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Article

Review

J. Microbiol. Biotechnol. 2019; 29(3): 339-346

Published online March 28, 2019 https://doi.org/10.4014/jmb.1812.12015

Copyright © The Korean Society for Microbiology and Biotechnology.

Metabolic Engineering for Improved Fermentation of L-Arabinose

Suji Ye , Jeong-won Kim and Soo Rin Kim *

School of Food Science and Biotechnology, Kyungpook National University, Daegu, Korea

Correspondence to:Soorin Kim
soorinkim@knu.ac.kr

Received: December 10, 2018; Accepted: January 29, 2019

Abstract

L-Arabinose, a five carbon sugar, has not been considered as an important bioresource because most studies have focused on D-xylose, another type of five-carbon sugar that is prevalent as a monomeric structure of hemicellulose. In fact, L-arabinose is also an important monomer of hemicellulose, but its content is much more significant in pectin (3-22%, g/g pectin), which is considered an alternative biomass due to its low lignin content and mass production as juiceprocessing waste. This review presents native and engineered microorganisms that can ferment L-arabinose. Saccharomyces cerevisiae is highlighted as the most preferred engineering host for expressing a heterologous arabinose pathway for producing ethanol. Because metabolic engineering efforts have been limited so far, with this review as momentum, more attention to research is needed on the fermentation of L-arabinose as well as the utilization of pectin-rich biomass.

Keywords: L-arabinose, pectin, pentose, metabolic engineering, Saccharomyces cerevisiae

Significance of L-Arabinose as a Bioresource

Bioconversion of lignocellulosic biomass such as agricultural residues and wood waste materials into fuels and value-added chemicals is technically challenging due to a variety of factors [1-4]. Lignocellulosic biomass is composed of 40-50% cellulose, 25-30% hemicellulose, and 15-20% lignin, and the high lignin content requires strong physical and chemical pretreatment for its decomposition [5]. Also, hemicellulose is hydrolyzed into a mixture of glucose, xylose, and other minor sugars such as L- arabinose, and their fermentation is not efficiently done by any native industrial microorganisms [6]. For these reasons, industrial bioprocesses utilizing lignocellulosic biomass have not been realized so far, and the search for other alternative renewable biomass continues [7-10].

Meanwhile, fruit processing wastes such as orange peels are becoming abundant with the growth of the fresh juice industry, but are not being efficiently utilized [11, 12]. Fruit processing wastes are high in pectin (12-35%, g/g dry weight) with much less lignin content (approximately 2%, g/g dry weight) than lignocellulosic biomass [13]. Therefore, this pectin-rich biomass can be easily broken down into monomers; however, pectin monomers, like hemicellulose monomers, are not easily metabolized by common industrial hosts [14].

The primary chemical structure of pectin is methylated polygalacturonic acid in an alpha-(1-4) chain with branched oligosaccharides consisting of arabinose, galactose, xylose, and some minor sugars [15]. Among them, L-arabinose is one of the most abundant pentose sugars in pectin [16]. Arabinose content in various fruits and vegetables ranges from 3.3 to 21. 6 g/l (summarized in Table 1) [14, 17, 18]. It is contradictory to lignocellulosic biomass which has limited arabinose content (approximately 0.2%, g/g dry weight) [19].

Table 1 . Representative pectin-rich biomass and their arabinose content..

SourceArabinose, %1)Other major sugars2)Refs
Sugar beet pulp21.6 (0.28)Glu[17, 18]
Lime peel8.5Glu[14]
Pear peel6.0Glu, Xyl, Fru[14]
Orange peel5.6 (0.20)Glu, Fru[14, 17]
Apple pomace5.5Glu, Fru, Suc[14]
Mandarin peel3.3Glu, Fru, Suc[14]

1)% Dry matter (g/g pectin)..

2)Higher content than arabinose. Glu, Glucose; Xyl, xylose; Fuc, Fucose; Suc, Sucrose..



L-Arabinose is a five-carbon sugar like xylose. Unlike other sugars that naturally occur in the D-form, such as D-xylose, L-arabinose is a component of pectin and hemicellulose, and it is more common than D-arabinose in nature. Although studies have been conducted extensively for xylose metabolism to realize lignocellulosic bioprocesses [20], L-arabinose metabolism has not received much attention. In the present review, microbial strains that can natively metabolize L-arabinose are summarized. In some studies, the strains were engineered to produce useful products such as ethanol. Moreover, metabolic engineering efforts to develop efficient L-arabinose-fermenting strains using non-native but industrial hosts are discussed, focusing on Saccharomyces cerevisiae.

