Enhanced production of intracellular dextran dextrinase from Gluconobacter oxydans using statistical experimental methods

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1 Afrcan Journal of Botechnology Vol. 9(8), pp , February, 010 Avalable onlne at ISSN Academc Journals Full Length Research Paper Enhanced producton of ntracellular dextran dextrnase from Gluconobacter oxydans usng statstcal expermental methods Xangzhao Mao #, Xaotong Lang 1,#, Shu Wang, We Dong 1,, Yanlong Xng, Huale Wang, Lzhong Guo 1 * and Dongzh We,3 * 1 Shandong Provnce Key Lab of Appled Mycology, Qngdao Agrcultural Unversty, Chna. Key Laboratory of Bofuels, Qngdao Insttute of Boenergy and Boprocess Technology, Chnese Academy of Scences, Chna. 3 State Key Laboratory of Boreactor Engneerng, East Chna Unversty of Scence and Technology, Chna. Accepted 14 January, 010 Optmzaton of the fermentaton medum for DDase producton by Gluconaobacter oxydans M5 was carred out n the shake flasks usng two knds of statstcal methods. Four varables, namely glucose, tryptone, yeast extract and sodum chlorde, were found to nfluence DDase producton sgnfcantly by the Plackett-Burman screenng. A four-factor fve-level central composte desgn (CCD) was chosen to explan the combned effects of the four medum consttuents. The optmum medum conssted of glucose ( g/l), maltobose (30 g/l), tryptone (1.198 g/l), yeast extract (13.58 g/l), ammonum ntrate (15 g/l), copper sulfate (0.01 g/l), znc sulfate (0.01 g/l), and sodum chlorde (0.009 g/l); the ntal ph 6.0 was set pror to sterlzaton. The DDase yeld obtaned from optmzed medum ncreased by 17-fold (0.38 U/mL) or so. Under these optmal condtons, the expermental values agreed wth the predcted values, ndcatng that the chosen method of optmzaton of medum composton was effcent, relatvely smple, tme reducng and materal savng. Key words: Dextran dextrnase, Gluconobacter oxydans, medum optmzaton, Plackett-Burman desgn, central composte desgn. INTRODUCTION Dextran, whch s syntheszed from sucrose by the dextran sucrase (EC.4.1.5, DSase) of Leuconostoc mesenterodes, s wdely used n pharmaceutcal and bochemcal felds (Mountzours et al., 1999; Robyt and Walseth, 1979; Sdebotham, 1974). Dextran dextrnase (EC.4.1.), produced by Gluconobacter oxydans, could also convert maltoolgosacchardes to dextran (Hehre, 1951), whch have consecutve (1,6)-lnked glucose resdues n the *Correspondng author. E-mal: lzguo@qau.edu.cn and dzhwe@ecust.edu.cn. Tel: and Fax: Abbrevatons: DDase, Dextran dextrnase; CCD, central composte desgn; DSase, dextran sucrase; NPG, p- ntrophenyl--d-glucopyranosde; R, determnaton coeffcent; RSM, response surface methodology. #These authors contrbuted equally to ths paper man chans and a wealth of (1,4), (1,3) and (1,)- branch lnkages (De Muynck et al., 007; Mountzours et al., 1999). Yamamoto et al. purfed the ntracellular DDase from G. oxydans ATCC11894 and reported three dfferent transglucosylaton modes of the DDase enzyme (Yamamoto et al., 199, 1993a). The dfference n structure between Gluconobacter and Leuconostoc dextran had been further studed and G. dextran could be used as a detary fbre (Yamamoto et al., 1993b). Furthermore, G. dextran was used not only as a fat replacer n acceptable low-fat foods but also for taste mprovement of the btter-sweet compound stevosde (Sms et al., 001; Yamamoto et al., 1994). What s more, G. dextran dsplayed shear-thnnng flow behavor (Naessens, 003). Accordng to the former research, the novel polysaccharde dsplayed lower vscosty than L. mesenterodes dextran of smlar molecular weght as a consequence of ts hgher degree of branchng, and t mght be sutable for certan food applcatons not asso-

