used to segregate types within certain groups of encapsulated bacteria. The results of spectral typing of purified pneumococcal polysaccharides (1) and of crude klebsiella polysaccharides (2) have paralleled the results of serological typing. In a few cases the spectral method was less sensitive, so that certain serological types could not be differentiated. In a few cases the spectral method was more sensitive in differentiating strains than standard capsular reactions and agglutination tests, and in these cases the subtypes established by spectral analysis received serological confirmation by the more refined method of capsular reactions with reciprocally absorbed serums (2). In the present study, the technique of infrared spectrophotometry has been applied to the yeast-like fungus, Cryptococcus neoformans. Strains of C. neoformans have been divided into three types by capsular, agglutination, and precipitin reactions (3, 4). The purpose of this report is to compare the infrared spectral analysis of purified cryptococcal capsular polysaccharides with the serological data. MATERIALS AND METHODS Cultures of C. neoformans were grown in neopeptone dialysate broth with constant agitation (5). In one instance, a type A culture was grown in a casein hydrolysate medium (ph 7) of the fol- Received for publication October 28, Supported in part by a research grant from the National Institutes of Health, Public Health Service. 269 lowing composition: Casein hydrolysate-acid (Nutritional Biochemicals Co.) Glucose Yeast extract (dialysate) 1.0% (vjv) 2.0% 0.1% Cell-free filtrates (5) of cultures were acidified by the addition of glacial acetic acid to give a final concentration of 1% (v/v). Following this, sodium acetate crystals (% w/v) were dissolved by stirring. The ph at this point was 5.3 to 5.4. The capsular polysaccharide (S) was precipitated by the addition of ethanol. Varying quantities were necessary to effect precipitation. Type A polysaccharide (SA) generally required from 1.5 to 2.0 volumes of ethanol. Type B (SB) precipitated with 0.6 to 0.9 volumes. Type C polysaccharide (SC) generally precipitated with 0.5 to 0.6 volumes. The S precipitate was then dissolved in water together with additional acetic acid and sodium acetate and the precipitation with ethanol was repeated as before from two to five times. Certain samples were subjected to other procedures before the final ethanol precipitation. A number of samples (see table 1) were freed from traces of protein by Sevag's method (4, 6). One type B preparation was precipitated initially with 2.5 volumes of ethanol (SB8); since this material was contaminated with fraction R it was further purified by precipitation with lead acetate (5). The S fraction precipitated while R remained in the supernate. This lead-precipitated material was also treated by Sevag's method and is referred to as SB1 in the table. The lead was removed by electromigration (5). Most S preparations have been given a final ethanol precipitation in the presence of sodium acetate and acetic acid, then rinsed with ethanol and ether on hard filter paper and desiccated. This procedure resulted in a high ash value (5) and necessitated a correction for sodium content when weighing. More recently, the final aqueous solution of the polysaccharide has been dialyzed against cold distilled water and lyophilized. The samples were dissolved in distilled water and air dried on the surfaces of silver chloride discs that were slightly tilted so as to produce wedge-shaped films of variable thickness (8). The spectrums were recorded automatically by a Perkin-Elmer model 21 double beam infrared Downloaded from at Penn State University (Paterno Lib) on May, 2016

2 270 SEYMOUR LEVINE, E. EDWARD EVANS, AND PAUL W. KABLER TABLE 1 Sample Strain Methods of purification Absorbance Absorbance Absorbance ratio 5.85 I' 6.25 I' 5.851'/6.25 I' SA2 RE E~1. 75) SA3 RE E 1.75)+S SA4 RE E(1. 75) SA6 RE E~1.75)+S SA5 DU E 1.5 )+S SA7 DU E~1.5 ) SA E 1. 75) SA9 732 E(1.5 ) SB E(2.5 ) SBI 1523 E(2.5 )+L+M+S SB E~0.6 )+S SB E 0.6 ) SB E(0.9 ) SB7 L2 E(0.75) SCI LE E(2.5 ) SC2 LE E(0.5 )+S SC3 LE E(0.8 ) Abbreviations: E =ethanol precipitation; figures in parentheses represent volumes of ethanol used; S = Sevag method of deproteinization; L =Iead precipitation; M =electromigration. spectrophotometer with sodium chloride prism. The variable thickness films were adjusted in the sample beam to give 15% transmission at 9.5 microns (p) wavelength. RESULTS AND DISCUSSION All the spectrums showed absorption maximums at nearly the same wavelengths, but there were differences in the intensity of the bands (figure 1). Occasionally a weak band in one spectrum was represented only by an inflection in another spectrum. The strongest band in all the spectrums was a broad absorption from 8.5 IJ. to.5 IJ.. Its deepest point was usually at 9.5 IJ., but especially in type Band C preparations, the band was resolved into two components with absorption maximums at 9.35 and 9.6 J.I.. The descending limb showed an inflection at 8.9 IJ. (and in type Band C preparations a second inflection at 8.7 IJ.), and the ascending limb showed an inflection at.2 IJ.. Klebsiella and pneumococcal polysaccharides, and in fact most carbohydrates, have their broadest and deepest infrared absorption in this region. Strong absorptions at about 6.2 and 7.1 IJ. were present in all the cryptococcal spectrums. These have been described previously in all klebsiella spectrums and in many of the pneumococcal spectrums, and evidence has been presented to indicate that they were due to the carboxylate ion, probably in the form of uronic acid salts (1). Weak absorptions or inflections were present at about.9, 11.2, and 12.5 IJ.. The long wavelengths have been called the "fingerprint region" because identifications of many organic compounds have been based on specific configurations in this portion of the spectrum; this was equally true in identifying closely related klebsiella and pneumococcal types. However, all the cryptococcal polysaccharides showed the same general configuration in this region, with minor differences in band depth that could not be correlated with serological type. All the cryptococcal polysaccharide spectrums had bands at about 5.8 IJ. and IJ.. In contrast to the above, the depths of these two bands varied greatly in the different spectrums. The 5.8 J.I. band was in the carbonyl region of the spectrum, while the 8.0 to 8.1 IJ. band was in a region where esters absorb strongly; it is likely that both bands were due to the ester linkage, probably acetyl groups bound to the hydroxyls of the constituent sugar chains. Also associated with these two bands was a weak absorption at about 7.25 IJ. which Downloaded from at Penn State University (Paterno Lib) on May, 2016