Native L-Arabinose-Fermenting Microorganisms

Arabinose catabolic pathways of native strains can be divided into the oxidoreductase (fungal) and isomerase (bacterial) pathways (Fig. 1). In both pathways, L-arabinose is converted into D-xylulose-5-phosphate, which is then canonically metabolized by the non-oxidative pentose phosphate pathway [21], or alternatively by the phospho- ketolase pathway such as that in Clostridium acetobutylicum [22].

Figure 1. Arabinose metabolic pathways in fungi (A) and bacteria (B). AR(XR); Aldose reductase, LAD; L-arabitol-4-dehydrogenase, LXR(ALX); L-xylulose reductase, XDH; D-xylulose reductase, XK; Xylulokinase, AI; L-arabinose isomerase, RK; L-Ribulokinase, R5PE; L-Ribulose-5-P-4-epimerase.

In L-arabinose-fermenting native fungi, L-arabinose is converted into D-xylulose by two reduction and two oxidation reactions, which are composed of NAD(P)H- specific aldose reductase (AR or XR), NAD+-specific L- arabitol-4-dehydrogenase (LAD), NAD(P)H-specific L-xylose reductase (LXR or ALX), and NAD+-specific xylitol dehydro- genase (XDH) [21]. Then, D-xylulose is phosphorylated into D-xylulose-5-phosphate by D-xylulokinase (XK). As highlighted in Fig. 1, fungal pathways of L-arabinose and D-xylose share three enzymes: AR (XR), XDH and XK. Although the cofactor preferences of AR and LXR (ALX) vary among fungal species, the first reductase enzyme usually prefers NADPH, while the two dehydrogenases strictly use NAD+. Therefore, redox balance of the pathway leading to efficient cell growth is achieved under aerobic conditions [23, 24]. Under oxygen-limited conditions, L- arabitol might be produced due to NAD+limitation, which is not found in the bacterial pathway of L-arabinose metabolism [25-27]. Because of the oxygen-dependent nature of the fungal pathway, ethanol production by these native strains is marginal [28, 29].

As early as 1990, a few native arabinose-fermenting fungi strains were identified, but the strains yielded a trace level of ethanol or even no ethanol production [26, 28]. In detail, 116 different yeast strains were screened for the ability to catabolize arabinose or xylose aerobically. As a result, four yeast strains (Ambrosiozyma monospora, and three Candida spp.) were found to ferment L-arabinose as a sole carbon source. Additionally, the ethanol yield was at most 0.18 (g/g consumed arabinose) with A. monospora and C. succiphila (Table 2).

Table 2 . Native arabinose-assimilating microorganisms and their engineered strains producing ethanol..

StrainGenotype1)Fermentation conditions2)Ethanol productionRefs

Arabinose (g/L)AerationTiter (g/L)Yield (g/g)
Yeast
Ambrosiozyma monospora Y-1484Wild type80OL4.10.18[28]
Candida succiphila Y-11998Wild type80OL3.90.05[28]
Bacteria
Sarcina ventriculiWild type19AN4.70.31[31]
Klebsiella oxytoca P2Zm_pdc, Zm_adhB80OL27.20.34[32]
Escherichia coli FBR3Zm_pdc, Zm_adhB, ldh△, pfl△100OL44.40.46[33]

1)Zm, Zymomonas mobilis; pdc, pyruvate decarboxylase gene; adhB, alcohol dehydrogenase gene; ldh, lactate dehydrogenase gene; pfl, pyruvate formate lyase gene..

2)All fermentations were performed with complex media with an initial arabinose concentration as shown above. Arabinose was the only carbon source available. OL, oxygen-limited conditions; AN, anaerobic conditions..



