tryptophane from amino acids alone and from amino acids and glucose, respectively. Only the partially exacting and exacting strains are considered
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1 THE MECHANISM OF RESISTANCE TO SULFONAMIDES III. PANTOTHENIC ACID AND TRYPTOPHANE METABOLISM: THE ROLE OF PANTO- THENIC ACID IN THE SYNTHESIS OF TRYPTOPHANE BY STAPHYLOCOCCUS AUREUS AND THE EFFECT OF VITAMINS ON TRYPTOPHANE IN EXERCISING ANTAGONISM TO SULFONAMIDES1 M. G. SEVAG AND MORRIS N. GREENS Department of Bacteriology, School of Medicine, University of Pennsylvania, Philadelphia 4, Pa. Received for publication July 19, 1944 It has been known for some time that pantothenic acid is effective as a growth vitamin for many bacteria (Williams, 1943). The mechanism involved in the effect of pantothenic acid on growth is, however, not known. The present report deals with a study which indicates that pantothenic acid is involved in the synthesis of tryptophane essential for the multiplication of Staphylococcus aureus. Pantothenate alone or in combination with other vitamins likewise exercises a marked effect upon the resistance of staphylococci to sulfonamides. The relationships between these observations will be described in this paper. It has been observed in this laboratory (see also Gladstone, 1937) that strains of S. aureus can be divided into three classes with respect to their nutritional requirements: 1. Nonexacting class. Those which are capable of multiplication in the absence of tryptophane in synthetic media made up of amino acids (table 1, footnote*), also in casein hydrolyzate (table 2, footnote*), each supplemented with vitamins and salts. 2. Partialy exacting class. Those capable of multiplication upon the addition of 0.5 per cent glucose to tryptophane-free media. 3. Exacting class. Those capable of multiplication only when tryptophane is added to these media, with or without the addition of glucose. The nonexacting and partially exacting strains apparently are able to synthesize tryptophane from amino acids alone and from amino acids and glucose, respectively. Only the partially exacting and exacting strains are considered in this paper. The work of this laboratory has indicated that in staphylococci an inhibition of tryptophane synthesis occurs as one of the results of sulfonamide action (Sevag and Green, 1944a, 1944b). An understanding of the mechanism of tryptophane synthesis by staphylococci is therefore essential from both physiological and chemotherapeutic standpoints, and also in understanding the mechanism of resistance to sulfonamides. RESULTS Source and Variation of Staphylococcus aureus. Through the courtesy of Dr. John E. Blair (Hospital for Joint Diseases, New York City) we obtained 4 strains This investigation has been aided by a grant from the Josiah. Macy, Jr. Foundation. 2 George Leib Harrison Fellow and Manfred Wahl Fellow. 631
2 632 M. G. SEVAG AND MORRIS N. GREEN of toxigenic S. aureus which were isolated from the blood in cases of septicemia. accompanying acute osteomyelitis. When we received them they were cultivated on brain-heart-infusion agar. Stoppered with cotton and cork, they- TABLE 1 The role of pantothenic acid on the synthesis of tryptophane and thereby of the growth of Staphylococcus aureus (B-523) TURBIDITY DUE TO TEHE TURBIDITY DUE. TO THE GROWTH vaxantstaix oi saurus(b.523) CALCIUM GROWTH (AFTER PANTOTHENATE snetchrj I SYNTHETIC ADDED ntin tic MEDIUM + GLUCOS-E 8ADDED medium* + measuredt (0.5%) + TRYPTOPHANE glucose (0.5%) aftr (1 X 10'4 H) pg/ml rcadingst days readings B-523N (3d daily subculture) B-523S (3d daily subculture) B-623SC (34th daily subculture) * Synthetic medium: 10 ml of the M/30 phosphate (ph 7.4) solution containing 6.6 X 104 M of alanine, valine, leucine, glycine, proline, oxyproline, aspartic acid, glutamic acid, 2.5 X 1O4 M of methionine, phenylalanine, tyrosine, hydrochlorides of histidine, lysine, 3.36 X 10-8 M of threonine, 3.05 X 10-3 M of isoleucine, 9.0 X 10-4 M of cysteine hydrochloride, 2.5 X 10-4 M of ferrous ammonium sulfate, 1 X 