Elegant and Efficient Biotransformation for Dual Production of d

Article Cite This: J. Agric. Food Chem. XXXX, XXX, XXX−XXX

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Elegant and Efficient Biotransformation for Dual Production of D‑Tagatose and Bioethanol from Cheese Whey Powder Zhaojuan Zheng,†,‡,∥ Jiaxiao Xie,§,∥ Peng Liu,§ Xin Li,‡ and Jia Ouyang*,†,‡ †

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Jiangsu Co-Innovation Center of Efficient Processing and Utilization of Forest Resources, Nanjing Forestry University, Nanjing 210037, People’s Republic of China ‡ College of Chemical Engineering, Nanjing Forestry University, Nanjing 210037, People’s Republic of China § College of Forestry, Nanjing Forestry University, Nanjing 210037, People’s Republic of China S Supporting Information *

ABSTRACT: In this study, the dual production of valuable D-tagatose and bioethanol from lactose and cheese whey powder is presented. First, a one-pot biosynthesis involving lactose hydrolysis and D-galactose isomerization for D-tagatose production was established using crude enzymes of recombinant Escherichia coli with L-arabinose isomerase (L-AI) at 50 °C. Compared to the current enzymatic system, only L-AI was overexpressed, because of the unexpectedly thermotolerant β-galactosidase in E. coli BL21(DE3). Moreover, this high temperature rendered the D-glucose catabolism of E. coli inactive, while retaining all fermentable sugars for bioethanol fermentation. Thereafter, the mixed sugar syrup was fermented by Saccharomyces cerevisiae NL22. A total of 23.5 g/L D-tagatose and 26.9 g/L bioethanol was achieved from cheese whey powder containing 100 g/L lactose. This bioprocess not only provides an efficient method for the functionalization of byproduct whey, but also offsets the high production cost of D-tagatose and bioethanol. KEYWORDS: D-tagatose, lactose, whey, bioethanol, biotransformation

1. INTRODUCTION D-Tagatose is a rare hexoketose and an isomer of aldohexose Dgalactose. Naturally occurring D-tagatose is found only in tree gum and dairy products.1 Compared to common sugars such as sucrose and glucose, D-tagatose has lower calorie content and similar sweetness, with 38% of the calories of sucrose and 92% of the sweetness of sucrose. Therefore, D-tagatose is a potential replacement for the use of high-calorie bulk sweeteners as food additives.1,2 Moreover, D-tagatose provides numerous health benefits, such as diabetes treatment activity, antihyperglycemic activity, and prominent prebiotic effects.3 In recent years, the biotransformation of agroindustrial waste into value-added products, known as green chemistry, has provided important environmental and economic benefits for society.4 As a byproduct of milk and cheese processing, whey is abundant and inexpensive. Moreover, because of its high demand for biochemical and chemical oxygen, whey is considered a serious environmental pollutant.5 As such, the importance of exploring strategies for the high-value utilization of whey has inspired researchers to develop efficient functionalization methods for this byproduct.6,7 Whey is rich in lactose, which is a disaccharide consisting of one molecule of D-glucose and one molecule of D-galactose linked by a β-1,4glyosidic bond and can be hydrolyzed by β-galactosidase (EC 3.2.1.238). Considering that commercial D-tagatose is usually produced by the isomerization of D-galactose via L-arabinose isomerase (L-AI, EC 5.3.1.4), the production of D-tagatose directly from lactose or whey by combining β-galactosidase and L-AI is feasible. Nonetheless, reports on D-tagatose production from lactose or lactose-rich substrates are much less common than those from D-galactose. Wanarska and Kur © XXXX American Chemical Society