Meanwhile, 15 xylose-fermenting microorganisms were screened to evaluate the ability to ferment L-arabinose to ethanol [26]. As a result, one bacterium (Erwinia chrysanthemi), six yeast strains (C. tropicalis, C. shehatae, Pachysolen tannophilusY-2460, P. tannophilus Y-12891, Scheffersomyces stipitis, and Torulopsis sonorensis), and one mold strain (Aspergillus oryzae) were confirmed to assimilate arabinose with xylose and glucose as co-substrates. While E. chrysanthemi and C. tropicalis consumed xylose and arabinose simultaneously, all other fungal strains preferred xylose over arabinose. During arabinose metabolism, S. stipitis was the only fungal strain producing ethanol at a yield of 0.15 (g/g consumed sugar) and arabitol at a yield of 0.24 (g/g consumed sugar).

In comparison to the above-mentioned fungal pathways, bacterial pathways of L-arabinose metabolism are relatively simple; 1) only three enzymes are needed to convert to D-xylulose-5-phosphate, and 2) no cofactor is involved. The bacterial pathway consists of L-arabinose isomerase (AI), L-ribulose kinase (RK), and L-ribulose-5-phosphate-4- epimerase (R5PE) encoded by the araA, araB, and araD genes, respectively (Fig. 1B) [30]. In addition, native bacterial strains such as Sarcina ventriculi can ferment L-arabinose anaerobically and produce ethanol efficiently at a yield of 0.3 (g/g consumed arabinose) [31]. For some bacterial strains lacking the pdc and adh genes (encoding pyruvate decarboxylase and alcohol dehydrogenase, respectively) such as Klebsiella oxytoca, introducing the genes from Zymomonas mobilis enabled ethanol fermentation from L- arabinose [32]. For native L-arabinose-metabolizing Escherichia coli, in contrast, deletion of lactate dehydrogenase (ldh) and pyruvate formate lyase (pfl) genes was required to enable ethanol production from L-arabinose [33]. As summarized in Table 2, native bacterial strains assimilating L-arabinose can be promising hosts for ethanol fermentation.

Engineering Saccharomyces cerevisiae for L-Arabinose Fermentation

S. cerevisiae, the industrial host for bioethanol production, cannot utilize L-arabinose as efficiently as it can utilize xylose. For cellulosic ethanol production, a great amount of effort has been focused on the development of xylose- fermenting S. cerevisiae strains, while there have not been many examples for L-arabinose.

There are a limited number of studies on the development of S. cerevisiae expressing a heterologous fungal pathway of L-arabinose metabolism compared to that expressing a heterologous bacterial pathway [30,34-38]. Usually, xylose- fermenting S. cerevisiae expressing heterologous AR, XDH, and XK is first engineered by expressing Scheffersomyces stipitis XYL1, XYL2, and XYL3 genes, respectively, in most cases [20]. It has to be noted that an AR is NAD(P)H- specific aldose reductase with specificity for both xylose and L-arabinose [39] with a 50% higher rate for L-arabinose metabolism when using NADPH as a cofactor [40]. Next, the resulting strain is further engineered to express LAD and LXR, which are T. reesei LAD1 and A. monospora ALX1 genes, respectively [24, 34]. The S. cerevisiae 424A(LNH- ST)/pLXRNAD_LAD strain, which was developed as above, produced 10 g/l ethanol from 45 g/l L-arabinose [35] as summarized in Table 3. In another study, T. reesei LXR1 gene was expressed instead of A. monospora ALX1 gene, but the resulting strain only produced 0.1 g/l ethanol from 50 g/l L-arabinose [35, 41]. The low ethanol production can be explained by the fact that T. reesei LXR1 gene is now functionally identified as mannitol dehydrogenase [42]. Another factor determining L-arabinose fermentation efficiency is aeration. The fungal L-arabinose pathway is not redox-neutral because of the dual cofactor preference of AR and LXR (NADPH and NADH) while XDH and LAD are NAD -specific. Therefore, the cofactor imbalance issue could be more severe than xylose fermentation requiring just AR and XDH.

Table 3 . Ethanol fermentation by engineered Saccharomyces cerevisiae using arabinose as the sole carbon source..

