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1 THE BACTERIAL OXIDATION OF AROMATIC COMPOUNDS IV. STITDIES ON THE MECHANISM OF ENZYMATC DEGRADATION OF PROTOCATECHuiC ACID' R. Y. STANIER Department of Bacteriology, University of California, Berkeley, California Received for publication January 16, 1950 Dried cells of Pseudomonas fluorescens, harvested after growth at the expense of p-hydroxybenzoic acid, catalyze a quantitative transformation of protocatechuic acid to,-ketoadipic acid (Stanier, Sleeper, Tsuchida, and Macdonald, 1950). The equation is: COOH COOH C CH H20- C=-O + C02 Q OH I OH (CH2) 2 COOH This equation clearly represents the over-all result of several distinct step reactions, which must include rearrangement, water addition, oxidation, and decarboxylation. Further work with the enzyme systems involved has shown that it is possible to dissociate the decarboxylative step from the other reactions, thus clarifying to some extent the course of biochemical events in this transformation. Materials and methods. Dried cells of P. fluorescens grown on p-hydroxybensoate and prepared as described by Sleeper, Tsuchida, and Stanier (1950) served as the source of enzymes. The analytical techniques used were those described by Stanier, Sleeper, Tsuchida, and Macdonald (1950). RESULTS Extraction of enzymes from whole dried cells. Contrary to our previous report (Sleeper, Tsuchida, and Stanier, 1950), the enzymes responsible for the degradation of protocatechuic acid can be obtained cell-free by extraction of certain batches of dried cells with distilled water and subsequent removal of the insoluble debris by centrifugation at high speeds (10,000 rpm). The ease of extraction varies from batch to batch of dried cells, and even with the most readily extractable batches it is not possible to obtain a complete separation of enzymatic activity from the insoluble cellular debris. This is shown by the following typical experiment: Two grams of dried cells were suspended in distilled water 1 This work was supported in part by a grant-in-aid from the American Cancer Society upon recommendation of the Committee on Growth of the National Research Council. 527

2 528 R. Y. STANIER [VOL. 59 and immediately centrifuged. After removal of the clear supernatant, the debris was resuspended in distilled water and kept for 16 hours at 5 to 10 C. Following a second centrifugation, the debris was extracted once more in the same manner. Thereafter, the enzymatic activities of the successive extracts and of the insoluble, washed debris were determined manometrically, by the rate of oxygen uptake with protocatechuic acid as the substrate. The results (table 1) show that in this experiment only 40 per cent of the total activity was removed by a single extraction, and that an approximately equal amount of enzyme could be obtained in solution by subsequent further prolonged extraction. Dissociation of the decarboeylative step. Successive extracts of dried cells, as well as the extracted residue, all oxidized protocatechuic acid at a steady rate and with a total oxygen uptake of one mole per mole of substrate. However, when Rothera tests were performed after completion of the oxidation, different results were obtained with different fractions. The first extracts from dried cells always gave the intense violet reaction characteristic of,b-ketoadipic acid, whereas later extracts and repeatedly extracted cell residues gave weak and TABLE 1 Distribution of protocatechuate-oxidizing activity in the 8uccessive extracts and the extracted residue of p-hydroxybenzoate-grown cells 03 UPTAX WrE VOLUME 0F FRACTION PIOTOCATECHUIC ATOxN, L TOTAL ACTIVITY ACED W/hrl/ml id 0/hr First extract... 6, ,000 Second extract... 8, ,000 Third extract... 4, ,000 Extracted residue*... 4, ,000 * Resuspended in distilled water. sometimes even negative reactions. Since the total oxygen uptakes in these latter cases were still characteristic of the over-all reaction, the anomalous outcome of the Rothera tests suggested that the decarboxylative step might have been affected. This possibility was checked by making systematic determinations of R.Q. values on the successive fractions of a single sample of extracted dried cells. The results presented in table 2 show that the R.Q. values obtained with the last extract and the extracted residue are markedly below the usual figure of unity. This decline of decarboxylative activity as a consequence of repeated extraction might be ascribable either to preferential extraction of the whole enzyme catalyzing decarboxylation or to the removal in the first extracts of a soluble coenzyme required for the decarboxylative step. In the latter case, dialysis of a first extract possessing full decarboxylative activity should also cause a decline of decarboxylation. Accordingly, a first extract was dialyzed in the cold against several successive changes of distilled water. After dialysis, the R.Q. of this preparation had fallen from an original value of 0.95 to From this

