Microbial and Enzymatic Process for Xylitol Production from D-glucose
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1 Send rders for Reprints to Current rganic Chemistry, 2014, 18, Microbial and Enzymatic Process for Production from D-glucose Xianghui Qi a*, Xu Wang a, Jing Lin a, Jingfei Zhu a, Yan Luo a, Wenying Deng a, Fei Wang a, Wenjing Sun a and Jianzong Meng b a School of Food and Biological Engineering, Jiangsu University, Zhenjiang, , China; b Gencata Biotechnology Co, Ltd. Nanning , China Abstract: A microbial and enzymatic process for xylitol production that initiates from D-glucose occurs by virtue of a three-step process in which D-arabitol is the first intermediate product and D-xylulose is the second. To date, the steps of the formation of D-arabitol and the conversion of xylitol from D-xylulose are key points of departure for promoting the overall process for xylitol production from D-glucose. This review provides comprehensive insights regarding potential methods of xylitol production from D-glucose, which might be an alternative to the classical process that utilizes D-xylose as substrate. Keywords: D-arabitol dehydrogenase (ArDH), D-arabitol, D-glucose, D-xylulose, xylitol dehydrogenase (), xylitol. 1. INTRDUCTIN, a five-carbon sugar-alcohol, has become widely used as an alternative natural sweetener in the food and confectionary industry because of its sweetening degree similar to that of sucrose and its useful and valuable properties [1]. In addition, the metabolism of xylitol in humans is independent of insulin, which makes it a recommended sugar substitute for diabetics [2]. It has also been utilized in oral health care and pharmaceutical industry due to its role in preventing dental caries [3]. is currently produced commercially by chemical and catalytic reduction (hydrogenation) of the five-carbon sugar, D- xylose, which is derived from hemicellulose-xylan hydrolysates of substrates such as birch wood or corn [4]. can also be produced at high volume by using natural or recombinant D-xyloseutilizing yeasts, such as Candida, Saccharomyces and Debaryomyces species [5]. Nevertheless, both processes rely on the hydrolysis and/or purification of D-xylose from lignocellulosic materials, which cause inevitable contamination. Additionally, xylitol cost is the major factor limiting the range of current applications in food and chemical technology, because the two processes are expensive and uncompetitive on account of the high cost of the substrate (Dxylose). To get rid of the defect, the initial conversion of D-glucose is available and much cheaper to develop a more economical and efficient technology for xylitol production. This review introduces the research progress of xylitol production from D-glucose with special emphases on its process of bioconversion, engineering microorganisms along with their biosynthetic pathway and metabolic characteristics, effects of culture condition and production properties and cofactor regeneration of the related enzyme as well. 2. PRGRESS F XYLITL PRDUCTIN FRM D- GLUCSE nishi and Suzuki described a three-step fermentation process to produce xylitol from D-glucose via D-arabitol and D-xylulose *Address correspondence to this author at the School of Food and Biological Engineering, Jiangsu University, Zhenjiang, , China; Tel: ; Fax: ; qxh@ujs.edu.cn (Fig. 1). As one alternative synthetic approach, the microbial conversion process is technically by far less costly than the transformation of hemicellulose into D-xylose. Primarily, the conversion of D- glucose to D-arabitol by some osmophilic yeasts strains belonging to the genera Pichia, Zygosaccharomyces, Hansenula, Saccharomyces, Candida and Debaryomyces has been reported [6]. The conversion of D-arabitol to xylitol involves successive enzyme reactions. D-arabitol was first oxidized to D-xylulose by using a membrane-bound D-arabitol dehydrogenase (ArDH), and subsequently reduced to