Strain namesStrain backgroundsArabinose pathwaysOptimization strategiesMediaArabinose (g/L)AerationTiter (g/L)Yield (g/g consumed)Refs
Heterologous fungal pathways
H2561CEN.PK2SsXYL1, SsXYL2, ScXKS1,TrLAD1, TrLXR1-Minimal50AN0.1-[34]
424A(LNH-ST)/pLXRNAD-LAD424ASsXYL1, SsXYL2, SsXYL3,TrLAD1, AmALX1-Complex45OL9.40.22[35]
Heterologous bacterial pathways
JBY25-4MCEN.PK2-1CBsaraA, EcaraB, EcaraD, ScGAL2-Minimal20OL60.3[36]
BWY1-4SCEN.PK2-1CBsaraA, EcaraB, EcaraD, ScGAL2Codon optimizationAdaptive evolutionMinimal30AN90.39[43]
IMS0002CEN.PK2-1CLparaA, LparaB, LparaDPPP overexpressionAdaptive evolutionComplex20AN8.920.45[30]
BSW3APCEN.PK102-3ALparaA, LparaB,
PPP overexpressionMinimal20OL6.90.43[37]
LparaDAdaptive evolutionAN-0.42
BSW3AGCEN.PK102-3ALparaA, LparaB,LparaD,ScGAL2PPP overexpressionAdaptive evolutionMinimal20AN-0.43[37]

OL, oxygen-limited conditions; AN, anaerobic conditions; Bs, Bacillus subtilis; Ec, Escherichiacoli; Sc, Saccharomyces cerevisiae; Tr, Trichoderma reesei; Am, Ambrosiozyma monospora; Pi, Piromyces sp.; Lp, Lactobacillus plantarum; Nc, Neurospora crassa; Mt, Myceliophthora thermophile; Ss, Scheffersomyces stipitis; PPP, pentose phosphate pathway. .



Meanwhile, the bacterial L-arabinose pathway is redox- neutral; thus, more studies have been performed for heterologous expression in S. cerevisiae from genes of Bacillus subtilis, Escherichia coli and Lactobacillus plantarum. The bacterial L-arabinose pathway consisting of araA, araB and araD genes was tested with various combinations from different origins (Table 3). The araA gene from Bacillus subtilis [36], Bacillus licheniformis [43, 44] and Lactobacillus plantarum [30, 37] and the araB and araD genes from Escherichia coli [43, 44] or L. plantarum [30, 37] were tested. Ethanol production from the engineered strains varied between 6-9 g/l from 20 g/l L-arabinose. Regardless of the origin of the heterologous genes, various approaches to improve L-arabinose fermentation have been performed. In general, the overexpression of the non-oxidative pentose phosphate pathway genes (TAL1, TKL1, RPE1 and RKI1) and adaptive evolution were required [30, 36, 43]. However, despite all optimizations, the fermentation productivity is limited by a bacterial pathway possibly because of the unfavorable thermodynamic properties of L-arabinose isomerase under ambient conditions [45].

It should be noted that adaptive evolution is proven to be an effective metabolic engineering strategy to improve xylose fermentation by engineered S. cerevisiae strains for both fungal and bacterial pathways [20, 46]. However, for L-arabinose fermentation, only the engineered strains with a bacterial pathway have been subjected to adaptive evolution (Table 2). It can be explained by the fact that L-arabinose fermentation has not been performed systematically and extensively compared to xylose fermentation. It is also possible that the heterologous expression of a fungal pathway in S. cerevisiae requires multiple strategies to be optimized to overcome the severe redox imbalance issue.

Arabinose fermentation can be improved by expressing L-arabinose-specific sugar transporters (Table 4). S. cerevisiae could uptake arabinose through some hexose transporters such as Hxt5 and Hxt7 with low affinity [47]. S. cerevisiae Gal2 had the highest affinity to L-arabinose (57 mM) among other native hexose transporters [48, 49]. It is also reported that S. cerevisiae Gal2 contributed to anaerobic arabinose fermentation when arabinose is the sole carbon source [37]. Several heterologous arabinose transporters have been identified from Neurospora crassa [50], Myceliophthora thermophile [50], Penicillium chrysogenum [51], Arabidopsis thaliana [48], and Scheffersomyces stipitis [48], and their ability to uptake L-arabinose varies significantly (0.02-116.7 mmol/h/g DCW). N. crassa LAT-1 was the most efficient L-arabinose transporter reported with a rate of 116.7 (mmol/h/g DCW), which is 2 orders of magnitude higher than that of S. cerevisiae GAL2 0.13 (mmol/h/g DCW) [50]. P. chrysogenum AraT was a high-affinity arabinose transporter with no activity with glucose and xylose, although it was still inhibited by the presence of glucose and xylose [51, 52]. At the present stage, no heterologous sugar transporter was reported to either improve L- arabinose fermentation or allow simultaneous uptake of arabinose and glucose. In arabinose metabolism, as in xylose’s case [53, 54], it can be assumed that arabinose catabolism is currently more limiting than non-specific arabinose uptake in engineered S. cerevisiae.

