Enzymatic Hydrolysis of Barley Starch Lipids
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1 Enzymatic Hydrolysis of Barley Starch Lipids S. Shamekh, 1 A. Mustranta, 1 K. Poutanen, 1 and P. Forssell 1,2 ABSTRACT Cereal Chem. 75(5): The efficiency of phospholipase and lipase preparations in the hydrolysis of lysophospholipids of native and gelatinized barley starch was examined. The degree of hydrolysis was analyzed by determination of the amount of released fatty acids by an enzymatic method. Thermal and structural properties of the enzyme-treated starch were studied by differential scanning calorimetry and light microscopy. Lysophospholipids of the gelatinized barley starch were easily hydrolyzed, in contrast to the lipids of the granular starch. The maximum degree of hydrolysis achieved for the gelatinized starch was 80% and for the native starch 20%. Gelatinization enthalpies and micrographs indicated that even though the amount of the released fatty acids from the native starch was small, formation of free fatty acids inhibited swelling and gelatinization of starch granules. Cereal starches contain lipids in quantities generally proportional to their amylose content (Morrison 1988). In barley, wheat, and rye starches, the starch lipids are almost exclusively lysophospholipids (LPL), which have been shown to exist as amyloselipid inclusion complexes in native starch granules rather than being formed during starch gelatinization (Morrison et al 1993a,b). The LPL content of normal barley starch is 1%, and the predominant component is lysophosphatidylcholine (Acker and Becker 1971). About 20% of the amylose of normal barley starch is complexed with lipids (Morrison et al 1993b). The amylose-lipid complex has a single helical structure, usually consisting of six glucosyl residues per turn (Morrison 1995). The hydrocarbon chain of the lipid lies within the hydrophobic amylose tube, but the polar ends are outside the helix. The complex structure has been studied by X-ray diffraction, molecular modeling, and differential scanning calorimetry (DSC) (Kugimiya et al 1980, Biliaderis and Seneviratne 1990, Godet et al 1993, Karkalas et al 1995). Heating barley starch-water suspensions at > C induces dissociation of the amylose-lipid (AML) complex (Morrison et al 1993b). The dissociation of the AML complex is a reversible phenomenon, and reformation of the complex occurs during cooling. The endotherm observed on reheating usually has a different shape than the original endotherm and is shifted toward higher temperatures, indicating the formation of a different polymorphic form of the complex (Kugimiya and Donovan 1981, Eliasson and Krog 1985). Lipids affect many technologically important properties of starchcontaining foods by changing the granule swelling, solubilization, and crystallization of starch polymers (Morrison 1978, Morrison and Milligan 1982). There is some evidence that amylose complexed with LPL increases gelatinization temperature, whereas lipid-free amylose has an opposite effect (Morrison et al 1993b). The associated process of granule swelling is considerably reduced if lipids are present, by a mechanism that probably involves an AML complex (Tester and Morrison 1990, Tester et al 1991). The effects of native or added lipids on extrusion processing of various starches have been the subject of numerous investigations. The formation of AML complexes during twin-screw extrusion of corn starch and soft wheat flour has been reported to decrease both starch solubility and the susceptibility of the extrudates to α-amylase digestion (Mercier 1980, Galloway et al 1989). The presence of added oleic acid in twin-screw extrusion of wheat flour decreased paste viscosity of the extruded wheat flour (Schweizer et al 1986). In glucose syrup production, the minor components of starch, such as 1 VTT Biotechnology and Food Research, PO Box 1500, FIN VTT Finland. 