2 Mao et al cated wth thckenng functonalty, such as a source of detary fbre or a low-calore bulkng agent for sweeteners (Naessens et al., 005). Above all, G. oxydans DDase could promse alternatves to L. mesenterodes DSase as bocatalysts for the synthess of dextran and olgodextrans. But the enzyme system had been studed far less extensvely than the glucosyltransferase of L. mesenterodes. In our group, G. oxydans have been studed for about 0 years n the applcatons of ncomplete oxdaton, such as syntheszng L-rbulose, D-tagatose, mgltol and chral aldehydes (Gao et al., 006; Gao and We, 006; Yang et al., 008). In the process of these studes, we have found the stran also has the potental ablty of nterconvertng between maltodextrns and dextran. It s known to all that changng envronmental factors, such as the medum composton and the concentraton of nutrent, can lead to an ncrease of DDase producton. The development of an economcally productve medum requres selectng carbon, ntrogen, on and trace element sources. And there were two ways by whch the problem of medum component lmtatons may be addressed: classcal and statstcal (Mao et al., 007). As for the classcal expermental desgn, there are several lmtatons towards complete optmzaton. Moreover, medum optmzaton by sngle dmensonal search needs a great deal of experments to determne optmum levels, whch are unrelable. Furthermore, t was hard to evaluate the relatve sgnfcance and the presence of complex nteractons of several affectng factors (Kammoun et al., 008; Mao et al., 007; Tan et al., 010). Compared wth the classcal method, the statstcal expermental desgn n the fermentaton medum optmzaton exhbts ts advantages, ncludng more advanced results wth less process varablty, closer confrmaton, less development tme and less overall costs. In ths study, medum optmzaton for producton of ntracellular DDase by G. oxydans was reported to make t clear that fermentaton factors nfluenced the DDase yeld under statstcal expermental desgn. MATERIALS AND METHODS Mcroorgansm The stran G. oxydans M5 was stored as 1 ml alquots n 0% glycerol at -7 C. The frozen cultures were plated perodcally to control ther vablty. Medum and growth condtons The G. oxydans grew n a medum contanng 80 g of D-sorbtol, 0 g of yeast extract, g of KH PO 4 and 0.5 g of MgSO 4 7H O n 1 L of deonzed water. The ntal ph was set at 6.0 pror to sterlzaton. The organsm was ncubated at 30 C at 00 rpm n a rotary shaker for 4 h. After 4 h cultvaton, 5 ml of the seed culture was used to noculate 50 ml of producton medum n a 50 ml glass flask and ths culture was grown under the same condtons as the seed culture. In the optmzaton process, the amounts of every component were changng n dfferent expermental processes. All the experments were carred out n three parallel tests. DDase assay The extracton method of G. oxydans DDase was as descrbed n the former research by Yamamoto et al. (199). The G. oxydans DDase actvty was determned n accordance wth the method descrbed by Naessens et al. wth some modfcatons (Naessens et al., 005). It was based on the release of ntrophenol from p- ntrophenyl--d-glucopyranosde (NPG), mmckng G utlzaton by the transglucosdase, whch was developed. The DDase specfcty of the test was proven va an NPG zymogram. All results representted an average of three separate determnatons. One unt of DDase actvty was defned as the amount of enzyme whch lberates 1 µmol of ntrophenol from NPG per mn under the standard assay condtons. Expermental desgn and response surface methodology Screenng for the mportant factors For screenng, the Plackett-Burman desgn was appled wth whch 1 runs would enable us to estmate all man effects for up to 11 factors. Table 1 showed the Plackett-Burman desgn used n ths study (Plackett-Burman, 1946). Snce there were only 9 factors n ths case, less than the maxmum allowable factors, the remaned factors became dummy factors whch would be used to estmate errors. The sgns -1 and +1 represented the lower and hgher levels of the correspondng components under nvestgaton. In ths experment, the hgher levels of the components were chosen to equal 1.5 tmes of ther lower levels (Table ). Central composte desgn (CCD) method Sodum chlorde, tryptone, glucose and yeast extract were four effectve nutrents n the Plackett-Burman desgn. These varables were selected to fnd the optmum condton for hgher DDase producton usng central composte desgn (CCD). In ths case, a 4 full factoral central composte desgn for four ndependent varables each at fve levels wth eght star ponts and sx replcates at the centre ponts was employed to ft a second order polynomal model, n whch 30 experments were requred n ths procedure (Box et al., 1978, Box, 1951). Each varable was desgned at fve levels (, 1, 0, 1, ) and the lowest and the hghest concentraton were: sodum chlorde, 0 and 0.0 g/l; tryptone, and 18 g/l; glucose, 5 and 55 g/l; yeast extract, and 18 g/l, respectvely. Table 3 showed the CCD desgn for the values and the observed response for the DDase actvty. The central values (zero level) chosen for expermental desgn were same as the lower level (desgnated -1) n the Plackett-Burman desgn. For statstcal calculaton, the relatonshp between the coded and actual values s descrbed as the followng equaton: X U U = U 0 where X s the coded value of the th varable, U s the actual value of the th varable, U 0 s the actual value of the th varable at the center pont and U s the step change of varable. The response varable (DDase actvty) sutable to a quadratc (1)