xylitol by a NAD-dependent xylitol dehydrogenase (). The transformation from D-arabitol to xylitol is realized by Gluconobacter oxydans because of its membrane-bound ArDH and soluble NAD-dependent [7]. D-arabitol is almost thoroughly converted into D-xylulose with a typical reaction characteristic of oxidative fermentation in acetic acid bacteria [8]. However, the conversion of D-xylulose into xylitol catalyzed by exceedingly limits the ultimate production of xylitol because of the low activity of. From the perspective of industry, improving the conversion rate of D-xylulose to xylitol would increase the yield of xylitol and refine the manufacturing process. 3. D-ARABITL ACCUMULATIN VIA SMPHILIC YEASTS SCREENED Microbial conversion process of D-glucose into D-arabitol provides a key point of departure for promoting the overall process for xylitol production from D-glucose. It is known that the production of D-arabitol from D-glucose using osmophilic yeast screened from nature samples has been investigated [9]. In addition, the biosynthetic pathway of D-arabitol in yeasts and its physiological role in cells have been reported. D-arabitol producing yeasts can be isolated from natural osmophilic sources such as soil of orchard, high sugar foods, honeybee hive and fresh pollen from flowers. After suitable processes and cultivation, the final aim is to obtain the single colonies of efficient D-arabitol producing strains from collected samples. For example, Kodamaea ohmeri NH-9, a previously screened novel strain from honeybee hive and flower samples, can be efficiently used to transform glucose into D-arabitol [5] D-arabitol Biosynthetic Pathway in smophilic Yeasts As shown in Figure (2), two D-arabitol biosynthetic pathways have been described in many fungi. The osmotolerant yeast species /14 $ Bentham Science Publishers
2 3132 Current rganic Chemistry, 2014, Vol. 18, No. 24 Qi et al. CH osmophilic yeasts ArDH NADH NAD PQQ PQQH 2 D-glucose D-arabitol D-xylulose Fig. (1). Fermentation process of xylitol production from D-glucose. D-glucose glucose-6-phosphate Ribulokinase Ribulose-5-phosphate Ribulose-5P-epimerase D-Ribulose D-Xylulose-5-phosphate Arabitol dehydrogenase Xylulokinase D-arabitol Arabitol dehydrogenase D-xylulose dehydrogenase Fig. (2). Biosynthetic pathway for conversion of glucose to D-arabitol in fungi. Zygosaccharomyces rouxii, Saccharomyces mellis, and Debaryomyces hansenii convert D-glucose to D-ribulose-5-P 4 via the pentose pathway, dephosphorylate D-ribulose-5-P 4, and then reduce D-ribulose to D-arabitol by an NADP-dependent pentitol dehydrogenase [10]. In addition, the marine fungus Dendryphiella salina and another strain of Z. Rouxii convert D-glucose to D-xylulose-5- P 4 via the pentose pathway, dephosphorylate D-xylulose-5-P 4, and then reduce D-xylulose to D-arabitol by an NAD-dependent pentitol dehydrogenase [11]. To characterize the biosynthetic pathway of D-arabitol further, Wong et al. [10] (1995) comparatively analyzed the labeling patterns in D-[ 13 C] arabitol from D-[ 13 C] glucose by the ard null mutant and by the wild-type Candida albicans They put forward two possibilities about the synthetic pathway of D-arabitol. ne is D-ribulose-5P 4 that is dephosphorylated, followed by the reduction of D-ribulose into D-arabitol by a second ArDH isoform. Alternatively, D-ribulose-5-P 4 could be reduced to D-arabitol-5-P 4 by a D-ribulose-5-P 4 reductase, followed by the dephosphorylation of D-arabitol. Their studies showed the synthesization and utilization of D-arabitol by Candida albicans via separate metabolic pathway, which were not formerly suspected for fungi. Suzuki et al. [12] reported a paper in 2003, which shows that there are two D- arabitol forming dehydrogenase activities and the pathway of D- arabitol production in this osmophilic yeast stains is still unclear. Some osmophilic yeasts have capabilities to transform D- glucose into D-arabitol, but cannot