2 Corresponding author. Pirkko.Forssell@vtt.fi Phone: Fax: Publication no. C R American Association of Cereal Chemists, Inc. lipids and proteins, may affect filtration rates and the final syrup quality (Bowler et al 1985). The accessibility of barley starch to α-amylase during different phases of gelatinization was studied in our laboratory by Lauro et al (1993). We also have studied the enzymatic hydrolysis of oat and soybean lecithin in relation to their functional properties (Aura et al 1994) and compared lipases and phospholipases in the hydrolysis of phospholipids (Mustranta et al 1995). Studies on enzymatic hydrolysis of LPL complexed with amylose have not been reported earlier. The aim of this work was to study the enzymatic accessibility of LPL of granular and gelatinized barley starch. MATERIALS AND METHODS Substrates Barley starch was of commercial origin (Primalco Ltd, Finland). Gelatinized barley starch was made by heating a 50% (w/w) starchwater dispersion for 15 min at 90 C and subsequent freeze-drying. Lysophosphatidylcholine (L-4129) was purchased from Sigma (St. Louis, MO). Enzymes The enzyme preparations used for the hydrolysis of LPL were phospholipase A1 and lipase (Biocatalysts, Ltd, Pontypridd, Great Britain). Both preparations were mixtures of enzymes containing a rather high lysophospholipase activity in addition to lipase and phospholipase activities. The lysophospholipase activities of these two enzyme preparations were determined using lysophosphatidylcholine (Sigma L-4129) as a substrate (Mustranta et al 1995). The liquid phospholipase A1 and powdered lipase preparations contained lysophospholipase activity of 500 nkat/ml and 14,000 nkat/g, respectively. The enzymes were dosed as lysophospholipase activity units (100 20,000 nkat/g of LPL). Hydrolysis of Lysophospholipids The hydrolytic reaction was done using 0.1% lysophosphatidylcholine or 1% native or gelatinized barley starch as the substrate in 50 mm acetic acid buffer, ph 5. The reaction mixture contained 5 ml of substrate solution and ml of enzyme dilution ( nkat/g of LPL). The reaction was done at 40, 50,and 60 C with magnetic stirring for 4 hr. The free fatty acids liberated were immediately analyzed with an enzymatic test kit (Boehringer Mannheim ). The solid residue was freezedried and used for microscopic and calorimetric studies. Microscopy Enzymatically treated native barley starch and control samples were suspended in distilled water, smeared onto an object glass, and viewed under an Olympus Vanox-T microscope using polarized light. 624 CEREAL CHEMISTRY
2 Fig. 1. Effect of enzyme concentration on the degree of hydrolysis of lysophospholipids (LPL) in water and on gelatinized and native barley starch dispersions at 40 C, when using phospholipase A1 (A) and lipase (B) preparations as the catalyst. = LPL dispersion; = native barley starch; n = gelatinized barley starch. Thermal Transitions The effects of enzymatic treatment on the thermal properties of barley starch were studied by DSC (Mettler DSC 30, Switzerland). Starch samples (3 7 mg, dwb) were weighed into medium pressure pans (Mettler ME-26929); water was added and mixed; and the pans were sealed and reweighed. The water content was 70% (w/w), and an empty pan was used as a reference. The pans were heated by DSC from 10 to 150 C with a scanning rate of 10 C/min. Three replicates were analyzed for each sample. Fig. 2. Effect of reaction temperature on the degree of hydrolysis of lysophospholipids (LPL) in water (white bar) and of gelatinized and native barley starch dispersions (black and gray bars, respectively), when using phospholipase A1 (A) and lipase (B) preparations as the catalyst (20,000 nkat/g of LPL). Statistical Analysis Statistical significance of the results was analyzed using singlefactor analysis of variance (ANOVA). Multiple comparisons were performed by least significant difference after a preliminary F- test. All tests were conducted at the 5% significance level. RESULTS AND DISCUSSION Effect of Hydrolysis Conditions The effects of enzyme concentration (100 20,000 nkat/g of LPL) on hydrolysis of LPL in water-dispersion and in native and gelatinized barley starch were studied at 40 C. The enzymes used were phospholipase A1 and lipase preparations, and the reaction time was 4 hr. LPL in water dispersion was readily hydrolyzed by both enzymes under the hydrolysis conditions used (Fig. 1A and B). About 90% of the LPL was hydrolyzed within 4 hr at the highest enzyme concentration using the phospholipase A1 