10-3 M of sodium dithiodiglycollate, 3.3 X 10-4 M of magnesium sulfate, 1 ;Lg/ml of medium of each of thiamine chloride and nicotinamide. t Turbidity readings represent growth per 3 ml culture which was diluted in a standard tube to 10 ml with saline, and the optical density of the suspension was determined with a Mlett-Summerson photoelectric colorimeter. A reading of 66 corresponds to 0.14 mg of staphylococcal nitrogen (or 1 mg of staphylococci) or approximately to 2.5 to 3.5 billion cocci. Inoculum: Staphylococci grown for 20 hours on 5 ml of slant extract agar were suspended in 60 to 80 ml of saline of which 0.2 ml was added aseptically to 10 ml culture medium. Or they were suspended in 5 ml of saline and a loopful used as inoculum. In either case the reading on the inoculated media was 0 at 0 hour of growth. t Measurements: 16 to 24 hours after the first appearance of growth. were kept at room temperature for 10 months before they were subcultured on extract agar and used in growth experiments. Unlike the other 5 nonexacting strains we had gathered from various sources, 3 strains of Blair were found to be
3 MECHANISM OF RESISTANCE TO SULFONAMIDES 633 partially exacting, and the fourth (B-523) exacting. A fresh culture of 523 (B-523N, table 1) received from Dr. Blair, on the other hand, behaved like a partiauy exacting strain. In the light of these facts it would seem that the B-523 TABLE 2 The role of vitamins on the 8ynthesis of tryptophane in relation to the growth and the reversal of the inhibition of the growth of S. aureus (B-52&S) by sulfonamides (Representative data) CONTROL % INHIBITIONxl OF GRowT BY NON O. DIt Growtbt Arylamine formed Sulfanilamide Sulfathiazole ore 0.04 ma ma SEC- NO. GrwtEDyamnU TION 0? MDUM Tryptophane added none I X 10-4 m none 1 X 10- X none I X 104 X none I X 10-4 A 1 Basal medium* glucose (0.5%) B 1 Basal medium glucose (0.5%) vitaminst O 1 Basal medium glucose (0.5%) calcium pantothenate * Basal medium: 10 ml of 1% casein hydrolyzate (SMACO, vitamin-free) contained various salts, thiamine chloride and nicotinamide (see footnote table 1). t Vitamins: Biotin 0.02 jg + folic acid jig + calcium pantothenate 1,g + pyridoxine 1,ug + B2 1 pg per ml of medium. t Growth: The measurement of growth was carried out as described in footnote to table 1. Inoculum: The age of inoculum used in experiments was as follows: exp. 1, 20 hours; exp. 2, 12 hours; exp. 3, 24 hours; and exp. 4, 48 hours. The number of organisms was identical as described in footnote to table 1. Arylamine: 3 ml of clear culture fluid was diazotized and coupled with N-(1-naphthyl)- ethylene diamine hydrochloride (4); a lavender color develops. The colored solution is diluted to 10 ml volume and the depth of color is measured with a Klett-SummersoD photoelectric colorimeter. control growth - growth in sulfonamides IPer cent inhibition of growth = coto rwhx 100. control growth strain on "aging" in our laboratory had lost the ability to synthesize tryptophane. We have derived 2 variants of this character (B-523S and B-523SC, table 1) from the original B-523 strain. Effect of Pantothenate upon Growth and Arylamine Production. Reference to table 1 shows: (a) B-523N strain does not require added tryptophane for growth
4 634 M. G. SEVAG AND MORRIS N. GREEN but grows in the presence of glucose alone, behaving like a partially exacting strain as defined above. Pantothenate definitely speeds up the growth of B-523N strain. This acceleration begins with a concentration of 0.01,g of pantothenate per ml. (b) Both B-523S and B-523SC strains require tryptophane for growth, behaving like exacting strains as defined above. In the absence of tryptophane, pantothenate in a concentration of 0.1 to 1.0,pg per ml is necessary before growth is obtained. In the B-523S strain, measurable growth does not appear until after about seven days (pantothenate concentration 1.0 pug per ml). With the B-523SC strain, however, growth appears within three days (pantothenate concentration 0.1 pug per ml). The B-523S strain, upon daily TABLE 3 The