Next Article in Journal
Online Monitoring of Flowmeter Anomaly in Tobacco Production Process Using Sliding Window Recursive Lasso
Previous Article in Journal
Modelling the Mechanism of Sulphur Evolution in the Coal Combustion Process: The Effect of Sulphur–Nitrogen Interactions and Excess Air Coefficients
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Processes
Volume 11
Issue 5
10.3390/pr11051516
processes-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Lignocellulose-Derived Arabinose for Energy and Chemicals Synthesis through Microbial Cell Factories: A Review

by
Samuel Jacob
1,*,
Aswin Dilshani
1,
Srinivasan Rishivanthi
1,
Pratham Khaitan
1,
Adhinarayan Vamsidhar
1,
Gunasekaran Rajeswari
1,
Vinod Kumar
2,
Rajiv Chandra Rajak
3,
Mohd Fadhil Md. Din
4,5 and
Vasudeo Zambare
4,6,*
1
Department of Biotechnology, School of Bioengineering, College of Engineering and Technology, Faculty of Engineering and Technology, SRM Institute of Science and Technology, Kattankulathur 603203, India
2
School of Water, Energy and Environment, Cranfield University, Cranfield MK43 0AL, UK
3
Department of Botany, Marwari College, Ranchi University, Ranchi 834008, India
4
Centre for Environmental Sustainability and Water Security (IPASA), Universiti Teknologi Malaysia, Bahru 81310, Malaysia
5
Department of Water and Environmental Engineering, School of Civil Engineering, Universiti Teknologi Malaysia, Bahru 81310, Malaysia
6
R&D Department, Om Biotechnologies, Nashik 422011, India
*
Authors to whom correspondence should be addressed.
Processes 2023, 11(5), 1516; https://doi.org/10.3390/pr11051516
Submission received: 17 April 2023 / Revised: 5 May 2023 / Accepted: 11 May 2023 / Published: 16 May 2023
(This article belongs to the Section Environmental and Green Processes)
Browse Figures
Review Reports Versions Notes

Abstract

:
The exploration of natural substrates for microbial conversion to synthesize industrial platform and fuel chemicals seems to be inevitable within a circular bioeconomy context. Hemicellulose is a natural carbohydrate polymer consisting of a variety of pentose (C5) sugar monomers such as arabinose, mannose, erythrose, and xylose. Among the C5 sugars, L-arabinose (L-Ara) is the second-most-abundant pentose sugar in the lignocellulosic biomass after xylose. L-Ara has been used as an industrial carbon source to produce several value-added chemicals such as putrescine, which is used to synthesize polymers in the textile industry; sugar alcohols that are used as sweeteners in diet foods; and amino acids such as L-lysine, L-glutamate, L-arginine, and L-ornithine, which are used in nutritional supplements, fertilizers, and other products in the food and beverage industries. L-Ara, a natural non-caloric sweetener, is used as a substitute in the food and beverage industry, when the risk of blood sugar and lipid levels could be reduced. Major use of L-Ara is also found in the medical and pharmaceutical sectors to treat several conditions, including mineral absorption disorder, constipation, and diabetes, among others. In recent years, there has been a rising interest in synthesizing various sugar alcohols and derivatives, including arabitol, xylitol, and 2,3-butanediol, through the modification of producer organisms either genetically or metabolically to produce value-added products. Understanding the current demand and the need to increase the diversified production of industrial green chemicals with the reduced waste of useful lignocellulosic resources, this review focuses on the background of L-Ara and its various sources, microbes that utilize L-Ara to produce high-value-added products, and the future prospects for strain improvements to increase the yield of high-value-added products.