preparation (Fig. 1A), and 77% was hydrolyzed using the lipase preparation (Fig. 1B). The extent of hydrolysis of LPL of gelatinized barley starch was almost as high as for the LPL dispersion. At the highest enzyme dosage the extent of hydrolysis of gelatinized barley starch was 75% by phospholipase A1 and 68% by the lipase preparation (Fig. 1A and B). The lipids in the native barley starch were difficult to hydrolyze. The highest degrees of hydrolysis were only 8.3 and 4% at 40 C for phospholipase A1 and lipase preparations, respectively (Fig. 1A and B). The results indicated that the lipase preparation was somewhat less effective than the phospholipase A1 preparation in the hydrolysis of lysophosphatidylcholine in all the substrates studied. In a previous study (Mustranta et al 1994) lipase preparations were more efficient than phospholipase A1 and Fig. 3. Calorimetric thermograms of native barley starch (A) and enzyme-treated barley starches at 40 (B), 50 (C), and 60 C (D). A2 preparations in the hydrolysis of soybean phosphatidylcholine. The effects of reaction temperatures was studied using the highest enzyme concentration of both enzyme preparations (20,000 nkat/g of LPL). The formation of fatty acids was only slightly affected by the reaction temperature. When the temperature was increased from 40 to 50 C, the degree of hydrolysis of barley starch LPL increased significantly (P < 0.05), but further increase in temperature did not affect the hydrolysis significantly (Fig. 2A and B). The extent of hydrolysis was higher with phospholipase A1 than with the lipase preparation. Using the phospholipase A1 preparation, 21% of the LPL of native barley starch was hydrolyzed at 50 C (Fig. 2A), whereas only 8.8% was hydrolyzed using the lipase preparation (Fig. 2B). At 60 C with the phospholipase A1 preparation as the catalyst, LPL dispersed in water was almost completely hydrolyzed (95%), and more than 80% of LPL in the gelatinized starch was hydrolyzed (Fig. 2A). Effect of Substrate Type The results regarding enzyme concentrations and temperature revealed that the LPL of the granular barley starch was much more Vol. 75, No. 5,
3 Fig. 4. Effects of enzyme treatment on the dissociation enthalpy of amylose-lipid complexes (AML) and on the gelatinization enthalpy of barley starch (phospholipase A1 preparation). = AML contol; _ = gelatinization contol; = gelatinization sample; n = AML sample. the granule structure. Amylose and AML have been assumed to be located in the amorphous regions of the granule, with increasing amounts from the hilum to the surface (Morrison 1995). Above room temperature, starch granules swell due to water diffusion inside the structure, and at 50 C a small amount of starch begins to diffuse into the surrounding water. The swelling starts from the hilum of the granule. The extent of swelling of barley starch granules has been observed to be much greater at 60 C than at 40 C (Tester and Morrison 1990). In this work, the degree of LPL hydrolysis in native starch increased significantly (P < 0.05) with increasing temperature from 40 to 60 C but was still rather small at 60 C (23%). This result indicated that LPL hydrolysis does not really occur before AML diffuses outside the granule. Fig. 5. Smear of barley starch-water dispersion of the control sample (A) and enzyme-hydrolyzed sample (B) treated at 40 C. difficult to hydrolyze than the LPL of gelatinized barley starch. This difference is understandable considering that the hydrolysis was inside the granule as compared with that in dilute water dispersion, but it was somewhat surprising that the LPL of the gelatinized starch was almost as easily hydrolyzed as the LPL in the water dispersion. Enzyme-catalyzed reactions take place through enzymesubstrate complexes. Lipases are able to catalyze reactions of a broad range of substrates containing an ester linkage. Ever though they exist in complexes with amylose, the lipids of the gelatinized starch in dilute water dispersion were hydrolyzed, indicating that the complex was flexible. The low enzymatic accessibility of the native barley starch was due to the high substrate concentration inside the granule and to Properties of Lysophospholipase-Treated