antagonistic action of pantothenic acid and riboflavin on the inhibition of the growth of Staphylococcus aureus (B-523) by sulfathiazole (Representative data) STAPHYLOCOCCUS AUREUS B-523 Control Inhibitiont of - growth by X SECTION EXP. MynIum Growth in sulfathlazole in Tryptophane added None I X 10-M None 1X 10 4X A i Basal medium* alone pantothenate 5,ug/ml riboflavin 4 Jug/ml riboflavin + pantothenate B 1 Basal medium + glucose 0.5% pantothenate 5 pg/ml riboflavin 4 pg/ml riboflavin + pantothenate * Basal medium: 1% casein hydrolyzate as described in the footnote to table 2. t See footnote to table 2. t The absolute amount of growth was too small to enable an accurate calculation of the percentage of inhibition. subculturing (resulting in the 523SC strain) becomes more amenable to the action of pantothenate. In the first article of this series, it was shown that the formation of arylamine is a result of the oxidation of tryptophane. In this connection, it is to be noted (compare controls table 2, sections A and C) that arylamines are formed in the presence of pantothenate and in the absence of added tryptophane (section C). Neither growth nor arylamines appear in the absence of tryptophane or panto- 3 The amount of arylamine calculated as p-aminobenzoic acid is several fold greater than the amount required to counteract completely the inhibition by sulfonamides. In view of the fact that the inhibition is not affected, the arylamine is not p-aminobenzoic acid.
5 MECHANISM OF RESISTANCE TO SULFONAMIDES thenate (section A). The B523N strain shown in table 1 produced fairly large quantities of arylamine, giving colorimetric readings between 43 and 51 (data not given in table 1), in the presence of pantothenate and in the absence of added tryptophane. In these cases, however, growth was delayed from 2 to 7 days. In a medium containing added tryptophane, although heavy growth was observed within 48 hours, no arylamine was found. Effect of Vitamins on Inhibition of Growth in the Presence of Sulfonamides. Reference to table 2 (section A) shows that the B-5238 strain is susceptible to the action of sulfonamides. In the presence of glucose and tryptophane, the average inhibition was 57 per cent with SA and 75 per cent with ST. (Under similar conditions, the inhibition of the resistant strain was -14 per cent [stimulation] with SA, and 9 per cent with ST; table 1, article II.) In the presence of pantothenate, riboflavin, pyridoxine, biotin, folic acid, the inhibition by SA was dramatically reduced to practically zero, and the inhibition by ST was reduced to an average of 13 per cent. Systematically controlled experiments were made in an effort to discover which of the five vitamins was responsible for the reduction of inhibition. Prelminary experiments eliminated folic acid, biotin, and pyridoxine, leaving pantothenate and riboflavin for further study. It is also to be noted that in sulfonamide-free media these vitamins did not stimulate growth in a manner similar to pantothenate. Throughout these experiments it can be observed that in general M ST exerted a much stronger inhibitory effect than 0.04 M SA. In order to secure maximum inhibition, providing also a better- test of the vitamin effects, ST was used in the succeeding experiments (table 3). In the absence of glucose and the presence of tryptophane, it was observed (section A, table 3) that riboflavin (4 ug/ml) had the greatest effect on abolishing the inhibitory action of ST (-38 per cent). Pantothenate (5 pg/ml) increased the inhibition to 100 per cent from the control value of 55 per cent. Both vitamins combined brought the inhibition down to 60 per cent. Upon the addition of glucose along with tryptophane, neither pantothenate nor riboflavin alone reduced the inhibition markedly. In contrast, the combined effect of both vitamins was very pronounced, not only abolishing the inhibition but causing a 38 per cent increase of growth. DISCUSSION 635 The Role of Pantothenate in the Synthesis of Tryptophane by Staphylococcus aureus. The data presented in table 1 show