transform D-arabitol into D- xylulose due to lacking of D-arabitol-4 dehydrogenase. Cheng et al. [13] cloned a NADP-dependent D-arabitol dehydrogenase gene from Gluconobacter oxydans CGMCC and expressed in Escherichia coli to convert D-arabitol to D-xylulose. So, it will be a new try to convert D-arabitol to D-xylulose if the ArDH gene can be introduced into osmophilic yeasts and a new method to product xylitol, since these osmophilic yeasts own xylitol dehydrogenase natively Effect of Cultural Conditions on D-arabitol Production The optimization of the microbial transformation of D-glucose into D-arabitol has not been researched thoroughly, but the consumption of D-glucose and the production of D-arabitol are seriously affected by the culture conditions such as culture temperature, the ratio of carton and nitrogen, and inoculation quantity and so on. In Table 1, the experimental conditions suitable for effective production with different strains are given. Culture temperature is a significant factor in D-arabitol fermentation and optimum temperature is mostly in the range of C. However, the maximal oxidase activity of ArDH at acid or alkaline ph was common characteristics of many polyol dehydrogenases from multiple microbial systems [14]. Thereby the ph range of indicated no con-
3 Microbial and Enzymatic Process for Production from D-glucose Current rganic Chemistry, 2014, Vol. 18, No Table 1. The experimental conditions suitable for effective production by different strains and their performances achieved with previous reports with different flask batch processes. Fermentative Mode: Batch Fermentation Monacell et al. [17] Nozaki et al. [12] Badal et al. [15] Zhu et al. [5] Song et al. [18] Strain P. ohmeri No. 230 M. reukaufii AJ14787 Z. rouxii NRRL K. ohmeri NH-9 Candida sp. H 2 Substrate concentration 100g/L 200g/L 175g/L 200g/L 250g/L Inoculum size 8% 5% 5% 5% 1% Fermentation conditions ph 6.6, 30 C, 125 rpm ph 5.0, 33 C, 350 rpm ph 5.0, 30 C, 350 rpm ph 6.5, 37 C, 220 rpm ph 6.0, 35 C, 200 rpm Fermentation period 96h 116h 240h 72h 96h D-arabitol yield 43.0g/L 81.4g/L 83.4g/L 81.2g/L 86.55g/L Maximum yield (ara/glu, g/g) Max volumetric Productivity (g/l h) spicuous impact on D-arabitol production [5]. Additionally, in the medium, appropriate balance of carbon/nitrogen sources ( g/l) could enhance the accumulation of D-arabitol [15], but it was not effective to add excess nitrogen sources or use organic nitrogen sources such as nucleic acids or amino acids [12]. An analogous result has also been covered in the case of erythritol production by Trichosporon sp. from D-glucose-containing corn steep liquor [16]. The inoculum quantity affects the production of D-arabitol and the D-arabitol yield presents positive growth with the increase of inoculum size. Agitation speed is essential for the production of D- arabitol, and the highest D-arabitol production occurred at in shake flasks [15]. In addition, the repeated-batch operation had a conspicuous effect on improving D-arabitol production as well [5] Drawbacks in Process from D-glucose to D-arabitol To date, a large part of this research has been devoted to increase D-arabitol production, but the optimization of microbial transformation of D-glucose into D-arabitol has not been well studied. Standing in the industrial point of view, the long cultivation time and the low productivity of D-arabitol were two major problems. A comparison of performances achieved with previous reports with different strains by flask batch fermentation is shown in Table 1 [5, 12, 15, 17, 18]. For example, Nozaki et al. described a process for the production of 81.4 g/l D-arabitol by Metschnikowia reukaufii in 116 h with g/l h productivity [12]. Additionally, certain osmophilic yeasts produce a variety of polyhydric alcohols as byproduct when grown in the presence of high concentration of glucose [9]. It has been shown that accumulation of polyols as undesirable byproducts in yeasts may be bound up with water activity and osmophilic stress in the medium, because these polyols can act as compatible solutes. The accumulation of byproducts can be decreased by controlling temperature alteration and D-glucose feeding. 