developed a simultaneous process for lactose hydrolysis and Dgalactose isomerization using a recombinant Pichia pastoris strain secreting β-galactosidase from Arthrobacter chlorophenolicus supplemented with the recombinant L-AI from Arthrobacter sp. 22c, obtaining a yield of 30% (calculated from D-galactose to D-tagatose).8 Xu et al. showed a single-step biotransformation for D-tagatose production from lactose using whole cell biocatalysis of recombinant Escherichia coli, which coexpressed an L-AI from Lactobacillus fermentum CGMCC2921 and a β-galactosidase from Thermus thermophilus HB27, obtaining a maximum yield of 20.2% (calculated from lactose to D-tagatose).9 However, considering the low conversion rate, there is still much room for improvement in the one-pot biotransformation process. A common problem in D-tagatose production from lactose is that most previous reports have mainly focused on D-tagatose concentration without taking into account the comprehensive utilization of released D-glucose and residual D-galactose. This results in the waste of carbon sources and leads to complex purification in the downstream process due to the similar properties of the mixed sugars. To address this issue, Wanarska and Kur utilized D-glucose to cultivate P. pastoris; however, the surplus D-galactose remained in the reaction mixture.8 Zhan et al. first achieved bioconversion of lactose to D-tagatose using E. coli-ZY (a recombinant strain coexpressing β-galactosidase and L-AI), and thereafter employed Saccharomyces cerevisiae NX-3 Received: September 28, 2018 Revised: December 24, 2018 Accepted: December 26, 2018

A

DOI: 10.1021/acs.jafc.8b05150 J. Agric. Food Chem. XXXX, XXX, XXX−XXX

Article

Journal of Agricultural and Food Chemistry

Figure 1. Scheme view of the dual production of D-tagatose and bioethanol. (A) Biocatalyst preparation. (B) Bioconversion process.

2. MATERIALS AND METHODS

to selectively consume the residual D-glucose and D-galactose. As the purpose of Zhan’s study was only to enhance the purity of D-tagatose, no result regarding the corresponding products from D-glucose and D-galactose was reported.10 In view of the above, in the present study, we aimed to not only develop an elegant and efficient one-step biotransformation method for D-tagatose production from lactose and cheese whey powder, but also establish a valorization of surplus Dglucose and D-galactose after hydrolysis and isomerization reactions. The scheme is depicted as Figure 1. The crude enzymes from a previously constructed strain, E. coli BL21(DE3) harboring pETDuet-araAF279I, which contains a thermophilic L-AI (F279I variant, which exhibited improved activity toward D-galactose) from Bacillus coagulans NL01,11 were used as the biocatalyst, and bioconversion was conducted at 50 °C. Thanks to the unexpectedly thermotolerant characteristic of β-galactosidase from E. coli BL21(DE3), no exogenous β-galactosidase was required. Furthermore, the crude enzymes of E. coli for D-glucose and D-galactose catabolism lose their activities at 50 °C such that no byproducts are derived from D-glucose and D-galactose. As such, all the remaining D-glucose and D-galactose was applied to bioethanol production. This strategy enabled contracted but efficient biotransformation for the dual production of Dtagatose and bioethanol from a relatively inexpensive material via an environmentally friendly route.

2.1. Materials and Bacterial Strains. Cheese whey powder, including 69.0% lactose, 11.8% protein, and 7.4% ash, was purchased from Lactalis Company. D-Galactose and D-tagatose were purchased from TCI. E. coli BL21(DE3) harboring pETDuet-araAF279I was constructed as in our previous study.11 S. cerevisiae NL22 was provided by Angel Company and used as a conventional strain for bioethanol fermentation in our laboratory.12 2.2. Preparation of Biocatalyst for D-Tagatose Production. E. coli BL21(pETDuet-araAF279I) was inoculated into 5 mL of Luria− Bertani (LB) medium containing 100 μg/mL ampicillin and incubated for 10−12 h at 37 °C, 200 rpm. Then, 5 mL of cell suspension was inoculated into 500 mL of LB medium containing 100 μg/mL ampicillin. For the expression of L-AIF279I, E. coli BL21(pETDuet-araAF279I) was grown to a density of OD600 nm 0.6−0.8 and then induced with 0.5 mM isopropyl-β-D-thiogalactopyranoside (IPTG) for 8 h at 25 °C and 200 rpm. The cells were harvested and washed with 0.85% (w/v) sodium chloride twice by centrifugation at 8000g for 10 min. The cell pellet was subsequently suspended in 50 mM phosphate buffer (pH 6.0) and disrupted by sonication. Thereafter, the crude enzymes obtained were heated at 50 °C for 3 h and centrifuged to remove thermolabile enzymes. The residual uninactivated crude enzymes were used as biocatalysts for Dtagatose production. 2.3. Optimization of One-Step Biotransformation for DTagatose Production. Typically, 10 mL of phosphate buffer (50 mM, pH 6.0) containing 60 g/L lactose, 1 mM Mn2+, and the uninactivated crude enzymes at 5 U/g lactose (all calculated on the basis of the activity of L-AIF279I in this study) was incubated at 50 °C B


