THE HYDROLYSIS OF STARCH BY HYDROGEN PEROXIDE AND FERROUS SULFATE*
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1 THE HYDROLYSIS OF STARCH BY HYDROGEN PEROXIDE AND FERROUS SULFATE* BY W. R. BROWN (From Ihe Laboratory of Biochemistry, University of Cincinnati, Cincinnati) (Received for publication, November 21, 1935) In 1924 Mathews (1) expressed the view that all matter exists in two forms, stable and reactive, due to the energy content of the molecule. On this basis he postulated that enzymes are substances which by their presence facilitate the transfer of energy from some external source to the substrate, thus raising its energy content and making it labile. The work of Hill (2), Boyd (3), and Sigal (4) from this laboratory has added evidence to support this view. Since oxygen is such a common source of energy for living matter, it is quite possible that amylase is a part of an oxidationreduction system, or is activated by such a system. On this hypothesis was based a series of experiments to ascertain just how closely the action of an oxidation-reduction chain upon starch parallels the action of amylase. Hydrogen peroxide and ferrous sulfate (Fenton s reagent) were chosen as a suitable oxidationreduction system for the basis of experimental study. Gatin-Grueewska (5) and Gerber (6), using hydrogen peroxide alone, and Durieux (7), using hydrogen peroxide and ferric chloride, had shown that starch is broken down by means of these substances with the formation of dextrins and reducing substances. All three concluded that the action was analogous to that produced by diastase. Omori (8), using several heavy metals with hydrogen peroxide upon starch, secured the hydrolysis, but concluded that the action was quite different from that of enzymes. * Part of a dissertation submitted to the Graduate School of the University of Cincinnati in partial fulfilment of the requirements for the degree of Doctor of Philosophy, June,
2 418 Starch Hydrolysis by H,O, and FeS04 EXPERIMENTAL The experiments were carried out according to the following scheme: 10 cc. of a 1 per cent soluble starch (Kahlbaum) solution, 2 cc. of acetate buffer (ph 3.8), 10 cc. of 1 per cent hydrogen peroxide (commercial 30 per cent diluted to 1 per cent), and 2 cc. of 0.01 M ferrous sulfate in a large test-tube were covered with toluene and placed in a bath at 37. At various intervals small portions were removed and tested with dilute iodine and the optical rotation was observed. At other intervals small aliquots were taken and the acidity and cupric reducing power by the Bertrand method were noted. As the reaction proceeded, the solution became water-clear and greatly reduced in viscosity. There was considerable production of cupric reducing substances (Table I) and a continuous decrease in the optical rotation of the solution (Table II). The tube containing 2 cc. of ferrous sulfate showed a decrease in optical rotation of 15.3 per cent of the original rotation in 3 hours. The tube containing 4 cc. of ferrous sulfate showed a decrease of 84.0 per cent in the same time. 6 cc. caused a decrease of 84.8 per cent in the 24 hours, while 8 cc. effected a decrease of 82.7 per cent in 2 hours. The color produced by addition of dilute iodine changed from blue to red and finally to colorless as the reaction proceeded. The rate of splitting of starch was directly proportional t.o the amount of iron added (Table II). In addition to ferrous sulfate, which has been shown to be very active in the catalysis of the action of hydrogen peroxide on starch, several other salts, which show some catalytic action, were tested. Ferric salts are of the same order of efficiency as the ferrous. Copper and manganese salts are greatly inferior to the iron. Complex salts, ferro- and ferricyanides, have very little effect, while manganese dioxide has no effect whatever. The efficiency of these salts bears no relationship to their peroxidase activity as measured by the benzidine reaction. Copper is by far the most efficient as a peroxidase, ferrous and ferric iron being considerably weaker. Manganese, which is as effective in the catalysis of starch as copper, has practically no peroxidase action. Tests were made upon the solution to ascertain if the action were a true hydrolysis with the liberation of free glucose or maltose.
