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Purification and Properties of the Inducible Coenzyme A-Linked Butyraldehyde Dehydrogenase from Clostridium Acetobutylicum NEIL R

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Purification and Properties of the Inducible Coenzyme A-Linked Butyraldehyde Dehydrogenase from Clostridium Acetobutylicum NEIL R JOURNAL OF BACTERIOLOGY, JUlY 1988, p. 2971-2976 Vol. 170, No. 7 0021-9193/88/072971-06$02.00/0 Copyright © 1988, American Society for Microbiology Purification and Properties of the Inducible Coenzyme A-Linked Butyraldehyde Dehydrogenase from Clostridium acetobutylicum NEIL R. PALOSAARI* AND PALMER ROGERS Department of Microbiology, University of Minnesota, Minneapolis, Minnesota 55455 Received 13 November 1987/Accepted 25 March 1988 The coenzyme A (CoA)-linked butyraldehyde dehydrogenase (BAD) from Clostridium acetobutylicum was characterized and purified to homogeneity. The enzyme was induced over 200-fold, coincident with a shift from an acidogenic to a solventogenic fermentation, during batch culture growth. The increase in enzyme activity was found to require new protein synthesis since induction was blocked by the addition of rifampin and antibody against the purified enzyme showed the appearance of enzyme antigen beginning at the shift of the fermentation and increasing coordinately with the increase in enzyme specific activity. The CoA-linked acetaldehyde dehydrogenase was copurified with BAD during an 89-fold purification, indicating that one enzyme accounts for the synthesis of the two aldehyde intermediates for both butanol and ethanol production. Butanol dehydrogenase activity was clearly separate from the BAD enzyme activity on TEAE cellulose. A molecular weight of 115,000 was determined for the native enzyme, and the enzyme subunit had a molecular weight of 56,000 indicating that the active form is a homodimer. Kinetic constants were determined in both the forward and reverse directions. In the reverse direction both the V,ax and the apparent affinity for butyraldehyde and caproaldehyde were significantly greater than they were for acetaldehyde, while in the forward direction, the Vmax for butyryl-CoA was fivefold that for acetyl-CoA. These and other properties of BAD indicate that this enzyme is distinctly different from other reported CoA-dependent aldehyde dehydrog- enases. Recently, there has been renewed interest in the obligate possible since the assay and stability problems have been anaerobe Clostridium acetobutylicum and its ability to fer- overcome. ment carbohydrates to acetone, butanol, and ethanol (21). We report here the induction of BAD activity and enzyme From an applications point of view, it is important to protein in cells just prior to solvent production and the maximize the efficiency of production of desired products purification and properties of BAD. We conclude that the and to be able to control the ratios of products based on CoA-linked BAD is most likely the branch-point enzyme for demand (2). To this end it is essential to understand the both ethanol and butanol synthesis from acetyl-CoA and regulation of the activity and the amount of the key enzymes butyryl-CoA. Furthermore, the properties of the BAD from that catalyze the fermentation. It has been known for some C. acetobutylicum indicate that it is significantly different time that, during this saccharolytic fermentation, C. aceto- from other reported CoA-linked aldehyde dehydrogenases. butylicum undergoes a shift from producing acetate and (Parts of this study were reported earlier [N. Palosaari and butyrate to forming butanol, ethanol, and acetone (10). The P. Rogers, Fed. Proc. 46:2293, 1987].) biochemical pathways for both modes of fermentation have been defined in a general way, and there has been some work MATERIALS AND METHODS done on elucidating the signals which affect the shift from Materials. Butyryl phosphate was synthesized with buty- acidogenic to solventogenic fermentation (for reviews, see ric anhydride (Eastman Kodak Co., Rochester, N.Y.) and references 17 and 21). Significant progress has been reported K2HPO4 and crystallized to greater than 95% purity by the on the analysis of the enzyme activities involved in the method of Stadtman (reference 27, procedure B) for the acidogenic stage of fermentation, in particular, the acyl preparation of acetyl phosphate. All aldehydes were ob- kinases and phosphoacetyltransferases from C. acetobutyli- tained from Aldrich Chemical Co. (Milwaukee, Wis.); cum and other clostridia that are involved in acetate and acetyl-CoA, reduced CoA (CoASH), NAD, NADH, NADP, (5, 12, 13, 26, 28-30). However, only the butyrate synthesis NADPH, and Reactive Blue-2 affinity gel were from Sigma coenzyme A (CoA)-linked aldehyde dehydrogenases from Chemical Co. Mo.); and Bio-Gel P200, Cellex T, Clostridium kluyveri (19, 25) and Escherichia coli (8, 9, 23, (St. Louis, and protein dye reagent were from Bio-Rad Laboratories 24) have been purified and characterized extensively, and (Richmond, Calif.). they are quite different than the enzyme butyraldehyde Preparation of butyryl-CoA. Butyryl-CoA was prepared dehydrogenase (BAD) from C. acetobutylicum that we re- enzymatically from