4. PRPERTIES F ARDH AND Several micro-organisms have potential to metabolize D- arabitol as the sole carbon source. The enzymatic step of the metabolism of D-arabitol is an oxidation reaction by a D-arabitol dehydrogenase. The ArDH (D-arabitol 2-dehydrogenase) structural gene (ARD) from fungi encoded a 30,643-Da member of the shortchain dehydrogenase enzyme family that catalyzed the reaction D- arabitol + NAD + D-ribulose + NADH [10], whereas the AraDH (D-arabitol 4-dehydrogenase) from bacterial oxidized D- arabitol to D-xylulose. The D-arabitol dehydrogenase gene belongs to the short-chain dehydrogenase family, and the DNA sequence surrounding the gene suggested that it is part of an operon with several components of a sugar alcohol transporter system [13]. Sugisawa and Hoshino [19] reported that ArDH was extremely similar to glycerol dehydrogenase and also to the membrane-bound D-sorbitol dehydrogenase from Gluconobacter suboxydans IF These enzymes have some similar aspects: the same molecular mass of kda in SDS-PAGE and absence of heme component in the enzyme. However, they have clear differences in the optimum ph. ArDH was stable below ph 5.0 and the optimum ph of D-arabitol oxidation with ArDH was found at 5.0. Adachi et al. [8] purified the membrane-bound ArDH and proved that the enzyme was a quinoprotein by PQQ detection and the most characteristic of ArDH was testified by its versatility of substrate specificity. Among diverse substrates, D-arabitol is the most effective substrate for ArDH. Thus, ArDH may have the main function in the oxidative fermentation of various ketoses production [7]. In previous studies, the s from Pachysolen tannophilus and Candida shehatae were shown to be highly specific for xylitol. Afterwards, Sugiyama et al. [19] demonstrated that increasing activity in G. oxydans improved xylitol yield since was specified for xylitol. Based on the NH 2 -terminal amino acid sequence, they constructed expression plasmids with the xdh gene which encodes a polypeptide composed of 262 amino acid residues with a molecular mass of 27.8 kda. The belongs to the shortchain dehydrogenase/reductase family by deducing its amino acid sequence. Then they utilized these plasmids to produce recombinant strains of G. xydans that was observed to have about 11-fold increase in activity compared to the wild-type strain. However, as the second intermediate product, D-xylulose still remained in the
4 3134 Current rganic Chemistry, 2014, Vol. 18, No. 24 Qi et al. Table 2. The enzymatic properties of ArDH and. ArDH Source Pichia stipites CBS 6054 [20] G. oxydans CGMCC 1.110[13] Galactocandida Mastotermitis [21] G. oxydans ATCC 621 [19] ptimal ph ptimal temperature 30 C 25 C 25 C 30 C Substrate D-arabitol D-arabitol D-xylulose D-xylulose product D-ribulose D-xylulose xylitol xylitol ptimal coenzyme NAD + NADP NADH NADH Note: ArDH: D-arabitol dehydrogenase; : xylitol dehydrogenase. reaction mixture, even using recombinant strains of G. xydans. Under controlled aeration conditions, the recombinant strains performed high-level expression of xdh, even the improvement was still unsatisfactory. Thereby, constructing a novel recombinant strain harboring a higher expression vector for xdh gene by the means of gene engineering might be a promising method to enhance the production of xylitol. The enzymatic properties of ArDH and from different strains are given in Table 2 [13, 19-21]. XYLITL PRDUCTIN FRM D-ARABITL Gluconobacter oxydans is important for commercial production of xylitol because it can incompletely oxidize sugars and sugar alcohols to ketoses due to its primary dehydrogenases [22]. Suzuki et al. [7] reported a novel bioconversion process by