3 118 Afr. J. Botechnol. Table 1. Plackett-Burman desgn for 11 varables wth coded values. S/N A B C D E F G H J K L DDase (U/mL) Table. Assgned concentratons of varables at dfferent levels n Plackett-Burman desgn. Factor Varables wth desgnate Lower level (-1) (per ltre) Hgher level (+1) (per ltre) 1 A Maltobose 30 g 37.5 g B Glucose 30 g 37.5 g 3 C Tryptone 10 g 1.5 g 4 D Yeast extract 10 g 1.5 g 5 E Ammonum ntrate 15 g g 6 F Copper sulfate 0.01 g g 7 G Znc sulfate 0.01 g g 8 H Sodum chlorde 0.01 g g 9 J Pror ph K Dummy 11 L Dummy equaton for the varables was as followng: Y = b 0 + b x + bj x x j + b x + j where Y s the measured response, X, X j are nput varables whch nfluence the response varable Y; b 0 s a constant; b s the th lnear coeffcent; b s the squared coeffcent and b j s the jth cross-product coeffcent. The Desgn Expert software (verson 7.1.6, Stat-Ease, Inc., Mnneapols, USA) was utlzed to analyze the sgnfcance of expermental results. The central composte desgn (CCD) employed to ft a second order polynomal model, had four varables, of whch everyone was at fve levels wth eght star ponts and sx replcates at the centre ponts and the result ndcated that 30 experments were requred for ths procedure (Cochran, 1957). RESULTS AND DISCUSSION Screenng for the mportant factors The effects of dfferent carbon sources on the growth of e () G. oxydans and DDase actvty were studed n the meda contanng yeast extract (%) as the ntrogen source. The results showed that glucose and maltobose were better than other carbon sources for the DDase producton; the effects of ntrogen sources on the DDase producton by G. oxydans were nvestgated usng glucose (%) as carbon source and t exhbted that tryptone was the best and yeast extract and ammonum ntrate was nferor (data not shown). Then the DDase yeld was determned for fermentaton contanng glucose (%) and tryptone (1%) as carbon and ntrogen sources and one of the followng ons (0.001, 0.01 and 0.1%) were used as addtves: KCl, NaCl, MgCl 6H O, FeCl 3 6H O, CoCl 6H O, BaCl H O, CaCl, FeSO 4 7H O, CuSO 4 5H O, ZnSO 4 7H O and MnSO 4 H O. Hgh yeld of DDase was observed when CuSO 4 or ZnSO 4 or NaCl was used as trace mneral cocktals for fermentaton (data not shown). Accordng to above study, whch was under the premse of keepng the other factors constant, we optmzed the composton of the producton medum as follows: glucose 30 g/l, maltobose 30 g/l, tryptone 10 g/