butyryl phosphate by using the phos- port here. Preliminary studies of BAD activity changes phate butyryltransferase (PBT; butyryl-CoA:orthophos- during fermentation by C. acetobutylicum have been re- phate butyryltransferase [EC 2.3.1.19]) from C. acetobutyli- ported (1, 13), although it was apparent that there were cum. The equilibrium of this reaction favors butyryl-CoA difficulties with the assay conditions. Similarly, studies on formation (Keq = 74 [26]). The partially purified PBT was the alcohol dehydrogenases of Clostridium beijerinkii (Clo- isolated from the same Cellex T column that was used to stridium butylicum) (16) and C. acetobutylicum (22) are now purify BAD. The PBT-active fractions were pooled, concen- trated, and applied to a P200 column as described below for BAD. The PBT-active fractions from the P200 column were * Corresponding author. pooled and used for the preparation of butyryl-CoA. The 2971 2972 PALOSAARI AND ROGERS J. BACTERIOL. preparative reaction (volume, 1.0 ml) contained potassium cell concentrator (Amicon) by using a PM10 tnembrane. The N-(morpholinopropionyl)sulfonate (MOPS; pH 7.0; 50 pool was then applied to a column (2.5 by 45 cm) of Bio-Gel ,umol), CoASH (4 ,umol), butyryl phosphate (6 imol), and P200 equilibrated with KPM buffer, and the column was partially purified PBT (5 U; see below). The reaction was eluted with the same buffer. incubated for about 5 min at room temperature and moni- (iv) Affinity gel chromatography. The active fractions from tored spectrophotometrically at 233 nm to determine com- the gel filtration column were pooled and made to 40 mM pletion of the reaction. The butyryl-CoA was separated from KCI by adding the solid salt. The pool was then applied PBT by dialysis in a centrifugal dialysis apparatus (Centricon slowly (about 10 ml/h) to a column (1.5 by 7.5 cm) of 30; Amicon Corp., Lexington, Mass.). The effluent with the Reactive Blue-2 affinity gel which had been equilibrated with butyryl-CoA was acidified with 6 N HCI to hydrolyze the 40 mM KCI in KPM buffer. The column was then washed remaining butyryl phosphate (2 min at pH between 2 and 4) stepwise with 15 ml each of KPM buffer containing 50 mM and then neutralized with 1 M MOPS to pH 7.0. The yield of KCI, 100 mM KCI, and 150 mM KCI. The enzyme activity butyryl-CoA was quantitated by ion-paired, reversed-phase was then eluted from the column with 20 ml of KPM buffer high-performance liquid chromatography (3). High-perfor- containing 200 mM KCl and 5 mM NAD. mance liquid chromatography was performed on a C18 Storage. The active fractions from the affinity column were column (4.6 mm by 25 cm; 10-,um-diameter particles), with pooled, and glycerol was added to 25% (vol/vol). The pool 10 mM tetrabutylammonium phosphate as the ion-pairing was then divided into 0.5-ml samples, quick-frozen on dry agent, in aqueous methanol (45% [vol/vol] methanol) at pH ice, and stored at -80°C. The activity of purified BAI) 6.0. The column was eluted isocratically at 1.0 ml/min. remained stable for several months under these conditions. Conversion of CoA to butyryl-CoA was consistently 94%, as Polyacrylamide gel electrophoresis. Nondenaturing poly- determined by high-performance liquid chromatography. acrylamide gel electrophoresis was performed in 7.5% acryl- Recovery after dialysis and acidification was typically 70 to amide gels with 15 mM potassium barbital buffer (pH 8.5) 80%. containing 5 mM 2-mercaptoethanol and 0.1 M sucrose at Organism and growth conditions. C. acetobutylicum B643 4°C for 3 to 3.5 h and 150 V. Sodium dodecyl sulfate- was obtained from L. K. Nakamura (Northern Regional polyacrylamide gel electrophoresis was done by the proce- Research Center, Peoria, Ill.). Cells were grown in yeast dure of Laemmli (18). Silver staining was done by the extract medium (YEM), which consisted of the glucose- procedure of Guevara et al. (11). minimal medium of O'Brien and Morris (20), without biotin Enzyme assays. Aldehyde dehydrogenase activity was or p-aminobenzoic acid, and supplemented with yeast ex- measured in the reverse direction (aldehyde-oxidizing direc- tract (8 g), casein hydrolysate (2.2 g), asparagine (1.0 g), and tion; see Table 3) in 1.0-ml reaction mixtures containing cysteine (0.5 g). The pH was adjusted to 7.0. Cultures were potassium 2-(N-cyclohexylamino)ethane sulfonate (CHES; grown and maintained under anaerobic conditions as de- pH 9.0; 50 ,umol), NAD (1.0 ,umol), dithiothreitol (10 ,umol), scribed previously (22). Larger cultures (12 liters of YEM CoA (reduced form; 0.2 ,umol), protein (2.5 to 250 jig), and with 5% glucose) were inoculated with 120 ml of exponen- butyraldehyde or another aldehyde (10 ,umol). The assay tially growing cells and grown in a 16-liter fermentor (New solutions were preincubated for 10 min at room temperature Brunswick Scientific Co., Inc., Edison, N.J.), which was before the reaction was initiated by the addition of aldehyde. stirred continuously at 100 rpm under an anaerobic atmo- Enzyme activity was measured by NADH formation, as sphere (5% hydrogen, 10% carbon dioxide, and 85% nitro- determined by measuring the increase in the A340 (14) on a gen) for 20 h.
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