Barley Starch The effects of lysophospholipase treatment on the microstructure and thermal properties of barley starch granules were studied using light microscopy and DSC. Some examples of the calorimetric thermograms (Fig. 3) demonstrate that the gelatinization endotherm was between 63 and 77 C and that the endothermic transition due to AML dissociation was at 100 C. The incubation temperature was observed to increase the peak temperature of the gelatinization and to narrow the gelatinization temperature range (Fig. 3). The barley starch treated by the enzyme at 40 C had a gelatinization enthalpy of 8.5 J/g and an AML dissociation enthalpy of 1.3 J/g, as compared with the values of the native starch, 12 J/g and 1.4 J/g, respectively. With increasing reaction temperature, the extent of gelatinization increased (Fig. 4). A small decrease in the AML-dissociation enthalpy was also observed due to hydrolysis of the LPL, confirming that the observed endotherms were due to dissociation of AML (Fig. 4). Incubation at C did not affect the enthalpy of the AML control sample, but the starch control sample was clearly more gelatinized at 60 C than the enzyme-treated starch. The gelatinization peak temperature of the starch treated enzymatically at 60 C was also significantly higher (70.5 C) than that of native barley starch (63.1 C). No remarkable changes occurred in starch granules during incubation for 4 hr at 40 C; only a few granules were swollen and had lost their birefringence (Fig. 5). At 50 C, granules of the control sample were slightly deformed (Fig. 6A), were more swollen, and had lost their birefringence more often than those of enzymetreated sample (Fig. 6B). Similar results were obtained using the lipase preparation at 40 and 50 C (results not shown). At 60 C, most of the granules of the control sample had lost their birefringence, and very few intact granules were observed (Fig. 7A), whereas in the enzyme treated sample (Fig. 7B), many intact (ungelatinized) granules were observed. Thus, at all reaction temperatures, granules of the enzymetreated starch were less swollen than those of the control starch, 626 CEREAL CHEMISTRY
4 Fig. 6. Smear of barley starch-water dispersion of the control sample (A) and enzyme-hydrolyzed sample (B) treated at 50 C. Fig. 7. Smear of barley starch-water dispersion of the control sample (A) and enzyme-hydrolyzed sample (B) treated at 60 C and, based on the calorimetric transitions, the enzyme-treated starch had higher gelatinization enthalpies than the control sample at 50 and 60 C. This indicated that, at these temperatures, less gelatinization occurred in the presence of the enzymes. The changes in AML endotherm correlated with the degree of hydrolysis of LPL. Earlier studies have shown that the swelling of wheat starch granules during heating was delayed in the presence of fatty acids and emulsifiers (Eliasson 1985). The lower degree of swelling and gelatinization of the enzyme-treated native starch as compared with the control starch must have been due to the released fatty acids. The limited swelling may also explain why the degree of hydrolysis of the native starch did not increase more when the temperature was increased from 50 to 60 C. CONCLUSIONS The amylose-bound LPL of barley starch can be hydrolyzed by enzymes after gelatinization of starch. Both phospholipase A1 and lipase preparations containing lysophospholipase activity were capable of catalyzing the hydrolysis. The degree of hydrolysis was almost as high as for pure LPL dispersed in water, which could indicate flexibility of the AML complex molecule in dilute water dispersions. LPL of the barley starch granules was hydrolyzed only slightly, due to the very tight and organized granular structure. Despite the low extent of hydrolysis of the barley starch granules, the degree of the gelatinization decreased significantly due to the hydrolyzed LPL. This information may be useful when elucidating barley starch granular structure. The result, which may be exploited by the starch processing industry was that barley starch lipids could be hydrolyzed to fatty acids and glycerol phosphocholine after AML had diffused outside the granule. ACKNOWLEDGMENTS We thank Karin Autio for helping with interpretation of the micrographs. LITERATURE CITED Acker, L., and Becker, G Neuere Untersuchungen über die Lipide der Getreidestärken. Staerke 23: Aura, A. M., Forssell, P., Mustranta, A., Suortti, T., and Poutanen, K Enzymatic hydrolysis of oat and soya lecithin: Effects on functional properties. J. Am. Oil Soc. 71: Biliaderis, C. G., and Seneviratne, H. D On the supermolecular structure and metastability of glycerol monostearate-amylose complex. Carbohydr. Polym. 