Article


Figure 2. Optimization of biotransformation conditions for D-tagatose production. (A) Temperature. (B) Divalent metal ions. (C) L-AIF279I. (D) Borate. The conditions not listed in the figure are as follows: (A) 60 g/L lactose, 1 mM Mn2+, and L-AIF279I with 5 U/g lactose at varying temperature; (B) 60 g/L lactose, 1 mM various metal ions, and L-AIF279I with 5 U/g lactose at 50 °C; (C) 60 g/L lactose, 1 mM Mn2+, and LAIF279I with different dosage at 50 °C; (D) 60 g/L lactose, 1 mM Mn2+, L-AIF279I with 14 U/g lactose, and borate with varying dosage at 50 °C. Different letters represent significant differences between treatments (p < 0.05). and 150 rpm. The parameters, including temperature, metal ions, enzyme dosage, and borate, varied as follows for optimization of the biotransformation conditions: Temperature ranged from 45 to 65 °C. Co2+, Mn2+, Fe2+, Mg2+, Ni2+, Ca2+, and Cu2+ were added separately at a final concentration of 1 mM. Enzyme dosage ranged from 4 to 16 U/g lactose. The molar ratio of borate to lactose was set from 0.0 to 3.0. Aliquots were withdrawn from the reaction mixtures at specified times and diluted with the corresponding mobile phase prior to HPLC analysis. The lactose hydrolysis rate was defined as the percentage amount of hydrolyzed lactose in the initial lactose. The Dtagatose yield was defined as the ratio of D-tagatose to the hydrolyzed lactose unless otherwise specified. 2.4. Dual Production of D-Tagatose and Bioethanol. DTagatose was produced from lactose or cheese whey powder under optimized conditions. The inoculum of S. cerevisiae NL22 was cultured in YPG broth, composed of 3 g/L yeast extract, 5 g/L peptone, and 20 g/L D-galactose, at 30 °C and 150 rpm for 24 h. Thereafter, S. cerevisiae NL22 was inoculated into 10 mL of the above mixed sugar syrup for bioethanol fermentation. When the substrate for D-tagatose production was lactose, 5 g/L yeast extract, 1.2 g/L (NH4)2SO4, 0.4 g/L ZnCl2, 0.4 g/L MgSO4, and 1 g/L CaCl2 were added to the mixed sugar syrup to maintain the growth of S. cerevisiae NL22. When the substrate for D-tagatose production was cheese whey powder, the above nutriments were unnecessary. The initial density of S. cerevisiae NL22 was an optical density of 10 (600 nm), and the initial pH was adjusted to 6.0. Bioethanol fermentation was carried out at 30 °C and 150 rpm for 28 h. Each flask was equipped with a needle-pierced silicone stopper to allow for the removal of CO2 produced during fermentation. Aliquots were withdrawn from the reaction mixtures at specified times and diluted with the corresponding mobile phase prior to HPLC analysis. The ethanol yield was calculated according to the following equation:

