THE CHEMISTRY OF THE LIPIDS OF TUBERCLE BACILLI

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1 THE CHEMISTRY OF THE LIPIDS OF TUBERCLE BACILLI LXXII. FATTY ACIDS OCCURRING IN THE WAX PREPARED FROM TUBERCULIN RESIDUES. CONCERNING MYCOCEROSIC ACID* BY LEONARD G. GINGER? AND R. J. ANDERSON (From the Department of Chemistry, Yale University, New Haven) (Received for publication, October 20, 1944) It has been found in previous studies reported from this laboratory (1) that the wax fractions isolated from the human tubercle bacillus, Strain H-37, contain a series of fatty acids combined with a specific polysaccharide (2). In addition to mycolic acid (3), which is the chief acid constituent, small amounts of normal fatty acids occur, such as palmitic, oleic, stearic, and hexacosanoic acids. The presence of tuberculostearic acid and the dextrorotatory phthioic acid has also been observed. What appears to be of special interest is the occurrence of fatty acids of high molecular weight that are levorotatory. These acids form lead salts that are easily soluble in ether. A levorotatory fatty acid was first encountered in the analysis of the purified wax (1). Later on an acid was isolated which melted at and its specific rotation was -6.1 (4). Its molecular weight and composition agreed approximately with the formula C30H6002. The low melting wax contained in the mother liquors in the purification of the phosphatide (5) cont,ained a levorotatory fatty acid which melted at 37-38, and the specific rotation of different fractions varied from -7 to The molecular weight and composition of these acid fractions were in agreement with the formula C3rH6202. In view of the fact that the purification of the levorotatory fatty acid has been found to be even more difficult than the purification of phthioic acid, the actual composition and specific rotation of the acid cannot be regarded as definitely established. It is moreover possible that homologous or even isomeric forms of the acid may be present. However, judging by observations in this laboratory extending over a period of years, there appears to be no doubt that a levorotatory fatty acid fraction having the ap- * The present report is a part of a cooperative investigation on tuberculosis; it has been supported partly by funds provided by the Research Committee of the National Tuberculosis Association. t Holder of a National Tuberculosis Association Fellowship at Yale University, The data are taken from the dissertation submitted by Leonard G. Ginger to the Faculty of the Graduate School, Yale University, 1943, in partial fulfilment of the requirements for the degree of Doctor of Philosophy. 203

2 204 LIPIDS OF TUBERCLE BACILLI. LXX11 proximate composition represented by the formula C&H6002 is a constant cleavage product of the wax fractions of the human tubercle bacillus, Strain H-37. In order to designate this acid by a characteristic name we propose to call it mycocerosic acid. Should it be found eventually that more than one such acid occurs, then the prefixes a-, /3-, etc., may be applied. The present investigation concerns itself primarily with a study of the levorotatory mycocerosic acid which was isolated from the wax fraction of cell residues from the preparation of the purified protein derivative PPD (6). As has been indicated in an earlier publication (7), the exact strain of tubercle bacilli used in the preparation of this lot of PPD is unknown, but it was undoubtedly a human strain, although certain differences in fatty acid constituents have been found, as well as differences in the polysaccharide component of the phosphatide. EXPERIMENTAL The crude chloroform-soluble wax which served as the starting materiai in this investigation had been isolated from cell residues, as described in. Paper LXVIII of this series (7). Purijcation of the Wax-For purification gm. of the crude wax were dissolved in 1.5 liters of warm ether and the solution was filtered to remove some filter paper fibers. The solution was cooled in ice water and about. an equal volume of methyl alcohol was added slowly with stirring. The precipitate that separated was filtered off and washed with methyl alcohol. The precipitate was redissolved in ether and precipitated by the addition of methyl alcohol. After these operations had been repeated four times, a nearly white powder was obtained which, after it had been dried in vacua, weighed gm. The mother liquors and washings were combined and the solvent was evaporated. The residue formed a deep yellowish salve-like mass which weighed 75.5 gm. This fraction was saved for future investigation. The purified wax softened at 43 and formed a clear melt at 53, [aid in CHC4 = f3.8. The substance was nearly saturated, since. the iodine number was only 2.3. Analysis-Found, C 76.49, H 12.85, N 0.10, P 0.12, ash 0.73 The high oxygen value, about 9.3 per cent by difference, suggests the presence of a considerable amount of carbohydrate. Xaponification of the Purified Wax-It has been found in earlier experiments in this laboratory that the tubercle bacillus wax on saponification yields carbohydrate, mycolic acid, certain normal fatty acids whose lead salts are insoluble in ether, levorotatory acids, and small amounts of other acids, such as oleic, tuberculostearic, and phthioic acids, whose lead salts