3 CRYPTOCOCCUS POLYSACCHARIDES 271 IIIftl.MIU IICt $ ,f--r-,rr-1-r,-r-r--r----,--,--,---,---, '0.1 r J L---L_L---L_L---L_L---L_L---L---J.' 0 0 to II IAVELElCnllIIIICI ' Type 6.1 J IIL--"---'---"---'---"---'---"---'---"---'.I' 0...,...-,--r-r---.~-~,----r--r-----r---, 5C-3 Type C FIG. I.-Infrared spectrums of purified cryptococcus polysaccharides of Types A, B, and C. The bands at 5.8 JL and at 8.0 to 8.1 JL are strong in SA6, weak in SC3 and intermediate in SBI. may have been due to the terminal methyl of the acetyl group. These bands have been described in many of the klebsiella and pneumococcal polysaccharides (1, 2). Their correlation II with serological typing of cryptococci is described below. As a group, the cryptococcal spectrums resembled the klebsiella more than the pneumococcal spectrums. All the cryptococcal and all the klebsiella spectrums showed strong carboxylate ion bands (6.2 and 7.1 )1.). A minority of the pneumococcal spectrums showed carboxylate bands, while amide bands were very frequently observed; amide bands were never observed ill either cryptococcal or klebsiella spectrums. Effect of method of preparation The growth medium is an important factor when spectrums of whole cells are recorded but IS much less important when purified polysaccharides are examined. Polysaccharide from a type A culture grown in neopeptone dialysate broth was not spectrally different from polysaccharide of the same strain grown in casein hydrolysate medium. Infrared spectrums are additive, so that impurities influence the spectrum in proportion to their amount. For example, the removal of traces of protein from a number of specimens influenced the spectrums very little or not at all. However, several of the spectrums showed evidence of sodium acetate impurity, in the form of broadening and deepening of the 6.2 and 7.1)1. carboxylate bands; this effect could be induced by deliberately adding sodium acetate to a pure preparation. Dialysis of the contaminated preparations resulted in sharpening and decreased intensity of the carboxylate bands. The presence of fraction R could not be detected in the spectrums. The spectrum of SB8, containing R, was identical with those of SB1 and SB2 whose fraction R had been removed. Similarly, SC1 which contained fraction R was spectrally identical with SC2 and SC3 which lacked it. Through the kindness of Mrs. Julia Downloaded from at Penn State University (Paterno Lib) on May, 2016