ethanol yield =

Δ(Cglu

Ceth × 100% + Cgal) × 0.51

where Ceth was the produced ethanol concentration, g/L; Δ(Cglu + Cgal) was the total consumption of D-glucose and D-galactose in the fermentation process, g/L; and 0.51 was the transformation factor from D-glucose and D-galactose to ethanol.13 2.5. Analytical Methods. L-AIF279I activity was measured by determining the amount of formed D-tagatose according to previous reports.14 The amount of lactose, D-glucose, D-galactose, and Dtagatose was determined using an HPLC system (Agilent 1200 series) equipped with a Sugar-pak1 column (6.5 × 300 mm) (Waters) and a refractive index detector (Shimadzu). The column was eluted with deionized water at a flow rate of 0.4 mL/min and 80 °C. The amount of ethanol was quantified using an HPLC system equipped with a BioRad Aminex HPX-87H column (300 × 7.8 mm) and a refractive index detector. The column was eluted with 5 mM H2SO4 at a flow rate of 0.6 mL/min and 55 °C. The results were expressed as the mean ± SD (standard deviation). Statistical analyses were performed using SPSS statistics 20.0. The differences of the corresponding values between exposed groups were tested by one-way analysis of variance (ANOVA). p < 0.05 was considered to be a significant difference.

3. RESULTS AND DISCUSSION 3.1. Feasibility of D-Tagatose Production Using Uninactivated Crude Enzymes in the One-Step Biotransformation System. All previous studies applying singlestep methods for the production of D-tagatose from lactose have employed both exogenous β-galactosidase and L-AI.8−10 In our study, we found that the native β-galactosidase of E. coli BL21(DE3) is competent in lactose hydrolysis even after being heated. Therefore, only the L-AIF279I was exogenously C


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Figure 3. Time course of D-tagatose production from (A) 100 g/L lactose, (B) 150 g/L lactose, (C) 100 g/L lactose with borate (the molar ratio of borate to lactose was 2.4), and (D) 100 g/L lactose in cheese whey powder.

due to the fact that Co2+ or Mn2+ sharply boosts the activity of L-AIs.11,14 As Mn2+ exhibited no retardation of lactose hydrolysis and also the best promotion of D-tagatose yield, it was added in all experiments. Regardless of the amount of crude enzymes added, the lactose hydrolysis rate was nearly always 100%, which also demonstrated that the endogenous βgalactosidase of E. coli is thermotolerant and robust (Figure 2C). In contrast, the activity of L-AIF279I in the crude enzymes was crucial for D-tagatose conversion. As shown in Figure 2C, the yield of D-tagatose increased steadily accompanied by increases in L-AIF279I from 4 to 10 U/g lactose. Statistical analysis revealed that the yield of D-tagatose was comparable between 10 and 12 U/g lactose, and 12 and 14 U/g lactose, but increased significantly from 10 to 14 U/g lactose. In subsequent experiments, the crude enzymes containing 14 U L-AIF279I were added per gram of lactose. Borate can form a sugar−borate complex whose binding affinity differs depending on the type of sugars. Borate was reported to show a higher affinity to D-tagatose than to Dgalactose, resulting in an equilibrium shift toward D-tagatose production.15 For an enhancement of the yield of D-tagatose, and for avoidance of the potential inhibition caused by high concentrations of borate, the optimal molar ratio between borate and lactose was assessed in the range 0.0−3.0. As shown in Figure 2D, the ratio at 2.4 gave a relatively better D-tagatose yield, and a higher ratio did not further increase the D-tagatose yield. Moreover, the hydrolysis of lactose was not influenced by the addition of borate (Figure 2D). 3.3. Time Course of D-Tagatose Production from Lactose and Cheese Whey Powder under Optimal Conditions. The production of D-tagatose using lactose and cheese whey powder at different concentrations was investigated and compared. The time course of D-tagatose