1. Introduction

In recent times, the term ‘Circular Bioeconomy’ is one of the keystones of the new economical and societal era to reverse climate changes and produce sustainable green chemicals from renewable carbon sources [1]. Among the various renewable resource options, lignocellulosic biomass (LCB) seems to be the major contributor, with an annual production of 0.2 trillion metric tons [2]. LCB also circumvents the food vs. fuel debate that is prominent among developing countries that reserve the most-abundant non-edible carbon feedstock either as an agro-industrial residue or as dedicated bioenergy crops. The plant biomass is mainly comprised of 65–85% of holocellulosic compounds (cellulose and hemicellulose) and 15–20% of lignin [3,4,5]. Over recent decades, substantial efforts have been taken for the conversion of cellulosic-derived glucose into biofuels and other value-added products. Hemicellulose is a natural carbohydrate polymer consisting of a variety of pentose (C5) sugar monomers such as arabinose, mannose, erythrose, and xylose. Among the C5 sugars, L-arabinose (L-Ara) is the second-most-abundant C5 sugar in LCB after xylose. L-Ara is used as an industrial carbon source to produce several value-added chemicals such as putrescine (a polymer used in the textile industry), ethanol/sugar alcohols (artificial sweeteners in diet foods, fuel additives, etc.), amino acids such as L-lysine, L-glutamate, L-arginine, and L-ornithine (nutritional supplements), fertilizers, and other products in the food and beverage industries [6,7,8,9]. Recent investigations revealed that the whole LCB could be an efficient resource for chemical and fuel production through a biorefinery framework, rather than only cellulose-based bio-renewables [10]. Therefore, a sustainable utilization of LCB prerequisites a completely integrated biorefinery framework that is analogous to a petroleum refinery. In a biorefinery, the holocellulosic fraction contributes a prime role in the production of bio-renewables, owing to its efficient hydrolysis into monomeric sugars that could be subsequently fermented into an array of high-value-added commodities. Table 1 represents a brief list of the value-added bioproducts that are produced. The global market value of food-grade L-Ara is expected to reach USD 33 million by 2028 [11]. In this regard, the valorization of L-Ara could be a promising alternative carbon source for industries that both economically and sustainably augment. There exists a bottleneck in the effective utilization of C5 sugars through microbial fermentation, wherein only a few industrially potent microbes are available for C5 sugar uptake through the specialized intramembrane transport mechanism and metabolic pathways, with a low product yield. However, the conventional metabolic pathway harbored by the microbial candidates possesses low-titer product yields. Hence, upgraded and adapted recent microbial technologies such as adaptive laboratory evolution (ALE) [12,13], metabolic engineering, and synthetic biology [14] have been recently emerging as a promising mitigation strategy to meet the industrial utilization of L-Ara for chemical synthesis and the purpose of establishing a sustainable greener technology [1]. To the best of the authors’ knowledge, this is the first report to shed light on the significance of hemicellulose-derived L-Ara as a renewable carbon source and its valorization toward several value-added commodity chemicals. It also highlights the different metabolic pathways involved in the assimilation of L-Ara by various microbial candidates for industrially important chemicals. In addition, different research directions in terms of metabolic engineering, synthetic biology, and microbial strain improvement strategies are discussed.

2. Abundance and Significance of L-Ara as a Bioresource

Hemicellulose, a heterogenous polymer that contains C5 sugars such as α- L-Ara and β-D-xylose, could reach 20–30% of the total LCB [17,18]. Figure 1 represents the potential of LCB, its sugar composition, and its valuable application in industries through microbial metabolic processes. In addition, some other sugars such as α -fucose and α-L-rhamnose are also present to a small extent, albeit rarely [19]. Based on the composition, presence, and side-chain ratio of the constituents, hemicellulose is distinguished as xyloglucan, glucuronoxylan, glucuronoarabinoxylan, galactoglucomanan, arabinoxylan, glucomannan, homoxylan, galactomannan, homomannan, arabinoxyloglucan, and arabinoglucuronoxylan. Among these, a considerable amount of L-Ara was found in arabinoglucuronoxylan, arabinoxyloglucan, glucuronoarabinoxylan, and arabinoxylan [20]. Rapid growth in the fresh juice industry has led to the abundance of fruit processing waste, which is not being efficiently utilized. Fruit processing waste such as pear peel, lime peel, orange peel, mandarin peel, and apple pomace is rich in pectin, i.e., 12–35% of the biomass dry weight has an insignificant amount of lignin (2%, w/w), compared to that of LCB [21,22,23,24,25]. Pectin is a complex heteropolysaccharide composed of α-1,4 linked D-galacturonic acid that contributes 70% of the total homogalacturonan polymer weight. When considering pectin, the presence of a limited amount of lignin merely enables the breakdown of polymers into monomers, where L-Ara becomes the most abundant of the C5 sugars. In addition to LCB, agro-industrial by-products such as wheat bran, corn fiber, sugar beet pulp, brewer’s spent grain, and sugarcane bagasse contain around 10.6%, 12.0%, 18.0%, 8.7%, and 1.3% of L-Ara, respectively [26,27,28,29,30,31]. Table 2 represents the different feedstocks/sources of L-Ara and its potential industrial applications. These abundant waste resources could be sustainably tapped for the L-Ara waste production of chemicals through various microbial candidates, which is discussed in the subsequent sections.