3 1950] BACTERIAL OXIDATION OF AROMATIC COMPOUNDS 529 experiment, it seems probable that a coenzyme is required for the decarboxylative step. Since the oxidizing capacity of the preparation was only slightly diminished by thorough dialysis, it is also evident that freely dissociable coenzymes are not needed for the oxidative step(s). The exploratory experiments described above made it possible to prepare very simply two kinds of cell-free enzyme systems, both capable of oxidizing protocatechuic acid with the full oxygen uptake of one mole per mole of substrate, but differing with respect to their decarboxylative capacities. In order to study the reaction catalyzed by a nondecarboxylating preparation, a cell-free enzyme solution was dialyzed until its decarboxylative activity had reached a negligible level. After dialysis, this preparation oxidized protocatechuic acid with an oxygen uptake of 1.05 moles per mole of substrate and an R.Q. of 0.02; the Rothera reaction was completely negative at the end of the oxidation. This system will henceforth be referred to as OE (oxidizing enzyme), in contradistinction to the complete system, which will be referred to as ODE (oxidizing and decarboxylating enzyme). TABLE 2 Oxygen uptakes and R.Q. values with protocatechuic acid determined on successive extracts from dried cells Oh UPTAKE, MOLES PERL MOLE O SUBSTRATE First extract Second extract * Third extract Fourth extract Extracted residue * Not determined. Formation of acid accompanying the nondecarboxylative oxidation of protocatechuic acid. The acid formation resulting from oxidation of protocatechuic acid by OE was determined manometrically, by carbon dioxide release from bicarbonate buffer. In making calculations, an oxygen consumption of one mole per mole of substrate and an R.Q. of zero were employed, on the basis of the figures given in the preceding paragraphs. At the end of the experiment, the Rothera reaction was negative. As shown in table 3, there is a net acid formation of nearly two equivalents per mole of protocatechuic acid oxidized. Since decarboxylation has not occurred, the substrate carboxyl group must still be present in the product of oxidation; accordingly, the product must contain three acidic groups, of which at least one is a carboxyl group. Enzymatic decarboxylation of the intermediate formed by the oxidation of protocatechuic acid. Since the full oxygen uptake necessary for the transformation of protocatechuic acid to,b-ketoadipic acid occurs when OE acts on protocatechuic acid, the product of this reaction should be transformable without further oxygen uptake into carbon dioxide and p-ketoadipic acid under the R.Q.

4 530 R. Y. STANIER [VOL. 59 influence of ODE. In order to test this conclusion, a known amount of protocatechuic acid was oxidized by OE and at the end of the oxidation aliquots of the mixture were subjected to treatment with ODE, oxygen uptake, carbon dioxide production, and B-ketoacid formation being determined. In order to simplify presentation of the results, the experimental procedure will be outlined in detail. A single Warburg vessel (A) was set up with 1.0 ml of OE and 2.0 ml of M/5 phosphate buffer (ph 7.0) in the main compartment, and 0.3 ml of M/25 Na-protocatechuate in the side arm. The contents of the vessel were mixed, and the course of the reaction was followed by observing oxygen uptake. When oxidation ceased, the vessel was removed from the manometer and 1.0-ml aliquots of its contents were pipetted into three other vessels, B, C, and D. A Rothera test was performed on the remaining contents of vessel A with negative results, showing that a negligible amount of,3-ketoadipic acid had been formed TABLE 3 Acidformationfrom protocatechuic acid by the nondecarboxylating enzyme system CONDITIONS Main compartment: 0.5 ml of enzyme and 1.5 ml of M/25 NaHCOs. Side arm: Na-protocatechuate in M/25 NaHCOs to give amount indicated. Atmosphere: air with 15 per cent carbon dioxide. RESULTS AND CALCULATIONS VESSEL 1 VESSEL 2 Na-protocatechuate supplied, micromoles Observed pressure change, mm Calculated pressure change for 02 consumed, mm (90/Ko) -106 (134/Ko,) Total pressure change for C02 released, mm Acid formed, microliters (111 X Kco,) 259 (180 X Kco) Acid formed, microequivalents Acid formed, equivalents per mole of protocatechuic acid oxidized during the initial oxidation. Vessels B, C, and D each had 0.3 ml of ODE in one side arm. Vessel B, used for determining oxygen uptake, contained KOH in the center well; vessels C and D, used for determining initial bound and final total CO2, respectively, had 0.3 ml of 50 per cent citric acid in a second side arm. (Since catalytic decarboxylations were to be performed on the contents of C and D, care was taken when dumping the acid not to rinse out the side arm that had contained it, this side arm being used subsequently for the addition of aniline citrate.) The contents of vessels B, C, and D were mixed in the usual manner, and readings taken until no further pressure changes occurred. At this time the contents of vessel B were used for a Rothera test, which was strongly positive. Vessels C and D received an addition of aniline citrate to the side arm that had previously contained citric acid; following this addition, catalytic decarboxylations were performed, a control vessel being included in the series