expressed in E. coli BL21(DE3). In addition, we aimed to ferment D-glucose in hydrolysates into bioethanol instead of being consumed by E. coli. To fulfill this goal, in contrast to conventional approaches, in which purified enzymes are used, or certain genes are knocked out or knocked down, we preheated the biocatalyst and conducted the bioconversion at 50 °C to inactivate the undesired reactions. To investigate the viability and efficiency of our approach, 0.8 g of lactose was mixed with 5 U L-AIF279I (added in the form of uninactivated crude enzymes as shown in Figure 1) in a one-pot reaction system of 20 mL. The biocatalytic reaction was carried out at 50 °C and 150 rpm. After 24 h, 9.3 g/L Dtagatose was obtained, while 20.4 g/L D-glucose and 12.4 g/L D-galactose were left. The mass balance indicated that the enzymes of the E. coli D-glucose catabolism were inactivated while endogenous β-galactosidase and exogenous L-AIF279I were robust. As a result, no undesirable byproducts were introduced, and the remaining D-glucose and D-galactose could be further fermented into bioethanol. 3.2. Optimal Conditions of D-Tagatose Production from Lactose. The catalytic conditions were further optimized in terms of D-tagatose production. Figure 2A shows that temperatures between 45 and 55 °C resulted in a similar lactose hydrolysis rate, although no thermostable βgalactosidase was heterogeneously expressed. The optimum temperature for D-tagatose production was 50 °C, most likely due to the fact that the optimal temperature of L-AIF279I is 50 °C. Both the lactose hydrolysis rate and the D-tagatose yield decreased sharply at temperatures above 60 °C. Figure 2B shows that none of the surveyed divalent metal ions had any obvious influence on lactose hydrolysis except for Cu2+, which had an adverse effect. In contrast, detectable D-tagatose was only produced in the presence of Co2+ or Mn2+, most likely D


Article


A convenient and economical approach for this is converting these fermentable sugars into ethanol using S. cerevisiae. It should be noted that the addition of borate significantly enhanced D-tagatose yield and showed a negligible influence on lactose hydrolysis, but inhibited the growth of S. cerevisiae (Figure S1). Therefore, only syrup without borate was fermented by S. cerevisiae NL22. For the fermentation of mixed sugar syrup from lactose, nutrients should be added simultaneously to maintain the growth of S. cerevisiae NL22. However, this is not necessary for the fermentation of mixed sugar syrup from cheese whey powder, as whey is rich in lactose in addition to soluble proteins, lipids, and mineral salts. Figure 4 shows the bioethanol fermentation process using S. cerevisiae NL22. The D-glucose was completely consumed at 4 h, while the D-galactose was exhausted at about 24 and 12 h for the mixed sugar syrup from lactose and cheese whey powder, respectively. The maximum ethanol concentration was 26.4 and 26.9 g/L, representing a yield of approximately 82.4% and 79.8%, respectively. During fermentation, no obvious changes were observed in D-tagatose concentration. These observations indicate that D-galactose and D-glucose in the mixture were selectively fermented by S. cerevisiae NL22. Over the last few decades, the production of D-tagatose by biocatalysis and biotransformation has been extensively studied, particularly the isomerization of D-galactose via L-AI (Table 2). However, these reports used expensive and uneasily obtainable D-galactose. As a result, utilization of raw materials as an alternative substrate to reduce the cost of D-tagatose production has recently received considerable attention.20 The large surplus of whey produced by the dairy industries could be used as a potential low-cost substrate for D -tagatose production, since lactose is a major constituent of whey. Because of the similar properties of D-glucose, D-galactose, and D-tagatose, an obstacle of one-step lactose hydrolysis and Dgalactose isomerization is the costly purification of D-tagatose. Currently, few studies have focused on downstream purification by S. cerevisiae, but none have taken bioethanol production into account, as the chosen biocatalysts fermented D-glucose to other byproducts (Table 2). Inspired by cell-free systems, we employed a temperature-controlled strategy to avoid D-glucose catabolism, which did not require purified enzymes or the knockout/knockdown of specific genes. In addition, the removal of D-glucose and D-galactose by S. cerevisiae NL22 not only contributed to D-tagatose purification