2.1. 2,3-Butanediol

2,3-Butanediol (2,3-BD) or 2,3-butylene glycol has various applications, such as as a chemical feedstock, a solvent, a liquid fuel, and a raw material for several resins and synthetic polymers [57]. A microorganism, identified as Enterobacter cloacae, was found to produce meso-2,3-BD as its primary product during fermentation. There are reports that pathogenic bacteria and other microbes produced 2, 3-BD. Klebsiella pneumoniae had the most significant 2, 3-BD titer of any bacterium, measuring 150 g/L [58]. Another productive maker of 2,3-BD, classified as a class 2 bacteria, was K. oxytoca, and this strain produced 2, 3-BD concentrations up to 130 g/L. Three bacteria with the Generally Recognized as Safe (GRAS) designation are effective 2, 3-BD producers: Bacillus amyloliquefaciens, B. licheniformis, and B. subtilis. The discovery of new strains and the enhancement of optical clarity has received abundant interest. Industrially applicable hosts, such as L. lactis, Saccharomyces cerevisiae, and Escherichia coli, are better-suited for large-scale production than indigenous hosts due to their effective genetics and well-proven cultivation techniques [59].
In a study conducted by Saha and Bothast, the authors checked the production of 2,3-BD by E. cloacae NRRL B-23289 by utilizing each of the following carbon sources individually: xylose, glucose, and L-Ara. The study was conducted at a pH of 5.0, a temperature of 30 °C, and 200 rpm. It showed that E. cloacae NRRL B-23289 utilizes the above-mentioned carbon sources in the order: xylose < glucose < L-Ara. About 0.37 g of glucose and 0.38 g of xylose were consumed in 63 h, and 0.43 g of L-Ara was consumed in 39 h. The bacteria were cultivated on mixtures of A and B, made of sugar, in proportions of 1:1:1 and 1:2:1 for glucose, xylose, and L-Ara, respectively. The bacterium variety was found to favor glucose over xylose and L-Ara over xylose. After a significant amount of L-Ara was consumed and only after all of the glucose was used up, the xylose started to vanish. Thus, the authors could use the E. cloacae NRRL B-23289 strain for the enhanced production of 2,3-BD using L-Ara as a carbon source [60].
For an array of sectors, including those in the chemical, cosmetics, agriculture, and medicine fields, 2,3-BD holds enormous potential. 2,3-BD has broad industrial applications, such as as a promising bulk chemical, which has plenty of further use. Its high heating value makes it an excellent drop-in fuel. It can also be converted to octane after adding the methyl ethyl ketone (MEK) and hydrogenation reaction, which is then used to produce superior aviation fuel. It is widely used to manufacture antifreeze agents, pharmaceuticals, synthetic rubber, fumigants, foodstuffs, perfumes, fuel additives, and printing inks [61].

2.2. Other Value-Added Products

For the past two decades, the market value for amino acids such as L-tryptophan, DL-methionine, L-lysine, L-aspartic acid, L-threonine, and L-glutamic acid has drastically increased owing to their wide range of applications in the food, cosmetics, agriculture, and pharmaceuticals sectors [62]. Recent studies reported the utilization of hemicellulose-derived L-Ara as the sole carbon source by engineering microbial strains for organic acids (lactic acid and succinic acid) and amino acids production [7,63,64]. Metabolic engineering of the Corynebacterium glutamicum ATCC 31831 strain resulted in the production of L-amino acids, namely, L-ornithine, L-lysine, L-threonine, L-methionine, L-glutamate, diamine putrescine (1,4-diaminobutane), and organic acids upon arabinose transporter gene (araE) expression [6,7,65]. On the other hand, overexpression of the ornithine decarboxylase gene (speC) from E. coli resulted in a high yield of putrescine by the C. glutamicum strain [16].

3. Overview of Distinct Natural Metabolic Pathways of L-Ara Assimilation by Microbes

Native microbes are able to grow on L-Ara derived from the hemicellulosic fraction of LCB via three distinct pathways, namely, the isomerase pathway, oxido-reductase pathway, and non-phosphorylative pathway (Figure 2). Firstly, the assimilation of L-Ara in eubacteria such as Streptomyces sp., lactococcus, Corynebacterium, and E. coli is initiated with the substrate uptake that is mediated by the active sugar transporters, followed by isomerization with L-arabinose isomerase to form L-ribulose. L-ribulose enters the central carbon metabolism (CCM) as D-xylulose-5-P through direct phosphorylation (catalyzed by L-ribulokinase) and epimerization (catalyzed by L-ribulose 5-P 4-epimerase) [1,66].
Secondly, in filamentous fungi, L-Ara metabolism is carried out by the oxido-reductive pathway. Similar to the isomerase pathway, L-Ara assimilation initiates with its uptake by relative sugar transporters. Concurrently, L-Ara reduces into L-arabitol by L-arabitol reductase (NADPH dependent) and then dehydrogenates into L and D-xylulose catalyzes by a series of enzymes such as L-arabitol dehydrogenase, L-xylulose reductase, and xylitol dehydrogenase. Finally, the phosphorylated D-xylulose enters the CCM pathway to recombine with glyceraldehyde-3-phosphate or its precursor molecule fructose-6-phosphate [26,67,68]. Though the overall pathway of L-Ara metabolism in filamentous fungi is redox-neutral, there exists a constraint in which a dissimilarity in the utilization of redox cofactors is observed. Thereby, making the C5 sugar, such as xylose, and L-Ara utilization as the sole carbon source possesses a major bottleneck for fermentative application. This is mitigated by employing a metabolic engineered yeast for fermentation [69]. Nevertheless, Pichia stipitis follows a distinct non-oxidative route, where D-xylulose is reduced into D-arabitol and then oxidized to D-ribulose by D-arabitol dehydrogenase and D-ribulose reductase, respectively [70]. This makes it a potent microbial candidate for C5 sugar fermentation.
The third pathway, known as non-phosphorylating pentose, is prevalent in archae bacteria where L-Ara is converted into either glycolaldehyde (Dahms pathway) and α-2-ketoglutarate (αKG) (Weimberg pathway) converges with CCM during the tricarboxylic acid cycle [71,72]. Enzymes such as L-arabinose dehydrogenase, L-arabinose lactonase, L-arabonate dehydratase, 2-keto-3-deoxy-l-arabinonate (KDA) dehydratase, and ketoglutarate semialdehyde (αKGSA) dehydrogenase are prominently involved in catalyzing L-Ara assimilation by the Weimberg pathway, as shown in Figure 2. The end product 2-keto-3-L-deoxypentonate formed in the Weimberg pathway takes an alternate route to form glycolaldehyde, which is catalyzed by 2-keto-3-deoxy L-pentanoate (KDP) aldolase and followed by αKGSA dehydrogenase to enter the CCM pathway. The promiscuity of metabolic enzymes remains uncertain owing to their redox cofactors’ dependence and also the co-existence of the Dahms and Weimberg biochemical routes in the same microbes, as represented in Figure 2 [1,73,74].