3 5. G. GINGER AND R. J. ANDERSON 205 are easily soluble in ether, neutral material, and sometimes glycerol. A method for the separation of these cleavage products was described by Reeves and Anderson (S), and the same procedure was applied in the present case. For saponification gm. of t.he purified wax were dissolved in about 2 liters of benzene and 500 cc. of normal methyl alcoholic potassium hydroxide were added. After the solution had stood at room temperature for a short time, a precipitate consisting of carbohydrate separated. The solution was warmed, after which the precipitate was filtered off, washed with hot benzene, and purified, as will be described later. To the combined filtrate and washings were added 15 gm. of potassium hydroxide dissolved in 100 cc. of methyl alcohol, and the solution was refluxed in an atmosphere of nitrogen for 72 hours. The reaction mixture was concentrated in vacua to a volume of about 700 cc., diluted with 1.5 liters of water, acidified with hydrochloric acid, and extracted five times with ether. The aqueous solution was neutralized with potassium hydroxide, evaporated in vacua to dryness, and examined in the usual manner for glycerol. The resulting product was a thick syrup that weighed 4.5 gm. It gave no Molisch reaction but a positive test for acrolein. The syrup was presumably crude glycerol, but it was not further identified. Separation of the Ether-Soluble Constituents-The ethereal solution was dried over sodium sulfate, filtered, and evaporated to dryness. The yellowish residue was dissolved in 400 cc. of ether and diluted with 600 cc. of alcohol, which caused a voluminous, finely divided precipitate to separate. After the mixture had been cooled in ice water the precipitate was filtered off, washed with alcohol, and dried in vacua over sulfuric acid. The slightly yellowish product, consisting mainly of crude mycolic acid, weighed gm. This substance was reserved for further investigation. The filtrate and washings were combined and the ether was removed by distillation, aft er which an excess of lead acetate dissolved in hot alcohol was added. After the solution had cooled and stood overnight, the lead salts of the fatty acids were filtered off, washed with alcohol, and dried in vacua over sulfuric acid. The lead salts, on treatment with ether, were separated into ethersoluble and ether-insoluble fractions which were decomposed in the usual manner with dilute hydrochloric acid. The ether-soluble lead salts gave 33.9 gm. of acids as a salve-like mass, while the ether-insoluble lead salts gave 30 gm. of solid fatty acids. The filtrate and washings from the alcohol-insoluble lead salts were combined and evaporated nearly to dryness in vacua. The residue was treated with 500 cc. of dilute acetic acid and extracted four times with ether. The aqueous portion was then discarded. The ethereal solution was