Table 4 . Characterization of putative arabinose transporters over-expressed in a hexose transporter null mutant of Saccharomyces cerevisiae.

Transporter genesArabinose uptake rate (mmol/h/g DCW)Arabinose affinity (mM)References
Neurospora crassa LAT-1116.758.12[50]
Myceliophthora thermophile LAT-110.2929.39[50]
Penicillium chrysogenum AraT5.300.13[51]
Saccharomyces cerevisiae GAL20.1357.00[48]
Arabidopsis thaliana Stp20.044.50[48]
Scheffersomyces stipites AraT0.023.80[48]

Engineering of Other Microorganisms for Arabinose Fermentation

Some non-native arabinose fermenting microorganisms have also been engineered to assimilate L-arabinose and produce ethanol or other products. Z. mobilis (pZB206), which natively carries pdc and adhB but lacked arabinose- assimilating enzymes, was constructed by introducing E. coli araABD, talB, tktA to metabolize arabinose to ethanol [55]. The resulting strain showed an ethanol yield of 0.49 by consuming 25 g/l L-arabinose. Unlike S. cerevisiae, Corynebacterium glutamicum expressing E. coli araABD was easily engineered to produce amino acids such as L- glutamate, L-lysine, L-ornithine and L-arginine with arabinose as the sole carbon source [56]. For example, one of the engineered C. glutamicum strains produced L-glutamate at a yield of 0.07 from 75 g/l L-arabinose. Rhodococcus opacus expressing Streptomyces cattleya araABD fermented 16 g/l L-arabinose as the sole carbon source and produced fatty acids at a yield of 0.13 (g/g consumed arabinose). The fatty acids were mostly palmitic acid with some cis-10- heptadecenoic acid, oleic acid, myristic acid, pentadecanoic acid, palmitoleic acid, heptadecanoic acid, and stearic acid. Although the examples are limited, non-Saccharomyces cerevisiae strains can also be engineered to ferment L-arabinose and produce various value-added products other than ethanol.

Future Outlook

Both crop biomass and cellulosic biomass do not support sustainable bioprocesses due to their low contribution to greenhouse gas reduction [57] and limited technologies to overcome the recalcitrance [58], respectively. Alternatively, pectin-rich biomass such as fruit-processing wastes can be an attractive choice due to low lignin content and the growing demands for fresh juice. L-Arabinose is a primary sugar of pectin structure and its content is minimal in other biomass. As discussed in this review, research for L-arabinose fermentation is in an early stage. Thus, all options are open to either optimizing native arabinose- assimilating strains or engineering non-native strains such as S. cerevisiae, Z. mobilis, C. glutamicum, and R. opacus depending on the desired products. Engineered S. cerevisiae strains fermenting L-arabinose are still limited to ethanol production, however, various chemicals and value-added products are expected to be studied as well. Additionally, the development of strains fermenting other pectin-derived monomers such as galacturonic acid and L-rhamnose needs to be considered.

Acknowledgments

This work was carried out with the support of the “Cooperative Research Program for Agriculture Science & Technology Development (Project No. PJ01279801)” Rural Development Administration, Republic of Korea.

Conflict of Interest


The authors have no financial conflicts of interest to declare.

Fig 1.

Figure 1.Arabinose metabolic pathways in fungi (A) and bacteria (B). AR(XR); Aldose reductase, LAD; L-arabitol-4-dehydrogenase, LXR(ALX); L-xylulose reductase, XDH; D-xylulose reductase, XK; Xylulokinase, AI; L-arabinose isomerase, RK; L-Ribulokinase, R5PE; L-Ribulose-5-P-4-epimerase.
Journal of Microbiology and Biotechnology 2019; 29: 339-346https://doi.org/10.4014/jmb.1812.12015

Table 1 . Representative pectin-rich biomass and their arabinose content..