that pantothenate is responsible for the growth of both the B-523S and B-523C strains under the conditions of these experiments (see also Sevag and Green, 1944e). Since these are exacting strains (requiring the addition of tryptophane for growth), pantothenate apparently mediates the synthesis of tryptophane from glucose and amino acids. It has been brought out above that under the influence of pantothenate arylamines are formed in a medium free from added tryptophane. In article I of this series, it has been shown that arylamines are formed as a result of the oxidation of tryptophane. The formation of arylamine by pantothenate in the
6 636 M..G. SEVAG AND MORRIS N. GREEN absence of added tryptophane, therefore, provides additional evidence for the synthesis of tryptophane under these conditions. In article III of this series, it was shown that inhibition of the synthesis of tryptophane was one of the results of sulfonamide action. If pantothenate promotes the synthesis of tryptophane, and riboflavin (a derivative of the coenzyme of amino acid oxidase) promotes the metabolism of tryptophane, we should expect a counteracting of the inhibitory action of sulfonamides. This result is indicated in table 2 and is brought out more definitely in table 3. These observations are interpreted as further evidence for the synthesis of tryptophane with the aid of pantothenate. Effect of Vitamins Upon the Mechanism of the Action of Sulfonamides.4 Since tryptophane is a critical growth amino acid, it is important that an inquiry be made into the relationship between the factors controlling the glucose tryptophane metabolism and that of tryptophane, and the antibacterial or chemotherapeutic action of sulfonamides. The results of experiments with the exacting variant strain B-523S (table 2) show that: (1) in the absence of the vitamins (section A), the addition of tryptophane to the medium does not appear to antagonize noticeably the inhibition of growth by sulfonamides; (2) the presence of vitamins alone (section B) does not antagonize sulfonamide action in the absence of added tryptophane; and (3) the simultaneous presence of both the vtamins and added tryptophane abolishes the inhibition of the growth by sulfonamides (section B).5 It seems reasonable to conclude that these vitamins exercise a significant role on the glucose tryptophane metabolism in counteracting the antibacterial action of sulfonamides. This role of vitamins appears to be limited (in the case of the strain used) to the utilization of the added tryptophane, and not to its synthesis from glucose and other amino acids. The inhibition of the synthesis of tryptophaie appears to be the critical action of sulfonamides. Of the vitamins studied, pantothenate and riboflavin exercise the most significant roles. The results (table 2, section C, experiments 1, 2, 3)6 show that only in the presence of added tryptophane is pantothenate alone capable of bringing about, partially or completely, the elimination of the inhibition of growth by sulfonamides. Sulfonamides block the metabolism of glucose leading to the synthesis of tryptophane, and not the utilization of added tryptophane in the presence of pantothenate. The results of experiments with the partially exacting strain B-523 (table 3, section A) show that the addition of pantothenate to the glucose-free medium ' We are indebted to Dr. R. Major of Merck and Company for a sample of biotin, and to Drs. E. L. R. Stokstad, B. L. Hutchings, and N. Bohonos of Lederle Laboratories for a sample of Lactobacillus casei factor. ' This may raise the question as to whether or not it is advisable to administer vitamins indiscriminately to patients who are undergoing intensive sulfonamide therapy during an infection. The answer to this question must come from clinical observations. Perhaps better results can be obtained by withholding vitamins temporarily. 6 A comparison of the results listed under experiments 1, 2, and 3 with those of experiment 4 shows that the age of the culture used as the inoculum may be an important factor.