which xylitol can be accumulated from D-arabitol with Gluconobacter oxydans, and they discovered that the species from Gluconobacter have two enzymes (ArDH and ) capacitating the production of xylitol from D-arabitol. Gluconobacter strains could oxidize D-arabitol to D-xylulose via ArDH and then D-xylulose was reduced to xylitol by with NADH as the necessary cofactor. D-arabitol is almost thoroughly converted into D-xylulose with a typical reaction characteristic of oxidative fermentation in acetic acid bacteria [23]. This bio-catalyzing reaction by is extremely dependent on NADH as the necessary cofactor (Fig. 3). However, it has been reported that Gluconobacter lacked succinate dehydrogenase, an essential enzyme in the TTC cycle, and phosphofructokinase, an essential enzyme in the EMP [24]. Thus the NADH generation mechanism of G. xydans remains unclear and few reports have employed the cofactor regeneration by co-expression systems. or D-xylulose NADH NAD CH H Acetate Ethanol H ADH(GDH) H H Glucono-lactone or Glucose Fig. (3). Flux of cofactors in the conversion from D-xylulose to xylitol. Supplying sufficient NADH would extremely improve the xylitol yield because is highly specific for the cofactor NADH in bio-catalysis reaction. Compared with the huge price of the pyridine cofactors, the regeneration of cofactor in situ is essential to the commercial and economic transformation of D-xylulose into xylitol in large-scale. Suzuki et al. [25] reported two xylitol-increasing factors, that one is transaldolase/glucose-6-phosphate isomerase (TAL-PGI) bifunctional enzyme and the other is ribulokinase. Then the enzyme activities of TAL, PGI, and ribulokinase can be related to the PPP [24]. They found that the addition of these two factors led to the increase of the xylitol production from D-arabitol in vitro. Therefore, Strains with enhanced ribulokinase and TAL-PGI activities may thus improve xylitol production via G. xydans by increasing the supply of NADH. Additionally, Ethanol can be oxidized by an NAD-dependent soluble alcohol dehydrogenase, resulting in the regeneration of NADH [7], and the xylitol yield increased to 57g/L (a 26% yield) via G. oxydans/psaup [19] by adding appropriate quantity of ethanol. A process by adding D-glucose can reach the same result [26]. Thus, the most low-priced and available process for regenerating pyridine cofactors might well be to use dehydrogenases by adding co-substrate D-glucose or ethanol, which recycles nicotinamide coenzymes [27]. To enhance the D-xylulose consumption and xylitol yield, Zhou et al. [26] constructed and detected the co-expression systems of the gene with either the glucose dehydrogenase (GDH) or the alcohol dehydrogenase (ADH) gene in Escherichia coli for NADH regeneration, in which GDH and ADH are obtained from Bacillus subtilis and G. xydans, respectively. They described that the concentrations of co-substrate (glucose or ethanol) and recombinant cells were significantly affected the total xylitol yield. Compared with that of G. xydans NH-10, the volume of xylitol production by co-expression systems improved to g/l by system 1(E. coli Rosetta/Duet-xdh-gdh) with a 92% transformation yield and 24.9 g/l by system 2 (E. coli Rosetta/Duet-xdh-adh, 85.2%). In addition, an engineered G. oxydans PXPG was constructed to coexpress the gene and glucose dehydrogenase gene acted as a cofactor regeneration enzyme, and the activities for both enzymes were more than two folds higher in the G. oxydans PXPG than in the wild strain [28]. Some previous studies have shown that a TTN of is adequate to make the process of xylitol production efficiently feasible [29]. The TTN was 32,100 for system 1 and 17,600 for system 2, which are distinctly higher than the standard mentioned above and implies that the two procedures are economically viable. CNCLUSIN In summary, a process for xylitol production that starts from D- glucose is technically much simpler and cheaper than the classical process which utilizes D-xylose as the substrate. Basing on the existing literatures, this paper presents a comprehensive account of the most potential approach of production for accumulating of xyli-