4 206 LIPIDS OF TUBERCLE BACILLI. LXX11 washed with water until the washings were neutral, after which it was extracted three times with 200 cc. portions of dilute sodium hydroxide. The alkaline solutions, on acidification with hydrochloric acid and extraction with ether, yielded 8.9 gm. of liquid fatty acids that had not been precipitated as lead salts. The ethereal solution, following the alkaline extractions, was washed with water, dried over sodium sulfate, filtered, and evaporated to dryness. The residue consisting of neutral material was a nearly white, partly crystalline mass that weighed 16.6 gm. Purification of the Carbohydrate-The precipitate that separated from the alkaline benzene solution, as mentioned previously, was dissolved in 200 cc. of water to give a cloudy solution that was strongly alkaline in reaction. The solution was acidified with acetic acid and filtered through a layer of norit. Neutral lead acetate was added to the filtrate and the slight precipitate that separated was filtered off and discarded. The carbohydrate was then precipitated by adding an excess of basic lead acetate and ammonia. The lead salt was filtered off and washed with water, after which it was suspended in water and decomposed with hydrogen sulfide. The lead sulfide was filtered off and the filtrate was concentrated in vacua to a thick syrup. The syrup on dehydration with absolute alcohol gave a white powder that weighed 8.3 gm., [cy]~ in Hz0 = +51.0, and there was no mutarotation. Analysis-Found, N 0.43, P 1.9 The substance gave no reduction with Fehling s solution until after it had been hydrolyzed. On refluxing with 5 per cent sulfuric acid the maximum reduction determined by the Shaffer-Hartmann method (9) was attained in about 3 hours and amounted to 67 per cent, calculated as glucose. The carbohydrate gave the usual pentose coior reactions and was apparently similar to the pentose-containing polysaccharide of the human tubercle bacillus. The various cleavage products of the wax are summarized in Table I. The balance of this investigation is concerned with a study of the fatty acids obtained from the ether-soluble lead salts, with the solid acids obtained from the ether-insoluble lead salts, and the acids obtained from the alcohol-soluble lead salts, that is, with Fractions 4, 5, and 6 of Table I. Investigations dealing with the crude mycolic acid, Fraction 3, and with the neutral material, Fraction 7, will be reported in subsequent papers. Fractionation of the Fatty Acids Obtained from the Ether-Soluble Lead Salts. Isolation of Mycocerosic Acid-The fatty acid, 33.9 gm., obtained from the ether-soluble lead salt was saturated, since it showed no iodine number. The acid was converted into the methyl ester by refluxing with

5 L. G. GINGER AND R. J. ANDERSON 207 absolute methyl alcohol containing 5 per cent of dry hydrochloric acid, after which the ester was isolated in the usual manner and yielded 32.1 gm. of ester as a soft, yellowish mass. The ester was distilled through a modified Widmer column, the apparatus being sealed on to the vacuum line. The system was evacuated by means of a diffusion mercury pump backed by an efficient Hyvac pump, and the pressure was measured on a McLeod gage. At a pressure of about 10e3 mm. the ester distilled at a bath temperature of with a vapor temperature of The distillate was almost colorless and it weighed 26.6 gm. The yellowish residue weighed 4.5 gm. Both fractions solidified at room temperature. It is obvious, in view of the high temperature at which the distillate came off, that no lower fatty acids could have been present. TABLE Hydrolysis Products from Gm. of Purified Wax Fraction No. Description I Weight - Purified carbohydrate Crude glycerol I mycolic acid Fatty acids from ether-soluble lead salts Solid I ether-insoluble lead salts Fatty alcohol-soluble I Crude neutral material I m Saponification of the Ester-The distilled ester was saponified by refluxing for several hours with an excess of alcoholic potassium hydroxide, after which the free acid was isolated and dried to constant weight in vacua over sulfuric acid. The crude mycocerosic acid formed a non-crystalline waxy solid. Rotation-O.4597 gm. of acid, dissolved in chloroform and diluted to 10 cc., gave in a 1 dm. tube (Y = ; hence [CX]~ = Titration-O.3695 gm. of acid, dissolved in 25 cc. of neutral alcohol, required cc. of N alcoholic potassium hydroxide. Found, mol. wt. 455 For CaoHe002. Calculated, mol. wt. 452 Fractionation of the Acid-Since Wieghard and Anderson (5) had found that the barium salt of the levorotatory acid that they examined had useful properties, an attempt was made to purify the present acid by the same method. For the preparation of the barium salt the acid was dissolved in