Kinetics of L-Ara Uptake by Different Microbes

In the near future, structural insights into highly conserved L-Ara catabolic enzymes and their substrate binding niche are likely to significantly progress. Herein, microbial genome data revealed that 30–40% of proteins belong to the paralogous/orthologous families, where the enzyme mechanism, the biochemical function, the oligomerization state, and protein–ligand interaction are uncovered by the protein structures [75,76]. In particular, Vermersch et al. [77] performed a mutation (Pro to Gly) in the L-Ara binding protein hinge, thereby enhancing and altering the binding and specificity. Thus, the structural and kinetic studies of the CAZymes in the L-Ara metabolic pathway provide an in-depth understanding of the enzyme mechanism for the entire pathway.
deGroot et al. [78] constructed a mathematical model based on the characterization of the kinetic parameters in various L-Ara catabolizing enzymes of Aspergillus niger such as L-arabitol dehydrogenase, D-xylose reductase, and L-arabinose reductase. The kinetic parameters of the relative enzymes such as L-arabinose reductase EW found to be Vmax −70 U/mg and Km −70 mM and Vmax −96 U/mg and Km −89 mM for L-arabitol dehydrogenase and Vmax-57 U/mg and Km-93 mM for D-xylose reductase in fungal L-Ara catabolism. Similarly, for A. nidulans, De Vries et al. [79] demonstrated that an increase in the production of L-Ara catabolizing enzymes enhances the accumulation of arabitol and, thus, reveals that sugar alcohol is a precise inducer of the system. Thus, the metabolic model could be used for analyzing the metabolite concentration and its flux in the L-Ara catabolic pathway, as indicated in Figure 2. Whereas, in the case of yeast, Fonseca et al. [80] investigated the L-Ara uptake kinetics for P. guilliermondii PYCC 3012 and Candida arabinofermentans PYCC 5603T, which showed a rapid and higher substrate-uptake rate. This study revealed that the aldopentose reductase of C. arabinofermentans PYCC 5603T such as aldose reductase or L-xylulose reductase (AR/LXR) showed a higher affinity toward the substrate, i.e., the L-Ara with 2.1 and 1.9 U/mg of Vmax, respectively, was higher than its counterpart. Recently, Lee et al. [81] intensified the thermophilic L-arabinose isomerase in the L-Ara catabolic pathway that is involved in catalyzing the L-Ara and L-ribulose interconversion. In detail, a comparative analysis of L-Ara catabolic protein structures such as AraA, AraB, AraD, and AraF was assessed to predict the L-Ara binding modules of Geobacillus stearothermophilus. In this study, the catalytic turnover rate (Kcat) of the mutant strains (11.9 to 27.8 s−1) was found to be three-fold less than that of the parental strain (33.8 s−1), which reveals that the mutation significantly reduced the Kcat. However, the Km values of the mutant strains were observed to be two-fold higher, while L-Ara is used as the sole carbon source when compared to the wild type. Thereby, the catalytic efficiency (Kcat/Km) of mutant strains such as E333, E261, and D195 was lowered as expected, which could play a vital role in the L-Ara binding affinity of G. stearothermophilus L-arabinose isomerase.