5 Microbial and Enzymatic Process for Production from D-glucose Current rganic Chemistry, 2014, Vol. 18, No tol from glucose via D-arabitol. Considering the overall fermentation process for xylitol commercial production from D-glucose, future studies on expounding the D-arabitol biosynthetic pathway, screening the high-yield strains of D-arabitol from natural sources, optimizing the culture conditions, constructing recombinant strains and supplying sufficient NADH are now in advance to further increase xylitol production from D-glucose, hence allowing the improvement of a more efficient and potential approach for the production of xylitol from D-glucose. CNFLICT F INTEREST The authors confirm that this article content has no conflict of interest. ACKNWLEDGEMENTS This work was supported by the Natural Science Foundation of China under Grant No Science & Technology Development Plan of Nanning (No ), ne Hundred Undergraduate Innovation Program of Jiangsu (No.744, 11A344, Y11A169) and A Project Funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions. REFERRENCES [1] Bura, R.; Vajzovic, A.; Doty, S.L. Novel endophytic yeast Rhodotorula mucilaginosa strain PTD3 I: Production of xylitol and ethanol. J. Ind. Microbiol. Biotechnol., 2012, 39(7), [2] Granström, T.B.; Izumori, K.; Leisola, M. A rare sugar xylitol. Part I: The biochemistry and biosynthesis of xylitol. Appl. Microbiol. Biotechnol., 2007, 74(2), [3] Prakasham, R.; Rao, R.S.; Hobbs, P.J. Current trends in biotechnological production of xylitol and future prospects. Curr. Trends Biotechnol. Pharm., 2009, 3(1), [4] Kim, S.H.; Yun, J.Y.; Kim, S.G.; Seo, J.H.; Park, J.B. 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A short-chain dehydrogenase gene from Pichia stipitis having D-arabinitol dehydrogenase activity. Yeast, 1995, 11(9), [21] Nidetzky, B.; Helmer, H.; Klimacek, M.; Lunzer, R.; Mayer, G. Characterization of recombinant xylitol dehydrogenase from Galactocandida mastotermitis expressed in Escherichia coli. Chemico-biol. Interact., 2003, 143, [22] Gupta, A.; Singh, V.K.; Qazi, G.; Kumar, A. Gluconobacter oxydans: Its biotechnological applications. J. Mol. Microbiol. Biotechnol., 2001, 3(3), [23] Sugisawa, T.; Hoshino, T. Purification and properties of membrane-bound D-sorbitol dehydrogenase from Gluconobacter suboxydans IF Biosci. Biotechnol. Biochem., 2002, 66(1), [24] Deppenmeier, U.; Hoffmeister, M.; Prust, C. Biochemistry and biotechnological applications of Gluconobacter strains. Appl. Microbiol. Biotechnol., 2002, 60(3), [25] Sugiyama, M.; Suzuki, S.; Tonouchi, N.; Yokozeki, K. Transaldolase/glucose-6-phosphate isomerase bifunctional enzyme and ribulokinase as factors to increase xylitol production from D-arabitol in Gluconobacter oxydans. Biosci. Biotechnol. Biochem., 2003, 67(12), [26] Zhou, P.; Li, S.; Xu, H.; Feng, X.; uyang, P. Construction and coexpression of plasmid encoding xylitol dehydrogenase and a cofactor regeneration enzyme for the production of xylitol from D-arabitol. Enzyme Microb. Technol., 2012, 51(2), [27] Weckbecker, A.; Gröger, H.; Hummel, W. Regeneration of nicotinamide coenzymes: principles and applications for the synthesis of chiral compounds. In: Biosystems Engineering I; Springer, 2010; pp [28] Zhang, J.; Li, S.; Xu, H.; Zhou, P.; Zhang, L.; uyang, P. Purification of xylitol dehydrogenase and improved production of xylitol by increasing activity and NADH supply in Gluconobacter oxydans. J. Agric. Food Chem., 2013, 61(11), [29] Zhao, H.; van der Donk, W.A. Regeneration of cofactors for use in biocatalysis. Curr. pin. Biotechnol., 2003, 14(6), Received: February 27, 2013 Revised: June 23, 2014 Accepted: June 23, 2014
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