3 W. R. Brown 419 After the achromic point with iodine had been reached, the solution reduced alkaline copper sulfate in the cold. This indicated a much stronger reducing agent than the simple sugars. The addition of TABLE Production of Reducing Substances Reaction mixture: 10 cc. of 1 per cent starch, 2 cc. of acetate buffer (ph 3.8), 10 cc. of 1 per cent HzO,, 5 cc. of 0.01 M FeS04. Temperature Control, no HzOs, no FeSOa. H202, no FeS04.. Reaction mixture.. I I Experiment No. 1 (No Hdh) I Time 0.05 N KMnOa hrs. cc. mo CU Iodine reaction Blue Deep violet Colorless I I TABLE II Change in Optical Rotation during Reaction Reaction mixture: 10 cc. of 1 per cent starch, 2 cc. of acetate buffer (ph 3.8), 10 cc. of 1 per cent hydrogen peroxide, 0.01 M FeSOb added as indicated. Temperature 37. Water added to make total volume of 30 cc. - Iodine reaction Angle of rotation 2 E To 3 4 _- k hrs. iegrees hrs. d egrees hrs. degrees 20 Blue Red min 30 Colorless min. 15 Pink I Colorless phenylhydrazine caused the formation of an orange amorphous precipitate which turned brown on standing but could not be induced to crystallize. Glucose or maltose as such were not present. The solution was tested with fuchsin-sulfur dioxide
4 420 Starch Hydrolysis by H202 and FeS04 reagent and with sodium bisulfite for the presence of free aldehyde. Both of these tests were strongly positive, indicating that the simple sugars were further attacked with the liberation of a free aldehyde group. Neither hydrogen peroxide nor iron interferes with any of these tests. There was no change in these tests after the removal of hydrogen peroxide by the use of manganese dioxide. Added amounts of hydrogen peroxide or ferrous sulfate to these tests, carried out upon known solutions, had no effect. Concentration of the reaction mixture in vacua at 3040 gave a distinctly acid distillate which did not reduce alkaline copper and did not restore the color to fuchsin-sulfur dioxide, but gave a strong reduction of ammoniacal silver nitrate. This was concluded to be probably formic acid. There was considerable acidity left in the residual solution. The acidity and aldehyde tests are considerably increased by the addition of glucose or maltose to the reaction mixture. A solution of glucose or maltose, when treated with hydrogen peroxide and ferrous sulfate, increased in acidity and decreased in optical rotation. Formic acid and free aldehydes are produced. Phenylhydrazine does not give the characteristic osazone, but an amorphous precipitate which could not be induced to crystallize. These tests are identical with those given by the solution of starch after treatment with hydrogen peroxide and ferrous sulfate, and upon this basis the conclusion is reached that glucose, and possibly maltose, is formed in the course of the reaction only to be further hydrolyzed and oxidized to form acids and free aldehyde. By the use of ethyl alcohol, there may be precipitated from the reaction mixture substances which have the properties of the dextrins formed by the action of acids or enzymes upon starch (Table III). By precipitating these substances while the solution still produced a red color with iodine (i), there was obtained a gummy residue which was quite soluble in water. Dialysis of this solution for 10 days removed all cupric reducing power, but left a solution which gave a deep red color with iodine and showed considerable optical activity. [ffl%,, = 100 x x 1.15 = Hydrolysis of this substance gave a quantitative yield of glucose.
5 W. R. Brown TABLE Precipitation and Dialysis of Dextrins Precipitated from Reaction Soluble III starch (Treated with HzOz and FeS04 until red color is produced with I,) Clear Gatery Dialyzed CtH,OH (i) Residue Clear gummy mass Red color with I2 Strong reduction (Benedict s) I Dextrorotatory C2H60H solution + NaCl + N&l (ii) Residue (ii, A) (Same as above, rotation and reduction less) in cellophane i (i, A) Filtrate Filtrate (Combined with i, A, alcohol removed) Reduction Formic acid I Free aldehyde Acids I No osazone (f) Residual solution (v) Dialysate (iv) Residual solution Rotation less Reduction No reduction I Reduction less Dextrorotatory Less rotation 1 Red color with 12 1 No osazone Molisch + (No osazone 1 No osazone HCl (boiled) HCl (boiled) HCl (boiled) I Sugar solution Sugar solution Sugar solution More reduction More reduction Reduction i Less rotation Less rotation 1 Less rotation (Glucosazone formed Glucosazone formed [Glucosazone formed
6 422 Starch Hydrolysis by H,O, and FeSO, The concentrated diffusate (ii, Table III) from the dialysis of the erythrodextrin was found to possess considerable optical rotation and some reducing power. [al::,, = 100 x 1.0 = 1.0 x l&90 = 100 X = 1.0 x R (cupric reducing power) = 23.8 (maltose = 100) This is in fair agreement with the constants for amylotriose from bacterial degradation of starch, given by Pringsheim (9). [(Y]~& = , R = 22.5 (maltose = 100) Hydrolysis of this solution by dilute acid increased the reducing power and decreased the optical rotation to that of a solution of glucose, and from the hydrolyzed solution the characteristic crystals of phenylglucosazone were obtained. Precipitation of the original mixture, after the achromic point had been reached, yielded a gummy precipitate (i, Table III) as in the case of the erythrodextrin. This substance was soluble in water but gave no color with iodine. Prolonged dialysis removed all reducing power, but the solution still showed optical activity. l&,, = f, ; ;5 = Hydrolysis of this solution by acid caused a reduction of optical rotation and an increase in the cupric reducing power until these agreed with those of a solution of glucose. The diffusate (v) from the dialysis of the achroodextrin was found to possess the following constants. r&:,, = 100 X X 1.58 = R = 4.1 (maltose = 100) Hydrolysis of this solution increased the reducing power and decreased the optical rotation to some extent. This solution was