6 208 LIPIDS OF TUBERCLE BACILLI. LXX cc. of ether and the solution was neutralized to phenolphthalein by the addition of a 10 per cent solution of barium hydroxide in warm methyl alcohol. After the mixture had stood overnight, the granular precipitate was filtered off, washed with methyl alcohol, and dried. The substance was a white powder which weighed 29.0 gm. The barium salt was dissolved in warm benzene and precipitated by the addition of methyl alcohol. The filtrate from this operation was cooled in ice water, which gave a second fraction. The final filtrate and washings on concentration to dryness gave a third fraction. These operations were repeated on each fraction several times, after which the various fractions were analyzed for barium by combustion to barium carbonate in a platinum crucible. Fractions of similar barium content and solubility were combined, and the free acids were regenerated by treatment in ether suspension F&fon TABLE II Properties of Mycocerosic Acid Obtained from the Barium Salts Weight [al, 40 RD M.p. Mol. wt. C II gm. C. $e? cent per cent with dilute hydrochloric acid. The properties of the acids purified over the barium salt are recorded in Table II. For CeHsoOz. Calculated, C 79.65, H 13.27, mol. wt. 452 It would appear that the values found agree most nearly with the calculated composition of an acid of the formula C30He002. As will be noted in Table II, the physical constants of the acid fractions are very similar, thus indicating at least a certain degree of purity. However, when the methyl ester was subjected to fractional distillation, a series of fractions was obtained that varied in properties, thus indicating that the acid was not homogeneous. A portion of the acid, Fraction 3, Table II, was esterified with diazomethane and 3.88 gm. of the ester were fractionated through a special co1umn.l The results are shown in Table III. The rotations of the first three fractions would indicate an admixture of dextrorotatory acids, such as phthioic acid, whereas the other fractions have more uniform properties. 1 This column had been constructed by Dr. S. F. Velick for the purification of the methyl ester of phytomonic acid.

7 L. G. GINGER AND R. J. ANDERSON 209 Saponi$cation of the Ester-The ester Fractions 6,7, 8, and 9 were.combined and saponified and the free acid was isolated. The acid was a waxy solid that could not be crystallized. It melted at 27-28, [a],, in CHCh = -5.7, mol. wt. by titration C:,,H,02. Calculated, mol. wt. 452 The p-bromophenacyl ester was prepared according to Judefind and Reid (10). The substance could not be crystallized, but separated as a white amorphous solid from alcohol, m.p ATMT&s~s-G~H~~O~B~ (648.9). Calculated, Br 12.31; found, Br The analytical data agree best with the formula C30Hc002 for the mycocerosic acid. - TABLE Fraction ation of the Methyl Ester of Mycocerosic Acid Bath Column temperature temperature - C. C. %. C III Weight M.p. k-4; in CHCls d n30 D , The Solid Fatty Acids Isolated from the Ether-Insoluble Lead Salt-The solid fatty acids, 30 gm., isolated from the ether-insoluble lead salts, were converted into methyl esters and fractionated through a short modified Widmer column at a pressure of about 0.1 mm. into three fractions and a large residue. The ester fractions were saponified and the free acids were recrystallized from acetone and were obtained as colorless plates. Fraction 1 appeared to be a typical mixture of palmitic and stearic acids. It melted at and the molecular weight was 261. Fraction 2 was an apparently similar mixture. Fraction 3 gave an acid which melted at The molecular weight was 298 and the acid evidently was a mixture of stearic and hexaccsanoic acids. No effort was made to purify these acids further, but it seems sase to assume that the principal components were palmitic and stearic acids.

8 210 LIPIDS OF TUBERCLE BACILLI. LXXII The residue from the distillation after it had been saponified gave an acid fraction that weighed 18.9 gm. It was dissolved in benzene and after standing and cooling it was possible to crystallize 2.5 gm. of an acid which melted at Four recrystallizations from benzene-acetone raised the melting point to The molecular weight by titration was found to be 394. Analysis-CzsHs202 (396). Calculated, C 78.78, H Found, average of three analyses, 78.99, Although the melting point is somewhat low, the composition of the acid indicates that it is mainly n-hexacosanoic acid. Examination of Mother Liquo.rs after Removing n-hexacosanoic Acid-The mother liquors on concentration to dryness left a waxy solid acid which weighed 16.3 gm. The acid was levorotatory, [a!]= in CHCI, = The presence of a levorotatory acid in the solid fatty acid fraction was no doubt due to the formation of mixed lead salts with the normal solid fatty acids, thus giving lead salts that were only slightly soluble in ether. Since the acid could not be crystallized, it was converted into the barium salt, as mentioned previously. The barium salt was separated into several fractions from benzene solution by the gradual addition of methyl alcohol. The main fraction of the acid regenerated from the barium salt was esterified with diazomethane and the ester was fractionated through the special column previously mentioned. The fore run had a low dextrorotation, probably due to admixture of phthioic acid. The next two fractions had low levorotations. The middle fractions corresponded in rotation and physical constants to the purified methyl ester of mycocerosic acid and these fractions were combined and saponified. The free acid corresponded to mycocerosic acid, [ain in CHCl, = -5.1 ; the molecular weight by titration was 450. The highest boiling ester fraction gave on saponification a levorotatory acid of very high molecular weight, [aid in CHC13 = ; the molecular weight by titration was 758. The non-volatile residue from the distillation had a levorotation, [(Y]= in CHCls = On saponification it gave an acid which had a molecular weight, by titration, of These last two fractions were most likely impure mixtures. Fatty Acids from the Alcohol-Soluble Lead Salts, Fraction 6, Table I-The fatty acid recovered from the alcohol-soluble lead salts weighed 8.9 gm. It was liquid at room temperature and the iodine number was 11. The acid was converted into the lead salt and the latter was treated with ether. The ether-insoluble lead salt gave 1.1 gm. of a white crystalline acid which was not further examined. The acid recovered from the ether-soluble lead salt was reduced with hydrogen and platinum oxide, after which the