8: Bowler, P., Towersey, P. J., and Galliard, T Some effects of the minor components of wheat starch on glucose syrup production. Starch/Staerke 37: Eliasson, A.-C Starch gelatinization in the presence of emulsifiers. A morphology study of wheat starch. Starch/Staerke 37: Eliasson, A.-C., and Krog, N Physical properties of amylosemonoglyceride complexes. Cereal Sci. 3: Galloway, G. I., Biliaderis, C. G., and Stanley, D. W Properties and structure of amylose-glyceryl monostearate complexes formed in solution or on extrusion of wheat flour. Food Sci. 54: Godet, M. C., Tran, V., Delage, M. M., and Buleon, A A molecular modelling of the specific interactions involved in amylose complexation by fatty acids. Int. J. Biol. Macromol. 15: Karkalas, J., Ma, S., Morrison, W. R., and Pethrick, R. A Some factors determining the thermal properties of amylose inclusion complexes with fatty acids. Carbohydr. Res. 268: Kugimiya, M., and Donovan, J. W Calorimetric determination of the amylose content of starches based on formation and melting of the amylose-lysolecithin complex. J. Food Sci. 46: Kugimiya, M., Donovan, J. W., and Wong, R. Y Phase transitions Vol. 75, No. 5,
5 of amylose-lipid complexes in starches: A calorimetric study. Starch/ Staerke 32: Lauro, M., Suortti, T., Autio, K., Linko, P., and Poutanen, K Accessibility of barley starch granules to α-amylase during different phases of gelatinization. Cereal Sci. 17: Mercier, C Structure and digestibility alterations of cereal starches by twin screw extrusion cooking. Pages in: Food Process Engineering, Vol. 1. P. Linko, J. O. Malkki, and J. Larinkari, eds. Applied Science: London. Morrison, W. R Cereal lipids. Pages in: Advances in Cereal Science and Technology, Vol. II. Y. Pomeranz, ed. Am Assoc. Cereal Chem.: St. Paul, MN. Morrison, W. R Lipids in cereal starches: A review. Cereal Sci. 8:1-15. Morrison, W. R Starch lipids and how they relate to starch granule structure and functionality. Cereal Chem. 40: Morrison, W. R., and Milligan, T. P Lipids in maize starches. Pages 1-18 in: Maize: Recent Progress in Chemistry and Technology. G. E. Inglett, ed. Academic Press: New York. Morrison, W. R., Law, R. V., and Snape, C. E. 1993a. Evidence for inclusion complexes of lipids with V-amylose in maize, rice and oat starches. Cereal Sci. 18: Morrison, W. R., Tester, R. F., Snape, C. E., Law, R. V., and Gidley, M. J. 1993b. Swelling and gelatinization of cereal starches. IV. Some effects of lipid-complexed amylose and free amylose in waxy and normal barley starches. Cereal Chem. 70: Mustranta, A., Forssell, P., Aura, A. M., Suortti, T., and Poutanen, K Modification of phospholipids with lipases and phospholipases. Biocatalysis 9: Mustranta, A., Forssell, P., and Poutanen, K Comparison of lipases and phospholipases in hydrolysis of phospholipids. Process Biochem. 30: Schweizer, T. F., Reimann, S., Solms, J., and Eliasson, A.-C Influence of drum drying and twin screw extrusion cooking on wheat carbohydrates. II. Effect of lipids on physical properties, degradation and complex formation of starch in wheat flour. Cereal Sci. 4: Tester, R. F., and Morrison, W. R I. Swelling and gelatinization of cereal starches. I. Effects of amylopectin, amylose and lipids. Cereal Chem. 67: Tester, R. F., South, J. B., Morrison, W. R., and Ellis, R. P The effects of ambient temperature during the grain fill-in period on the composition and properties of starches from four barley genotypes. Cereal Sci. 13: [Received November 27, Accepted May 12, 1998.] 628 CEREAL CHEMISTRY
TABLE I 24-hr Annealing: Effect of Annealing Temperature (0 C) on Gelatinization Characteristics of Normal and Waxy Maize Starch Primary Endotherm
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