7 W. R. Brown undoubtedly a mixture of the oxidation products of glucose containing a small amount of a substance of high optical rotation. DISCUSSION Hydrogen peroxide and ferrous sulfate react with starch to produce a hydrolysis. The opalescence of the starch is lost, its viscosity and optical rotation are reduced, its ability to reduce alkaline copper is increased, and from the reaction there may be isolated dextrins and the oxidation products of the simple sugars. With the exception of the further oxidation of the simple sugars produced, these characteristics are identical with those produced by enzymic or acid hydrolysis of starch. On this fact is based the conclusion that the action of the system is a true hydrolysis, analogous to that produced by the amylolytic enzymes. The role of the metal in the reaction was adduced from several facts. First, the presence of iron or similar metal appears to be necessary for the hydrolysis. Although metal-free starch was not used in the experiments, the rate of the reaction without added metal was very slow, requiring several days to go to completion. The dependence of the rate of hydrolysis upon the amount of added iron (Table II) indicates that the complete removal of iron would cause the hydrolysis to be immeasurably slow. Iron has the ability to catalyze the decomposition of hydrogen peroxide as does heat and alkalinity. The fact that the ability of the metals to catalyze the hydrolysis of starch is not in the order of their ability to catalyze the decomposition of the peroxide indicates that the iron plays a part other than the mere liberation of energy from the peroxide. The decomposition of the peroxide by heat or alkalinity does not cause hydrolysis of the starch in a measure to be expected from the amount of energy liberated. The starch, peroxide, and iron must be in the same solution for the hydrolysis to occur, indicating a loose chemical union. That the union between the iron and starch is at the alcoholic group seems unlikely, since such compounds are formed only in alkaline solution. The logical point of attachment is through the residual valences of the oxygen of the glucoside linkage of the starch, for at this point the splitting occurs. In the light of these facts, it seems that the iron (or other metal), in addition to catalyzing the liberation of energy from the peroxide,
8 424 Starch Hydrolysis by H,Oz and FeS04 unites with the starch in a loose chemical union to pass the energy of the peroxide decomposition into the starch molecule. The energy level of the starch is thus raised, causing the starch to be reactive. The following theory of the mechanism of starch hydrolysis is thus advanced: The iron atom forms an unstable combination with the starch, possibly through the residual valences of the oxygen of the glucoside linkage. The iron gives up its energy to the starch molecule, thus raising the energy level of the starch molecule, and making it, more reactive. The iron, even in its highest energy level, does not contain enough energy to split the starch except, at a very slow rate. The decomposition of the peroxide produces large quantities of energy which is taken up to form activated iron, and the energy of the iron is passed into the starch molecule. The activated starch reacts with water and is hydrolyzed. Enough energy is put into the starch molecule to cause a quite rapid hydrolysis. The iron, upon giving up the energy to the starch molecule, reverts to a lower energy level, is again activated by the peroxide, and in turn passes this energy to another molecule of starch. The reaction is a true catalysis, since the iron left is available for many transfers of energy. This is in line with Warburg s (10) suggestion that FeIV is the form of iron in its active state. Fe -+ Fe --+ Fe 1, dextrins Fe + starch + Hz Fel + glucose 1 oxidation products The peroxide-iron-starch system appears to be identical with the hydrolytic enzymes except for the fact that the supply of available energy is limited to the amount of peroxide present, and the system may be called an artificial enzyme. SUMMARY The action of hydrogen peroxide and ferrous sulfate upon starch is a hydrolysis, producing in the course of the reaction dextrins, sugars of high molecular weight, and simple sugars. The reaction is analogous to that produced by amylase, differing only
9 W. R. Brown 425 in the fact that the simple sugars produced are further hydrolyzed and oxidized to acids and aldehydes. The reaction appears to be a true catalysis, the iron acting to transfer energy from the peroxide breakdown to the starch molecule, thus raising the energy level of the starch and causing it to be reactive. I wish to take this opportunity to express my sincere gratitude and appreciation to Dr. Albert P. Mathews for advice and assistance during the course of this study. To Mr. Charles G. Merrell I am deeply indebted for the donation of the William S. Merrell Fellowship. BIBLIOGRAPHY 1. Mathews, A. P., in Cowdry, E. V., General cytology, Chicago, 15 (1924). 2. Hill, E. S., J. Biol. Chem., 96,197 (1932). 3. Boyd, M. J., J. Biol. Chem., 103,249 (1933). 4. Sigal, A., Thesis, University of Cincinnati (1932). 5. Gatin-Gruzewska, M., Compt. rend. Sot. biol., 68, 1084 (1910). 6. Gerber, C., Compt. rend. Sot. biol., 72,1002 (1912). 7. Durieux, O., Bull. Sot. chim. Belgique, 27,90 (1913). 8. Omori, T., J. Biochem., Japan, 14, 339 (1931); 16,483 (1932). 9. Pringsheim, H., Ber. them. Ges., &I,1581 (1924). 10. Warburg, O., Science, 61,575 (1925).
10 THE HYDROLYSIS OF STARCH BY HYDROGEN PEROXIDE AND FERROUS SULFATE W. R. Brown J. Biol. Chem. 1936, 113: 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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