4. Native L-Ara Fermenting Strains and Its Metabolic Pathway

Among the C5 sugars predominant in hemicellulose hydrolysate, D-xylose is more often studied as a significant bioresource, whereas L-Ara utilization by any native industrial microbes remains unexplored. The catalytic pathways of the L-Ara in native fermenting strains are divided into the isomerase and oxidoreductase pathways for bacteria and fungi, respectively. The native fungal L-Ara pathway constitutes AR/LXR coupled with NAD(P)H oxidation to NADP+, whereas D-xylitol dehydrogenase (XDH) and L-arabitol-4-dehydrogenase (LAD) are coupled with the NAD+ cofactor followed by D-xylulose phosphorylation by D-xylulokinase (XK) [82,83]. The bacterial pathway for L-Ara catabolism is relatively simple when compared to the aforementioned fungal pathway, where araA encoding L-arabinose isomerase, araB encoding L-ribulose kinase, and araD genes encoding L-ribulose-5-phosphate-4-epimerase are the key enzymes involved [84]. In both pathways, D-xylulose-5-phosphate is formed from L-Ara, which is then either ideally metabolized by the phosphate ketolase pathway (as in C. acetobutylicum) or by the non-oxidative phase of the pentose phosphate pathway [85].
The native fungal pathway of C5 sugars such as L-Ara and xylose would share three enzymes in common: (NAD(P)H-specific AR/LXR and NAD+-specific xylose dehydrogenase. Thus, the redox balance of the metabolic pathway in fungi under an aerobic condition leads to effective cell growth, whereas under an anaerobic condition L-arabitol is produced, owing to the NAD+ limitations that are lacking in the bacterial pathway of L-Ara. Among the 116 identified native arabinose fermenting microbes, three Candida sp. and one Ambrosiozyma monospora were able to catabolize L-Ara (80 g/L) as the sole carbon source, and the ethanol yield was found to be 0.18 g/g under an oxygen-limited condition [86]. Meanwhile, Millan and Boynton [87] screened and evaluated the efficiency of 15 native xylose-fermenting strains’ ability to ferment L-Ara for ethanol production. In this study, L-Ara assimilated strains such as yeast (C. tropicalis, C. shehatae, Pachysolen tannophilus Y-2460, P. tannophilus Y-12891, Scheffersomyces stipitis, and Torulopsis sonorensis), mold (A. oryzae), and bacteria (Erwinia chrysanthemi) were identified as fermenting L-Ara combined with glucose and xylose as a co-substrate. During L-Ara metabolism, only S. stipitis produced 0.15 g/g of ethanol and yielded 0.24 g/g of arabitol compared to its other counterparts.
In general, the transport of sugar across the cell membrane is the foremost step in C5 sugar metabolism; nevertheless, only a meager amount of information is available on the yeast-based L-Ara transporters that could utilize L-Ara. In the case of C. shehatae, a native xylose-fermenting strain possesses a proton/L-Ara symporter [88]. Several types of yeast were identified as L-Ara assimilators, which produce cell biomass under aerobic and oxygen-limited conditions for L-arabitol production [80,89].

5. Metabolic Engineering of Microbial Cell Factories for Improved L-Ara Fermentation

The biosynthesis of biomass-based liquid biofuels and building block chemicals has been regarded as a renewable alternative to the conventional petroleum refinery. Over recent decades, extensive fundamental research on strain improvement has revealed that S. cerevisiae, E. coli, and Zymomonas mobilis possess innumerable desired characteristic features to be ideal candidates for the metabolic engineering and industrial production of the product spectrum such as sugar alcohols, biofuels, and value-added chemicals for a biomass-based biorefinery [90,91,92,93]. Different strategies for strain improvement such as mutagenesis, specific gene knockout, metabolic engineering, and ALE could aid a microbial candidate’s amenability for the significant production of different value-added products [94,95,96,97,98,99].

5.1. Engineering Zymomonas Mobilis for L-Ara Fermentation

Z. mobilis, a promising ethanologenic candidate; the homologous recombination of genes such as xylose reductase-XR (which improves xylose utilization), lactate dehydrogenase-IdhA, alcohol dehydrogenase-adhB and pyruvate decarboxylase-pdc (which has a lower lactate and ethanol yield which improves the succinate from glucose, respectively), and glucose fructose oxidoreductase-gfo (which reduces in ethanol production under ethanol, heat, and osmotic stress), were selected as a target of specific gene knockout for improving the specific phenotype (Figure 3) [100,101]. ALE in a model organism emerged as a prevailing strategy, where adaptation and metabolic engineering were synergistically employed in S. Cerevisiae [94,95,96,97], E. coli [98,99], and Z. mobilis for strain improvement. In the case of Z. mobilis, certain features such as the simultaneous utilization of glucose and C5 sugars and inhibitor tolerance were developed by many researchers through ALE to substitute lignocellulosic hydrolysate as an alternate for a conventional biorefinery. Among them, Z. mobilis CP4 (pZB5) and Z. mobilis CP4 (pZB206) were the first recombinant strains developed, where operons encoding pentose phosphate, the xylose assimilation pathway, and five L-Ara metabolic genes were introduced from E. coli, which could ferment C5 sugars such as xylose and L-Ara into 86% and 98% theoretical ethanol yields, respectively [102,103]. Then, Zhang et al. [104] constructed a co-fermenting strain (Z. mobilis 206C (pZB301)) for glucose and C5 sugars’ fermentation that resulted in 82%–84% of ethanol. However, the stability of recombinant strains is highly undesirable in large-scale fermentation; thereby, the genetic stability of the Zymomonas genome was enhanced by integrating all the necessary genes of pentose utilization to obtain a stable co-fermenting strain, Z. mobilis AX101 [105]. Compared to E. coli, Z. mobilis was developed as an effective ethanologenic-engineered strain, owing to its distinct metabolic pathway with a higher restriction-modification system of enzyme activity that is not borne by bacteriophages [93]. In addition, its osmo-tolerant ability benefits in industrial fermentation, by tolerating a high sugar medium and the utilization of C5 sugars (xylose, L-Ara) in addition to glucose, makes it a novel candidate for future biomass-based biorefineries [106]. Functional genomics, omics-related approaches, clustered regularly interspaced short palindromic repeats (CRISPR)/Cas system, Zinc-finger nucleases, global transcription machinery engineering, genome shuffling, and site-specific recombinase provide a base to improve the robustness and fitness toward environmental stress in order to enhance cellular traits. Further implementation of these representative biotechnologies will pave the way for a promising future in optimizing the metabolic pathway of Z. mobilis for the production of biofuels and value-added commodity chemicals to establish a sustainable green chemistry, as represented in Figure 3 [107,108,109,110,111,112].