9 L. G. GINGER AND R. J. ANDERSON 211 lead salt-ether separation was repeated. The solid reduced acid obtained from the ether-insoluble lead salt weighed about 1.0 gm. It melted at and the molecular weight by titration was 292. This material was not further examined. The acid obtained from the ether-soluble lead salt was esterified by diazomethane and the ester was fractionated repeatedly through the special column, as mentioned previously. The results indicated that the ester was a complex mixture. The first ester fraction gave on saponification a small amount of a solid fatty acid which was not identified. The next fraction on saponification gave an optically inact.ive liquid-saturated acid that corresponded in properties and composition to tuberculostearic acid, C~H3802. The third fraction was dextrorotatory and on saponification gave an acid that had [aid = +5.0 and the molecular weight by titration was 397. The fourth fraction was levorotatory and on saponification an acid was obtained that corresponded in properties to mycocerosic acid, [a],, in CHCI, = -5.1, molecular weight by titration 448. SUiMMARY An examination has been made of the fatty acids contained in the wax isolated from tubercle bacilli residues from the preparation of the purified protein derivative PPD. The normal fatty acids were represented by palmitic, stearic, and hexacosanoic acids and an unsaturated acid, probably oleic acid. The branched chain fatty acids giving ether-soluble lead salts were separated into tuberculostearic acid, dextrorotatory acids analogous to phthioic acid, and a levorotatory acid. The name mycocerosic acid is proposed to designate the levorotatory acid which has been found to be a characteristic constituent of all the wax fractions of the human tubercle bacillus. Mycocerosic acid was obtained as a non-crystalline waxy solid, m.p , 1011~ in chloroform -5 to - 6, and its composition corresponds to the formula CaoHsoOz. BIBLIOGRAPHY 1. Anderson, R. J., J. Biol. Chem., 63, 505 (1929). 2. Roberts, E. G., and Anderson, R. J., J. Biol. Chem., 90,33 (1931). 3. Stodola, F. H., Lesuk, A., and Anderson, R. J., J. Biol. Chem., 126,505 (1938). 4. Anderson, R. J., J. Biol. Chem., 97, 639 (1932). 5. Wieghard, C. W., and Anderson, R. J., J. BioZ. Chem., 126, 515 (1938). 6. Seibert, F. B., and Glenn, J. T., Am. Rev. Tuberc., 44,9 (1941). 7. Creighton, M. M., and Anderson, R. J., J. BioZ. Chem., 164,581 (1944). 8. Reeves, R. E., and Anderson, R. J., J. BioZ. Chem., 119,535 (1937). 9. Shaffer, P. A., and Hartmann, A. F., J. BioZ. Chem., 46,365 ( ). 10. Judefind, W. L., and Reid, E. E., J. Am. Chem. Sot., 42,1043 (1920).

10 THE CHEMISTRY OF THE LIPIDS OF TUBERCLE BACILLI: LXXII. FATTY ACIDS OCCURRING IN THE WAX PREPARED FROM TUBERCULIN RESIDUES. CONCERNING MYCOCEROSIC ACID Leonard G. Ginger and R. J. Anderson J. Biol. Chem. 1945, 157: Access the most updated version of this article at Alerts: When this article is cited When a correction for this article is posted Click here to choose from all of JBC's alerts This article cites 0 references, 0 of which can be accessed free at tml#ref-list-1

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