4 Mao et al Table 3. The CCD desgn for the values n coded and the observed values n response. S/N Sodum chlorde (g/l) Tryptone (g/l) Glucose (g/l) Yeast extract (g/l) DDase (U/mL) 1 CENTER CENTER CENTER CENTER CENTER CENTER L, yeast extract 10 g/l, ammonum ntrate 15 g/l, copper sulfate 0.01 g/l, znc sulfate 0.01 g/l, sodum chlorde 0.01 g/l and the ntal ph 6.0 was set pror to sterlzaton. The culture was ncubated at 30 C at 00 rpm n a rotary shaker for 6 h. After above optmzaton, the Plackett-Burman technque was used to select the most mportant factors whch would nfluence the DDase yeld. In ths secton, twelve experments were mnmum runs to screen the mportance of nne complcatons, namely glucose, maltobose, tryptone, yeast extract, ammonum ntrate, copper sulfate, znc sulfate, sodum chlorde and ph. The Model F-value of 0.84 mpled the model was sgnfcant. There was only a 4.66% chance that a Model F-Value ths large could occur due to nose. Values of Prob > F less than ndcated model terms were sgnfcant. The expermental date analyss showed that four varables, namely glucose, tryptone, yeast extract and sodum chlorde out of nne varables nfluenced the DDase yeld sgnfcantly. Central composte desgn (CCD) method Wth the central composte desgn method, the experments wth dfferent combnaton of glucose, tryptone, yeast extract and sodum chlorde were performed. A four-factor fve-level central composte desgn was used based on the Desgn Expert software (verson 7.1.6) and expermental data s presented n Table 3. By statstcal analyss, a mathematcal model was obtaned to descrbe the relatonshp between the DDase producton (Y) and the test varables n coded factors (concentraton of glucose, tryptone, yeast extract and sodum chlorde, respectvely):

5 1184 Afr. J. Botechnol. Table 4. ANOVA for response surface quadratc model. Source Sum of Squares DF Mean Square F Value R Model Resdual Lack of Ft Pure Error Cor Total Table 5. The least-squares ft and coeffcent estmate. Factor Coeffcent estmate Standard error 95% CI Lower lmt 95% CI Upper lmt F Value p-value Prob > F Intercept X X X < X X 1 X X 1 X X 1 X X X X X X 3 X X X X X CI = Confdence nterval; Prob = probabalty; F = frequency. Y = X X X X X X 0.014X X X X X X X X X 4 3 X 0.013X X X X The coeffcent values of the model and factors were calculated by Desgn Expert Software and ther values are shown n Tables 4 and 5. The results of the second order response surface model fttng n the form of ANOVA were gven n Table 4. In Table 5, the Model F-value of 13.8 mpled that the model was sgnfcant. There was only a 0.01% chance that a Model F-Value ths large could occur due to nose. The Lack of Ft F-value of mpled the Lack of Ft was sgnfcant. The well ft of the model was checked by determnaton coeffcent (R ). In ths case, the value of the determnaton coeffcent (R = 0.980) ndcated that t was reasonable to use the regresson model to analyze the tendency (Akhnazarove, 198; Khur and Cornell, 1987). Table 5 shows the sgnfcance of each coeffcent determned by F-value and P-value. Values of Prob > F less than ndcate model (3) terms were sgnfcant. In ths case X, X 3, X 4, X 3 X 4, X 1, X, X 3, X 4 were sgnfcant model terms. Fgures 1-6 shows the response surface for the varaton n the producton of DDase, from whch the values of DDase actvty for dfferent concentratons of the varables could be predcted. Each contour curve represented an nfnte number of combnatons of two test varables wth another mantaned at ther zero level. Fgures 1-3 show that ncreasng the sodum chlorde concentraton from to 0.01 g/l ncreased DDase producton. The maxmum producton was obtaned wth the concentraton of sodum chlorde at about 0.01 g/l. The two ntrogen sources, tryptone and yeast extract, were mportant to ncrease the DDase yeld. From the response surface contour plot, the concentratons of tryptone and yeast extract were around 1-14 g/l, respectvely, to result n the maxmum DDase yeld. In ths study, glucose was also a sgnfcance parameter. Fgures, 4 and 6 have shown that the maxmum DDase actvty appeared at the concentraton of g/l. Accordng to the optmzed mathematcal model, the optmal values of the test varables n coded unt were as follows: X 1 = , X = 0.549, X 3 = , X 4 = 0.88