5.2. Engineering Saccharomyces Cerevisiae for L-Ara Fermentation

As reported in earlier studies, the L-Ara metabolic pathway in bacteria is cofactor-dependent, and lacks an effective enzymatic assay, and the pathway optimization was not straightforward in S. cerevisiae. Based on this study, the E. coli genes (araA, araB, and araD) expressed in S. cerevisiae were not able to assimilate L-Ara; however, only after the replacement of the isomerase gene, along with the araA from B. subtilis with an ALE, then ethanol was produced from L-Ara [113,114]. Further, improvement in L-Ara utilization was investigated by modifying the bacterial codon usage to be the ideal yeast codon [115]. Thus, the L. plantarum metabolic genes for L-Ara were found to be more closely matched with the S. cerevisiae genes. Further, overexpression of this metabolic gene resulted in a high ethanol yield (0.43 g/g), with a 0.70 g/h/g dry cell weight (DCW) of the L-Ara consumption rate under an anaerobic condition [78]. Similarly, Wang et al. [116] modified the L-Ara metabolic pathway and transporter genes to investigate the metabolic ability of evolved S. cerevisiae with the overexpressed strain, where the recombinant strain resulted in a maximum ethanol yield of 0.43 g/g from L-Ara fermentation. Though many studies are focused on developing the D-xylose that assimilates S. cerevisiae strains, some [11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,84,85,86,87,88,89,90,91,92,93,94,95,96,97,98,99,100,101,102,103,104,105,106,107,108,109,110,111,112,113,113,114,115,116,117,118,119] are focused on the heterologous expression of the fungal and bacterial pathways of the L-Ara metabolism. For instance, the heterologous expression of the xyl1, xyl2, and xyl3 genes from the Scheffersomyces stipitis in S. cerevisiae possessed with NAD(P)H-dependent heterologous XDH, AR, and XDH genes showed a 50% higher L-Ara metabolism rate. Further, expressing LXR from A. monospora ALX1 and the LAD of T. reesei LAD1 in the parent recombinant strain assimilated 45 g/L of L-Ara into 10 g/L of ethanol [117,118,120]. In addition, the fungal metabolic pathway of L-Ara is considered to be non-redox-neutral, as it prefers dual cofactors (NAD(P)H and NADH), while the bacterial pathway is redox-neutral.
In order to enhance the D-xylose fermentation, ALE is proven to be an effective metabolic engineering strategy for both the bacterial and fungal pathways in an engineered strain of S. cerevisiae. Nevertheless, only engineered strains of S. cerevisiae with a bacterial L-Ara pathway were unveiled for ALE, as the optimization of multiple strategies is required to overcome the redox imbalance in S. cerevisiae during the heterologous expression of the fungal L-Ara pathway [82,121,122]. On the other hand, specific sugar transporters of L-Ara could be expressed to improve sugar fermentation; for example, S. cerevisiae could uptake L-Ara with some glucose sugar transporters (Hxt5 and Hxt7). It was reported that S. cerevisiae Gal2 had contributed to anaerobic fermentation with a high affinity toward L-Ara when used as the sole carbon source. The ability of some heterologous L-Ara-specific transporters in sugar uptake ranges from 116.7 mmol/h/g for DCW N. crassa LAT-1 to 0.13 mmol/h/g DCW for S. cerevisiae GAL2. Similar to xylose, in L-Ara metabolism, catabolism is more limited than the non-specific uptake of L-Ara by the engineered S. cerevisiae strain [116,123,124,125,126].
Both types of metabolic pathways of L-Ara are well-established in a native ethanologenic S. cerevisiae, yet it lacks the ability to ferment L-Ara. The engineered S. cerevisiae strain expresses NADH-specific genes (AR and LXR) to reduce the redox imbalance associated with the fungal metabolic pathway, where the arabitol yield was high with 0.48 g/g of sugar consumption when co-fermented with L-Ara and xylose [127,128]. Thus, the sugar uptake rate is the foremost step in utilization and prerequisites an efficient sugar transporter in order to attain enhanced C5 fermentation. Some of the hexose (Hxt5 and Hxt7) and galactose transporters (Gal2) show a high affinity toward C5 sugar assimilation [129,130]. Meanwhile, some of the C5 transporters such as XAT-1 specifically differentiate and effectively transport L-Ara rather than D-xylose. As reported earlier, the L-Ara fermentation of the engineered S. cerevisiae using hemicellulosic hydrolysates remains as the major bottleneck, Li et al. [126] functionally characterized the two transporters, namely, LAT-1 and MtLAT-1 from Neurospora crassa (FGSC 2489) and Myceliophthora thermophila (ATCC 42464), respectively. Thus, heterologous expression of C5 sugar-specific transporters could alleviate the inhibition of sugar uptake as well as enhance the co-fermentation of C5 and C6 sugars by rewiring the pentose assimilation [131].
Though many studies highlighted the native organism involved in L-Ara assimilation, the commercial application has been limited owing to its inhibition by furfurals and low tolerance toward ethanol. As S. cerevisiae is an amenable industrial candidate for metabolic engineering, owing to it resistance in various stress environments, Ye et al. [132] recently performed the heterologous integration of the fungal L-Ara pathway by deleting a phosphatase gene (PHO13). Herein, this gene deletion enhanced the consumption rate of L-Ara and the specific productivity of ethanol, and further TAL1 gene activation resulted in the depletion of sedoheptulose. Thus, engineering the PHO13 gene in a recombinant strain has ample potential as an industrial strain for L-Ara assimilation to ethanol. A schematic representation of the construction of a recombinant S. cerevisiae strain for the production of second-generation ethanol and arabitol using L-Ara is shown in Figure 4.