production with 100 and 150 g/L lactose without borate is shown in Figure 3A,B, respectively. The lactose was almost completely hydrolyzed in 3 h, and the concentration of Dtagatose increased quickly in the first 3 h, reaching equilibrium after 12 h of biotransformation. The final concentrations of Dtagatose were 25.5 and 36.2 g/L, respectively. Strikingly, the concentration of D-tagatose was significantly enhanced to 43.6 g/L (using about 100 g/L lactose as substrate) in the presence of borate that is 171% of the borate-free result, respectively (Figure 3C). We then further investigated the biotransformation process from cheese whey powder and compared it with that from lactose. In addition to lactose, the cheese whey powder contains other unspecified components, which may influence the activity of L-AIF279I and decrease the D-tagatose concentration. Figure 3D shows that when the substrate was replaced by cheese whey powder containing 100 g/L lactose, the concentration of D-tagatose declined slightly to 23.5 g/L, decreasing by 7.8% compared to the concentration from lactose. However, for all the reactions in Figure 3, D-glucose was not consumed and was retained for the following bioethanol fermentation. The lactose hydrolysis rate and D-tagatose yield were calculated and are shown in Table 1. Regardless of the Table 1. Lactose Hydrolysis and D-Galactose Isomerization under Different Reaction Conditions D-tagatose

lactose (g/L) 100a 150a 100a + borateb 100c

(g/L) 25.5 36.2 43.6 23.5

± ± ± ±

0.3 0.4 0.4 0.6

lactose hydrolysis rate (%)

D-tagatose

± ± ± ±

25.9 22.3 40.0 21.8

99.7 99.4 99.8 99.6

0.03 0.02 0.04 0.01

yield

(%) ± ± ± ±

0.5 0.3 0.4 0.6

a

Lactose concentration. bThe molar ratio of borate to lactose is 2.4. Lactose concentration in cheese whey powder.

c

presence of borate or unspecified contents in the cheese whey powder, the lactose hydrolysis rate was unaffected. In contrast, the D-tagatose yield was distinctly improved by the addition of borate and was reduced slightly by the presence of unspecified contents in the cheese whey powder. 3.4. Bioethanol Production from the Remaining Fermentable Sugars. After D-tagatose production, the further utilization of surplus D-glucose and D-galactose is essential for substrate valorization and D-tagatose purification.

Figure 4. Fermentation of mixed sugar syrup derived from (A) lactose and (B) cheese whey powder by S. cerevisiae NL22. E


Article

Journal of Agricultural and Food Chemistry Table 2. D-Tagatose Production from Different Substrates by Biocatalysis and Biotransformation D-tagatose

biocatalyst crude enzyme of E. coli BL21 expressing L-AIF279I

whole cells of E. coli BL21 coexpressing β-galactosidase and L-AI whole cells of E. coli BL21 coexpressing β-galactosidase and L-AI recombinant P. pastoris secreting β-galactosidase and purified L-AI permeabilized and immobilized Lactobacillus plantarum purified L-AI from Clostridium hylemonae whole cells of E. coli BL21 expressing L-AIF279I surface-displayed L-AI on Bacillus subtilis 168 surface-displayed L-AI on Bacillus subtilis DB403

50 °C, 12 h 50 °C, 12 h 70 °C, 16 h 34 °C, 24 h 30 °C, 144 h 50 °C, 48 h 60 °C, 10 h 50 °C, 48 h 70 °C, 24 h 67 °C, 28 h

(g/L)

lactose hydrolysis rate (%)

D-tagatose

yield (%)

ref

lactose,a 100 g/L

43.6

99.8

40.0b

whey containing 100 g/L lactose

23.5

99.6

21.8b

84

20.2b

this study this study 9

condition

substrate

lactose,a 500 g/L

101

lactose,a 50 g/L

10.75

95

43c

10

whey permeate containing 110 g/L lactose hydrolyzed whey permeate containing 300 g/L D-galactose D-galactose, 10 mM

14.8

90

30c

8

44c

16

45.9c

17

132 4.6 mM

D-galactose,

150 g/L

67.5

46c

11

D-galactose,

100 g/L

75

75c

18

D-galactose,

125 g/L

96.4

77.2c

19

a

Adding borate. bYield calculated from lactose to D-tagatose. cYield calculated from D-galactose to D-tagatose.