7 MECHANISM OF RESISTANCE TO SULFONAMIDES.637 does not appear to influence the metabolism of added tryptophane in counteracting the inhibition by sulfonamide. However, in the presence of glucose the utilization of tryptophane is promoted by pantothenate and the inhibition by sulfonamides undergoes a certain degree of reduction. A similar effect on the synthesis of tryptophane under these conditions is not apparent (table 3, section B). These observations emphasize the interrelationship of glucose tryptophane pantothenate metabolism. In experiments with the B-523 strain, on the other hand, the sulfonamideantagonizing action of riboflavin appears to be independent of the presence of glucose if tryptophane is added to the medium. Inhibition under these conditions is not only abolished, but growth increases 38 per cent (table 3, section A, exp. 3). In the presence of glucose, but in the absence of added tryptophane, riboflavin alone or in combination with pantothenate is ineffective, or partially effective (table 3, section B, exp. 3 and 4); indicating that under these conditions the metabolism of glucose leading to the synthesis of tryptophane from other amino acids is blocked by sulfonamides. In contrast, in the presence of added tryptophane, pantothenate, and riboflavin there occurs a 38 per cent increase in growth, despite the presence of M sulfathiazole. These observations indicate that the utilization of added tryptophane under these conditions is not affected by the action of sulfonamides. It is also to be noted that in the absence of vitamins added tryptophane is capable of antagonizing the inhibitory action of sulfonamides only when glucose is present in the medium (table 3, section B, exp. 1; compare the inhibitions in the last two columns). Vitamins carry this antagonizing effect to completion. These and the previously cited facts appear to show that the metabolism of glucose and that of tryptophane are interrelated in antagonizing sulfonamides; individually they appear to be deficient in this respect. Inability of Staphylococcus aureus to Synthesize Pantothenic Acid as the Possible Mechanism of Variation. In understanding the mechanism of the variation of the staphylococcal strain B-523 the following considerations may be of interest. The ability of the nonexacting strains to grow in tryptophane-free amino acid medium indicates that they are capable of synthesizing tryptophane from other amino acids in the absence of both glucose and pantothenic acid. The partially exacting strain (B-523N) is capable of achieving the same result in the absence of pantothenic acid, but only when glucose is present; whereas the exacting strains (B-523S and B-523SC) require the presence of both pantothenic acid and glucose for the synthesis of tryptophane. These observations indicate that there are several stages in the processes of variation. In the case of the partially exacting strain, the presence of glucose is essential for the synthesis of tryptophane, and therefore for growth. This may indicate that pantothenic acid is readily synthesized by the cell, or is already stored within the cell. In the former case, glucose may be essential for the synthesis of pantothenate, which is then followed by the synthesis of tryptophane. In the latter case, it may be incapable of mediating the synthesis of tryptophane from other amino acids unless glucose is present. In the case of the exacting strain, a further degradation
8 6008 M. G. SEVAG AND MORRIS N. GREEN has apparently taken place. With this strain, the presence of glucose is inadequate for the synthesis of tryptophane unless pantothenic acid is provided. The loss of the ability to synthesize pantothenic acid therefore appears to be one of the critical changes in the enzyme system of the exacting variant of Staphylococcus aureus. SUMMARY Pantothenic acid mediates (a) the metabolism of glucose leading to, or involved in, the synthesis of tryptophane essential for the growth of the exacting strains of Staphylococcus aureus; (b) in the presence of glucose the oxidation of tryptophane to one or more arylamines (not p-aminobenzoic acid); and (c) the glucose tryptophane metabolism in counteracting the inhibitory action of sulfonamides on the utilization of added tryptophane. Hence, the inhibition of the synthesis of tryptophane from glucose and amino acids appears to be the critical action of sulfonamides on S. aureus. REFERENCES BR*TTON, A. C., AND MARSHALL, E. K., JR A new coupling component for sulfanilamide determination. J. Biol. Chem., 128, GLADSTONE, G. P The nutrition of Staphylococcus aureus: Nitrogen requirements. Brit. J. Exptl. Path., 18, SEVAG, M. G., AND GREEN, M. N. 1944a The metabolism of tryptophane by Staphylococcus aureus as a critical factor in relation to the mode of action of sulfonamides. Am. J. Med. Sci., 207, 686. SEvAG, M. G., Aim GREEN, M. N. 1944b Lack of correlation between the formation of arylamine (p-a.b.a.?) and resistance of staphylococcus to sulfonamides. J. Bact., 47, 451. SXVAG, M. G., AND GREEN, M. N. 1944c The mechanism of resistance to sulfonamides. I. Factors controlling the formation of arylamine from tryptophane by Staphylococcus aureus. J. Bact., 48, SEVAG, M. G., AND GREEN, M. N. 1944d The mechanism of resistance to sulfonamides. II. Absence of correlation between resistance and the formation of arylamine by Staphylococcus aureus. Non-interference with the utilization of glucose as a critical factor in the development of resistance to sulfonamides. J. Bact., 48, SEVAG, M. G., AND GRmEEN, M. N. 1944e The r6le of pantothenic acid in the synthesis of tryptophane. J. Biol. Chem., 154, WILLIAMS, R. J The chemistry and biochemistry of pantothenic acid. Advances in enzymology, 3,
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