SourceArabinose, %1)Other major sugars2)Refs
Sugar beet pulp21.6 (0.28)Glu[17, 18]
Lime peel8.5Glu[14]
Pear peel6.0Glu, Xyl, Fru[14]
Orange peel5.6 (0.20)Glu, Fru[14, 17]
Apple pomace5.5Glu, Fru, Suc[14]
Mandarin peel3.3Glu, Fru, Suc[14]

1)% Dry matter (g/g pectin)..

2)Higher content than arabinose. Glu, Glucose; Xyl, xylose; Fuc, Fucose; Suc, Sucrose..


Table 2 . Native arabinose-assimilating microorganisms and their engineered strains producing ethanol..

StrainGenotype1)Fermentation conditions2)Ethanol productionRefs

Arabinose (g/L)AerationTiter (g/L)Yield (g/g)
Yeast
Ambrosiozyma monospora Y-1484Wild type80OL4.10.18[28]
Candida succiphila Y-11998Wild type80OL3.90.05[28]
Bacteria
Sarcina ventriculiWild type19AN4.70.31[31]
Klebsiella oxytoca P2Zm_pdc, Zm_adhB80OL27.20.34[32]
Escherichia coli FBR3Zm_pdc, Zm_adhB, ldh△, pfl△100OL44.40.46[33]

1)Zm, Zymomonas mobilis; pdc, pyruvate decarboxylase gene; adhB, alcohol dehydrogenase gene; ldh, lactate dehydrogenase gene; pfl, pyruvate formate lyase gene..

2)All fermentations were performed with complex media with an initial arabinose concentration as shown above. Arabinose was the only carbon source available. OL, oxygen-limited conditions; AN, anaerobic conditions..


Table 3 . Ethanol fermentation by engineered Saccharomyces cerevisiae using arabinose as the sole carbon source..

Strain namesStrain backgroundsArabinose pathwaysOptimization strategiesMediaArabinose (g/L)AerationTiter (g/L)Yield (g/g consumed)Refs
Heterologous fungal pathways
H2561CEN.PK2SsXYL1, SsXYL2, ScXKS1,TrLAD1, TrLXR1-Minimal50AN0.1-[34]
424A(LNH-ST)/pLXRNAD-LAD424ASsXYL1, SsXYL2, SsXYL3,TrLAD1, AmALX1-Complex45OL9.40.22[35]
Heterologous bacterial pathways
JBY25-4MCEN.PK2-1CBsaraA, EcaraB, EcaraD, ScGAL2-Minimal20OL60.3[36]
BWY1-4SCEN.PK2-1CBsaraA, EcaraB, EcaraD, ScGAL2Codon optimizationAdaptive evolutionMinimal30AN90.39[43]
IMS0002CEN.PK2-1CLparaA, LparaB, LparaDPPP overexpressionAdaptive evolutionComplex20AN8.920.45[30]
BSW3APCEN.PK102-3ALparaA, LparaB,
PPP overexpressionMinimal20OL6.90.43[37]
LparaDAdaptive evolutionAN-0.42
BSW3AGCEN.PK102-3ALparaA, LparaB,LparaD,ScGAL2PPP overexpressionAdaptive evolutionMinimal20AN-0.43[37]

OL, oxygen-limited conditions; AN, anaerobic conditions; Bs, Bacillus subtilis; Ec, Escherichiacoli; Sc, Saccharomyces cerevisiae; Tr, Trichoderma reesei; Am, Ambrosiozyma monospora; Pi, Piromyces sp.; Lp, Lactobacillus plantarum; Nc, Neurospora crassa; Mt, Myceliophthora thermophile; Ss, Scheffersomyces stipitis; PPP, pentose phosphate pathway. .


Table 4 . Characterization of putative arabinose transporters over-expressed in a hexose transporter null mutant of Saccharomyces cerevisiae.

Transporter genesArabinose uptake rate (mmol/h/g DCW)Arabinose affinity (mM)References
Neurospora crassa LAT-1116.758.12[50]
Myceliophthora thermophile LAT-110.2929.39[50]
Penicillium chrysogenum AraT5.300.13[51]
Saccharomyces cerevisiae GAL20.1357.00[48]
Arabidopsis thaliana Stp20.044.50[48]
Scheffersomyces stipites AraT0.023.80[48]

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