6 Mao et al Fgure 1. Effect of sodum chlorde and trypotone concentraton on the DDase producton by G. oxydans. Other varables are held at zero level. Fgure. Effect of sodum chlorde and glucose concentraton on the DDase producton by G. oxydans. Other varables are held at zero level.

7 1186 Afr. J. Botechnol. Fgure 3. Effect of sodum chlorde and yeast extract concentraton on the DDase producton by G. oxydans. Other varables are held at zero level. Fgure 4. Effect of trypotone and glucose concentraton on the DDase producton by G. oxydans. Other varables are held at zero level.

8 Mao et al Fgure 5. Effect of trypotone and yeast extract concentraton on the DDase producton by G. oxydans. Other varables are held at zero level. wth the correspondng maxmum DDase producton Y = 0.09 U/mL (a possble varaton s between 0.17 and 0.5 mg/l) n the confdence range of 95%. Puttng the respectve values of X n Equaton (1), the concentraton of sodum chlorde, tryptone, glucose and yeast extract were at 0.009, 1.198, and g/l, respectvely. It was clear that the optmal values from response surface plots were almost consstent wth those from optmzed mathematcal equaton. In order to verfy the predcted results, the experment was performed wth the optmzed medum and the maxmum DDase producton was found to be 0.38 U/mL, whch was obvous n close agreement wth the model predcton. After optmzaton, compared wth the mnmum medum, the producton of DDase was enhanced about 17 fold, expermentally (Table 6). To our best knowledge, the DDase producton n ths research s hgher than any other reported results (Naessens et al., 005). the DDase producton from G. oxydance. The method used was effectve n the screenng for nutrtonal requrements n a lmted number of experments. It enabled us to screen a large number of expermental factors and was useful to determne the optmum levels of medum components concentraton that sgnfcantly nfluenced the DDase producton n a perfect way. The chosen method of optmzaton of medum composton was effcent, relatvely smple, tme reducng and materal savng. The fnal composton of defnte medum after the optmzaton was as follows: glucose g/l, maltobose 30 g/l, tryptone g/l, yeast extract g/l, ammonum ntrate 15 g/l, copper sulfate 0.01 g/l, znc sulfate 0.01 g/l, sodum chlorde g/l, respectvely, and the ntal ph was set at 6.0. The optmzaton of the medum resulted n an about 17-fold (0.38 U/mL) ncrease n DDase yeld. Ths work would provde a stable foundaton for the ndustralzaton of DDase. Conclusons Plackett-Burman screenng and response surface methodology (RSM) for medum optmzaton were employed for ACKNOWLEDGEMENTS Fnancal support from the Natonal Scence Foundaton of Chna ( ) and Natonal Basc Research Pro-