5.3. Fusants-A Distinct Hybrid Yeast

The genetic manipulation of microbes has opened new avenues in biomanufacturing. Among the different strategies, protoplast fusion technology (PFT) is a type of modification at the genomic level by the fusion of two protoplasts to form a hybrid cell, called a fusant. This PFT was proven to be a potential genetic manipulation, wherein the digestion of the cell wall by enzymes and the transfer of genetic material to the host strain enabled the combination of the superior traits of two different strains in a single producer strain. Some studies reported that yeast hybrids, known as fusant yeasts, attained through PFT are able to produce arabitol from fermentable sugars. Lin et al. [133] investigated the efficacy of a Schizosaccharomyces pombe and Lentinula edodes hybrid to produce L-arabitol with a yield of 0.76 g/g, using L-Ara as the sole carbon source. Karyoductants, obtained after a distinct fusion between the nuclei and protoplast of P. stipitis CCY 39501 and S. cerevisiae, respectively, would assimilate L-Ara; however, fusants named SP-K7 are identified by the ability to produce a high amount of L-arabitol (16.3 to 18.9 g/L) under the optimum condition [134].

5.4. Engineering Bacteria for L-Ara Fermentation

Recent studies are focused on improving the microbial capabilities for the overproduction of sugar alcohol such as sorbitol, xylitol, and mannitol by bacteria through various metabolic engineering strategies, for example, the co-expression of mannitol dehydrogenase, the facilitator protein of glucose, and formate dehydrogenase for mannitol production in Corynebacterium glutamicum; whereas, xylitol production is enhanced in E. coli through the heterologous expression of xylose reductase from yeast as well as achieving a higher sorbitol yield from glucose by overexpressing the sorbitol-6-phosphate dehydrogenase in L. plantarum that is deficient in the lactate dehydrogenase gene [135]. In a native strain such as E. coli, the deletion of some genes such as pyruvate formate lyase (pfl) and lactate dehydrogenase (Idh) was required in order to enable ethanol fermentation using L-Ara [136]. Nevertheless, K.oxytoca lacks adh and pdc genes encoding alcohol dehydrogenase and pyruvate decarboxylase, respectively. Thus, Bothast et al. [137] studied the strain fermentabilities by introducing Z. mobilis genes to enable L-Ara-based ethanol fermentation. Recently, Xiong et al. [138] engineered metabolically versatile oleaginous Rhodococcus jostii RHA1 through the heterologous expression of araBAD, a catabolic operon from E. coli, and, thus, the recombinant strain could assimilate L-Ara as the sole carbon source. Further, the cell biomass and lipid yield were improved by the overexpression of the L-Ara transporter gene araFGH and the atf1 gene (diglyceride acyltransferase) from E. coli and R. opacus PD630, respectively. Kawaguchi et al. [139] investigated the functional analysis of the gene cluster that encompassed the 6-cistron transcription unit that is involved in the utilization of L-Ara in C. glutamicum ATCC 31831. In this study, catabolic genes and operons such as araE and araBDA expression induced L-Ara and were negatively regulated by the AraR transcriptional regulator. Further, a unique L-Ara regulon (group of genes or operons) was found to be a distinct regulatory mechanism from the carbon catabolite repression of other bacterial strains. Table 3 represents the different organism types that were employed for L-arabitol production by utilizing L-Ara.