5 1950] BACTERIAL OXIDATION OF AROMATIC COMPOUNDS 5301 to correct for volume changes. The results, calculated in terms of the total contents of the original vessel A, are presented in table 4. From this experiment, the following conclusions can be reached: first, the intermediate compound formed from protocatechuic acid by OE is enzymatically decarboxylated by ODE with a C02 evolution of approximately one mole per mole of protocatechuate originally oxidized, the decarboxylation not being accompanied by further oxygen uptake; second, the intermediate itself cannot be catalytically decarboxylated by aniline citrate; and, third, after enzymatic decarboxylation an amount of,t-ketoacid has been formed that is roughly equimolar with the amount of C02 released. The rate of catalytic decarboxylation by aniline citrate in vessel D was identical with that previously observed (Stanier, Sleeper, Tsuchida, and Macdonald, 1950) for,-ketoadipic acid; taken in conjunction with the characteristic violet Rothera reaction obtained with the con- TABLE 4 The enzymatic decarboxylation of the intermediate formed by the oxidation of protocatechuic acid Na-protocatechuate supplied: 12 micromoles MICRO_ OiMOLES/MOLE VESSEL REACTION OBSERVED MYICROLITERS MOLES PROTOCATECEUIC ACID A 02 uptake with nondecarboxylating enzyme system B Further 02 uptake on addition of decarboxy lating enzyme system D-C C02 production on addition of decarboxylating enzyme system C f3-ketoacid present before addition of decar boxylating enzyme system D j3-ketoacid present after action of decarboxy lating enzyme system D-C Net fb-ketoacid formed by decarboxylating enzyme system tents of vessel B after treatment with ODE, this provides convincing evidence that the product of the enzymatic decarboxylation is,b-ketoadipic acid. DISCUSSION The experiments described above clearly place the decarboxylative step in the transformation of protocatechuic acid to,b-ketoadipic acid after the oxidative step(s). Two pieces of evidence, taken in conjunction, show that the intermediate formed by the nondecarboxylative attack on protocatechuic acid must be a tricarboxylic acid: first, the concomitant production of two equivalents of acid; and, second, the nonoxidative enzymatic decarboxylation of the intermediate to I3-ketoadipic acid. Consequently, the first steps in the degradation of protocatechuic acid must involve oxidative rupture of the benzene ring with the production of an aliphatic, tricarboxylic acid containing seven carbon

6 ,5,302 R. Y. STANIER [VOL. 59 atoms. As yet the constitution of this acid has not been established, although we have produced several millimoles of it by the enzymatic degradation of protocatechuic acid. It is an extremely unstable compound, and we have been unable so far to isolate sufficient amounts in a pure state to permit of chemical characterization. However, the demonstration of its enzymatic decomposition to C02 and fb-ketoadipic acid limits the possibilities to a very small number of compounds. The most obvious possibility, already suggested previously on the basis of other considerations (Stanier, Sleeper, Tsuchida, and Macdonald, 1950), is malonosuccinic acid (Bi-keto,y-carboxyadipic acid). However, this compound appears to be eliminated by the fact that the intermediate is not decarboxylated by aniline citrate. Malonosuccinic acid, by analogy with oxalosuccinic acid (Ochoa, 1948), should be decarboxylated by this reagent. SUMMARY Cell-free enzyme preparations, capable of oxidizing protocatechuic acid to,b-ketoadipic acid, have been obtained by the aqueous extraction of dried, p- hydroxybenzoate-grown cells of Pseudomonas fluorescens. Such preparations completely lose their decarboxylative activity following thorough dialysis against distilled water, but their oxidative activity is only slightly affected by this treatment. Nondecarboxylating preparations oxidize protocatechuic acid with the formation of a tricarboxylic acid containing seven carbon atoms. On subsequent treatment with a decarboxylating enzyme preparation, this intermediate tricarboxylic acid is decomposed without oxygen uptake to carbon dioxide and jl-ketoadipic acid. REFERENCES OcHOA, S Biosynthesis of tricarboxylic acids by carbon dioxide fixation. I. The preparation and properties of oxalosuccinic acid. J. Biol. Chem., 174, SLEEPER, B. P., TsUCHIDA, M., AND STANIER, R. Y The bacterial oxidation of aromatic compounds. II. The preparation of enzymatically active dried cells, and the influence thereon of prior patterns of adaptation. J. Bact., 59, STANIER, R. Y., SLEEPER, B. P., TsUCHIDA, M., AND MACDONALD, D. L The bacterial oxidation of aromatic compounds. III. The enzymatic oxidation of catechol and protocatechuic acid to j3-ketoadipic acid. J. Bact., 59,

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