9 1188 Afr. J. Botechnol. Fgure 6. Effect of glucose and yeast extract concentraton on the DDase producton by G. oxydans. Other varables are held at zero level. Table 6. Expermental verfcaton of combned effect of optmzed medum on the response of DDase producton. Varables Levels after optmzaton Coded Uncode (g/l) Sodum chlorde Tryptone Glucose Yeast extract DDase producton (U/mL) Unoptmzed New medum medum Predcted Expermental gram of Chna (973 Program) (009CB74703) s gratefully acknowledged. REFERENCE Akhnazarove SAKV (198). Experment optmzaton n chemstry and chemcal engneerng. Moscow: Mr Publshers. Box GEP, Hunter WG, Hunter JS (1978). Statstcs for expermenters. New York, Wley, pp Box GEP, Wlson KB (1951). On the expermental attanment of optmum condtons. J. R. Stat. Soc. B, 13: Cochran WG, Cox GM (1957). Expermental desgn, nd ed. New York. John Wley and Sons, pp De Muynck C, Perera CS, Naessens M, Parmenter S, Soetaert W, Vandamme EJ (007). The genus Gluconobacter oxydans: comprehensve overvew of bochemstry and botechnologcal applcatons. Crt. Rev. Botechnol. 7: Gao KL, We DZ (006). Asymmetrc oxdaton by Gluconobacter oxydans. Appl. Mcrobol. Botechnol. 70: Gao K, Song Q, We D (006). Couplng of enantoselectve booxdaton of DL-1, -propanedol and boreducton of pnacolone va regeneraton cycle of coenzyme. Appl. Mcrobol. Botechnol. 71: Hehre EJ (1951). The bologcal synthess of dextran from dextrns. J. Bol. Chem. 19: Kammoun R, Nal B, Bejar S (008). Applcaton of a statstcal desgn to the optmzaton of parameters and culture medum for -amylase producton by Aspergllus oryzae CBS grown on gruel (wheat

10 Mao et al grndng by-product) Boresour. Technol. 99: Khur AI, Cornell JA (1987). Response Surfaces: Desgn and Analyss. New York, Marcel Dekker. Mao XZ, Shen YL, Yang L, Chen S, Yang YP, Yang JY, Zhu H, Deng ZX, We DZ (007). Optmzng the Medum Compostons for accumulaton of the Novel FR-008/Candcdn Dervatves CS101 by a Mutant of Streptomyces sp. Usng Statstcal Expermental Methods. Process Bochem. 4: Mountzours KC, Glmour SG, Jay AJ, Rastall RA (1999). A study of dextran producton from maltodextrn by cell suspensons of Gluconobacter oxydans NCIB J. Appl. Mcrobol. 87: Naessens M (003). Dextran dextrnase from Gluconobacter oxydans: producton and characterzaton. PhD thess, Ghent Unversty, p. 56. Naessens M, Cerdobbel A, Soetaert W, Vandamme EJ (005). Dextran dextrnase and dextran of Gluconobacter oxydans. J. Ind. Mcrobol. Botechnol. 3: Plackett RL, Burman JP (1946). The desgn of optmum multfactoral experments. Bometrka, 33: Robyt JF, Walseth TF (1979). Producton, purfcaton, and propertes of dextransucrase from Leuconostoc mesenterodes NRRL B-51F. Carbohydr. Res. 68: Sdebotham RL (1974). Dextrans. Adv. Carbohydr. Chem. Bochem. 30: Sms IM, Thomson A, Hubl U, Larsen NG, Furneaux RH (001). Charactersaton of polysacchardes synthessed by Gluconobacter oxydans NCIMB Carbohydr. Polym. 45: Tan KT, Lee KT, Mohamed AR (010). A glycerol-free process to produce bodesel by supercrtcal methyl acetate technology: An optmzaton study va Response Surface Methodology. Boresour. Technol. 101: Yamamoto K, Yoshkawa K, Ktahata S, Okada S (199). Purfcaton and some propertes of dextrn dextranase from Acetobacter capsulatus ATCC Bosc. Botechnol. Bochem. 56: Yamamoto K, Yoshkawa K, Okada S (1993a). Detaled acton mechansm of dextrn dextranase from Acetobacter capsulatus ATCC Bosc. Botechnol. Bochem. 57: Yamamoto K, Yoshkawa K, Okada S (1993b). Structure of dextran synthessed by dextrn dextranase from Acetobacter capsulatus ATCC Bosc. Botechnol. Bochem. 57: Yamamoto K, Yoshkawa K, Okada S (1994). Effectve producton of glycosyl-stevosdes by -1, 6 transglucosylaton of dextrn dextranase. Bosc. Botechnol. Bochem. 58: Yang XP, We LJ, Ye JB, Yn B, We DZ (008). A pyrroloqunolne qunne-dependent membrane-bound d-sorbtol dehydrogenase from Gluconobacter oxydans exhbts an ordered B B reacton mechansm. Arch. Bochem. Bophys. 477:

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