Notes

but also increased the price competitiveness of bioethanol production. To our knowledge, this is the first study to report simultaneous D-tagatose production and bioethanol fermentation from whey. In conclusion, this study demonstrated the dual production of D-tagatose and bioethanol from lactose and cheese whey powder, a relatively inexpensive and readily available material. For D-tagatose production, no exogenous β-galactosidase was required, and the biotransformation process was simplified; for bioethanol production, the temperature-controlled biotransformation rendered D-glucose catabolism inactive while retaining all fermentable sugars for yeast fermentation. Using this efficient bioprocess, we make full use of lactose and cheese whey powder, and establish a labor-saving and cost-saving biotransformation process. The temperature-controlled biotransformation strategy may be applicable to numerous biocatalytic reactions in other industries.

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The authors declare no competing financial interest.

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(1) Kim, P. Current studies on biological tagatose production using L-arabinose isomerase: a review and future perspective. Appl. Microbiol. Biotechnol. 2004, 65, 243−249. (2) Xu, Z.; Li, S.; Feng, X.; Liang, J.; Xu, H. L-Arabinose isomerase and its use for biotechnological production of rare sugars. Appl. Microbiol. Biotechnol. 2014, 98, 8869−8878. (3) Lu, Y.; Levin, G. V.; Donner, T. W. Tagatose, a new antidiabetic and obesity control drug. Diabetes, Obes. Metab. 2007, 10, 109−134. (4) Koutinas, A. A.; Vlysidis, A.; Pleissner, D.; Kopsahelis, N.; Garcia, I. L.; Kookos, I. K.; Papanikolaou, S.; Kwan, T. H.; Lin, C. S. K. Valorization of industrial waste and by-product streams via fermentation for the production of chemicals and biopolymers. Chem. Soc. Rev. 2014, 43, 2587−2627. (5) Prazeres, A. R.; Carvalho, F.; Rivas, J. Cheese whey management: a review. J. Environ. Manage. 2012, 110, 48−68. (6) Jin, Y.; Parashar, A.; Mason, B.; Bressler, D. C. Simultaneous hydrolysis and co-fermentation of whey lactose with wheat for ethanol production. Bioresour. Technol. 2016, 221, 616−624. (7) Liu, P.; Zheng, Z.; Xu, Q.; Qian, Z.; Liu, J.; Ouyang, J. Valorization of dairy waste for enhanced D-lactic acid production at low cost. Process Biochem. 2018, 71, 18−22. (8) Wanarska, M.; Kur, J. A method for the production of D-tagatose using a recombinant Pichia pastoris strain secreting β-D-galactosidase from Arthrobacter chlorophenolicus and a recombinant L-arabinose isomerase from Arthrobacter sp. 22c. Microb. Cell Fact. 2012, 11, 113. (9) Xu, Z.; Xu, Z.; Tang, B.; Li, S.; Gao, J.; Chi, B.; Xu, H. Construction and co-expression of polycistronic plasmids encoding thermophilic L-arabinose isomerase and hyperthermophilic βgalactosidase for single-step production of D-tagatose. Biochem. Eng. J. 2016, 109, 28−34. (10) Zhan, Y.; Xu, Z.; Li, S.; Liu, X.; Xu, L.; Feng, X.; Xu, H. Coexpression of β-D-galactosidase and L-arabinose isomerase in the production of D-tagatose: a functional sweetener. J. Agric. Food Chem. 2014, 62, 2412−2417. (11) Zheng, Z.; Mei, W.; Xia, M.; He, Q.; Ouyang, J. Rational design of Bacillus coagulans NL01 L-arabinose isomerase and using its F279I variant in D-tagatose production. J. Agric. Food Chem. 2017, 65, 4715−4721.

ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jafc.8b05150.

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REFERENCES

Results of cultivation of S. cerevisiae NL22 in the presence of borate (PDF)

AUTHOR INFORMATION

Corresponding Author

*Phone: 86-025-85427129. Fax: 86-025-85427587. E-mail: [email protected]. ORCID

Jia Ouyang: 0000-0002-3467-253X Author Contributions ∥

Z.Z. and J.X. contributed equally to this work.

Funding

This study was supported by the National Natural Science Foundation of China (51561145015) and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD). F


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Elegant and Efficient Biotransformation for Dual Production of d

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