4 272 SEYMOUR LEVINE, E. EDWARD EVANS, AND PAUL W. KABLER Einbinder we were able to examine capsular polysaccharides prepared from a pathogenic strain of C. neoformans and from a strain of C. neoformans var. innocuous by a completely different method (extraction with 30% potassium chloride and 1% potassium carbonate) (7). The configurations of the spectrums were similar to those illustrated here except that the 5.8 and 7.25 JL bands were absent and the 8.0 to 8.1 JL band was very weak. In contrast, spectrums of whole untreated cryptococcal cells, of both strains, showed that the three bands were present along with bands attributable to other cell constituents. These results suggested the possibility that the method of extraction had destroyed acetyl groups and thus altered the polysaccharide spectrum. In order to test this possibility, aliquot samples of the dried whole cryptococcal cells were subjected to extraction by boiling water, by water at 0 C, by water at room temperature, by 30% potassium chloride at room temperature, and by 30% potassium chloride plus 1% potassium carbonate at room temperature. The polysaccharides were isolated by alcohol precipitation and examined without further purification. The acetyl bands at 5.8, 7.25, and 8.0 to 8.1 JL were present in the first four preparations and almost completely absent from the last. These results indicated that the potassium carbonate was responsible for the loss of acetyl groups and consequent spectral alterations. Potassium carbonate is an alkaline salt, and ester linkages are readily hydrolyzed at alkaline ph. Potassium chloride is a neutral salt and hence inactive in this respect. This experiment was also carried out on a klebsiella strain with identical results. Correlation of spectral results and serological typing Spectral comparison of all the preparations showed large and consistent differences only in the acetyl bands (5.8 JL carbonyl band and 8.0 to 8.1 JL ester band) (figure 1). All the type C preparations had very weak carbonyl and ester bands. All the type A and B preparation had strong or moderate carbonyl and ester bands; those in type A tended to be stronger than those in type B, but there was sufficient overlap to prevent spectral differentiation. In the table the depth of the 5.8 JL carbonyl band of each preparation has been indicated by its absorbance value. It is possible to compare the values taken from different spectrums because each spectrum was recorded in an area of the polysaccharide film whose thickness was the same (8) (15% transmission at 9.5 JL). Therefore the lower absorbances (higher transmissions) recorded for type C preparations probably mean lower carbonyl (acetyl) content. The figures cannot be interpreted quantitatively because of uncontrollable factors such as nonspecific light-scattering. Another approach is the calculation of the ratio between the absorbance at 5.8 JL and the absorbance of the neighboring carboxylate band at 6.2 JL; these absorbance ratios are listed in the table and they may give a slightly more accurate indication of the relative acetyl content of the polysaccharides. Visual comparison of the depths of the 5.8 and 6.2 JL bands (first two bands in each of the spectrums in figure 1) gives essentially the same indication of relative acetyl content. Neither these ratios nor a number of others permitted the spectral differentiation of types A and B due to the overlap of some of the values.* In contrast, type C preparations were easily identified by their low acetyl content. A parallel may be noted with serological results which have demonstrated * It is possible that this differentiation would be facilitated by a more quantitative technique, such as the incorporation of the polysaccharide in potassium bromide peliets. Downloaded from at Penn State University (Paterno Lib) on May, 2016

5 CRYPTOCOCCUS POLYSACCHARIDES 273 a closer relation between types A and B than between type C and either A or B (3,4). In view of the basic similarity of the cryptococcal spectrums, it seems possible that their differences in serological reactivity may depend in part on the degree of acetylation of the polysaccharide chains. The previous studies of the pneumococcal (1) and klebsiella (2) groups showed that many types were easily identified by numerous type-specific spectral bands and configurations. There were only a few instances in which spectral differentiation was difficult or impossible, or in which differentiation had to be based on differences merely in intensity of certain bands (acetyl bands), and these instances occurred in closely related strains. Therefore the present results with cryptococcal polysaccharides have provided additional evidence that they are, as a group, closely related. SUMMARY Infrared spectrums of purified cryptococcal capsular polysaccharides have been presented. Some of the absorption bands were attributed to carboxylate ions and to acetyl groups in ester linkage; these bands have been described previously in klebsiella and some pneumococcal capsular polysaccharides. Klebsiella and pneumococcal polysaccharides were characterized by many type-specific bands and configurations, but polysaccharides from the three cryptococcal types showed generally similar bands indicating the close relationships in this group. There were, however, large differences in the intensity of certain bands. Type C with very weak acetyl bands was easily differentiated from types A and B with strong and intermediate acetyl bands; different strains of types A and B showed some overlap in values. The spectral results thus paralleled the previous demonstration of a closer relation between types A and B than between type C and either A or B. It is possible that differences in degree of acetylation play an important role in determining the serological specificity of cryptococcal capsular polysaccharides. Impurities of protein or fraction R were not detectable in the spectrums. Contamination with sodium acetate was detected in some preparations and was eliminated by dialysis. Evidence is presented to show that the acetyl groups in ester linkage were destroyed if alkaline salts were employed in the preparation of polysaccharides. REFERENCES 1. Levine, S., Stevenson, H. J. R. and Kabler, P. W. 1953, Arch. Biochem. Biophys. 45: Levine, S., Stevenson, H. J. R, Bordner, R H. and Edwards, P. R. 1955, J. Infect. Dis. 96: Evans, E. E. 1950, J. Immuno!' 64: Evans, E. E. and Kessel, J. F. 1951, J. Immuno!' 67: Evans, E. E. and Theriault, R J. 1953, J. Bact. 65: Sevag, M. G. 1934, Biochem. Ztschr. 273: Einbinder, J. M., Benham, R. S. and Nelson, C. T. 1954, J. Invest. Dermat. 22: Riddle, J. W., Kabler, P. W., Kenner, B. A, Bordner, R H., Rockwood, S. W. and Stevenson, H. J. R. 1956, J. Bact. 72: Downloaded from at Penn State University (Paterno Lib) on May, 2016

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