6. Conclusions and Future Perspectives

The advent of lignocellulosic biomass-based biorefining strategies paves the way for the valorization of agro-industrial waste with abundant C5 sugars into various biofuels and high-value-added products. L-arabinose (L-Ara), a C5 sugar, is the second-most-predominant pentose sugar in LCB that has been utilized as an industrial carbon source for the production of various value-added chemicals such as ethanol, sugar alcohols, putrescine, fertilizers, and amino acids. There is a need for the exploration of non-conventional sugars (other than glucose) for microbial fermentation, which seems to be inevitable for an economic edge in bioproducts’ development at an industrial scale. This review could provide a comprehensive aspect of arabinose, its natural availability, and an abundance of the lignocellulosic residue and microbial candidates suitable for arabinose valorization to chemicals and fuels. Though many industrial microbial candidates are able to naturally produce bio-compounds, genetic engineering strategies such as laboratory adaptive evolution have been widely explored for enhanced production. Whereas, non-native microbial candidates could be altered through metabolic engineering to facilitate the assimilation of hemicellulose-derived L-Ara. This would direct researchers and industry to explore the potential benefits of arabinose.

Author Contributions

Conceptualization, S.J. and V.K.; writing—original draft preparation (equal first author contribution), A.D., S.R., P.K., A.V. and G.R.; writing—review and editing, V.Z., M.F.M.D., V.K., R.C.R. and S.J.; visualization, G.R.; supervision, S.J., V.K. and V.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

The data presented in this study are available on request from the corresponding author. The data are not publicly available due to privacy.

Acknowledgments

R.G. and S.J. would like to acknowledge the Directorate of Research, SRM Institute of Science and Technology, Kattankulathur, for the financial support of their lignocellulosic research through the Selective Excellence Research Initiative scheme. A.D., S.R., P.K., A.V. and G.R. are grateful to the Department of Biotechnology, School of Bioengineering, SRM Institute of Science and Technology, Kattankulathur, for the infrastructure support to carry out their research work.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Francois, J.; Alkim, C.; Morin, N. Engineering microbial pathways for production of bio-based chemicals from lignocellulosi/.c sugars: Current status and perspectives. Biotechnol. Biofuels 2020, 13, 118. [Google Scholar] [CrossRef]
  2. Paul, S.; Dutta, A. Challenges and opportunities of lignocellulosic biomass for anaerobic digestion. Resour. Conserv. Recycl. 2018, 130, 164–174. [Google Scholar] [CrossRef]
  3. Holtzapple, M.T. Cellulose, hemicelluloses, and lignin. In Encyclopedia of Food Science, Food Technology, and Nutrition; Macrae, R., Robinson, R.K., Sadler, M.J., Eds.; Academic Press: London, UK, 1993; pp. 2731–2738. [Google Scholar]
  4. Sekeri, S.H.; Ibrahim, M.N.M.; Umar, K.; Yaqoob, A.A.; Azmi, M.N.; Hussin, M.H.; Othman, M.B.H.; Malik, M.F.I.A. Preparation and characterization of nanosized lignin from oil palm (Elaeis guineensis) biomass as a novel emulsifying agent. Int. J. Biol. Macromol. 2020, 164, 3114–3124. [Google Scholar] [CrossRef] [PubMed]
  5. Yaqoob, A.A.; Sekeri, S.H.; Othman, M.B.H.; Ibrahim, M.N.M.; Feizi, Z.H. Thermal degradation and kinetics stability studies of oil palm (Elaeis Guineensis) biomass-derived lignin nanoparticle and its application as an emulsifying agent. Arab. J. Chem. 2021, 14, 103182. [Google Scholar] [CrossRef]
  6. Schneider, J.; Niermann, K.; Wendisch, V. Production of the amino acids L-glutamate, L-lysine, L-ornithine and L-arginine from L-Ara by recombinant Corynebacterium glutamicum. J. Biotechnol. 2011, 154, 191–198. [Google Scholar] [CrossRef] [PubMed]
  7. Meiswinkel, T.; Gopinath, V.; Lindner, S.; Nampoothiri, K.; Wendisch, V. Accelerated pentose utilization by Corynebacterium glutamicum for accelerated production of lysine, glutamate, ornithine and putrescine. Microb. Biotechnol. 2012, 6, 131–140. [Google Scholar] [CrossRef]
  8. Rao, J.; Lv, Z.; Chen, G.; Peng, F. Hemicellulose: Structure, Chemical Modification, and Application. Prog. Polym. Sci. 2023, 140, 101675. [Google Scholar] [CrossRef]
  9. Pauly, M.; Gille, S.; Liu, L.; Mansoori, N.; de Souza, A.; Schultink, A.; Xiong, G. Hemicellulose biosynthesis. Planta 2013, 238, 627–642. [Google Scholar] [CrossRef]
  10. Banu, J.R.; Kavitha, P.S.; Tyagi, V.K.; Gunasekaran, M.; Karthikeyan, O.P.; Kumar, G. Lignocellulosic biomass based biorefinery: A successful platform towards circular bioeconomy. Fuel 2021, 302, 121086. [Google Scholar] [CrossRef]
  11. Market Watch. Food Grade L-Arabinose Market Demand by 2030. Available online: https://www.marketwatch.com/press-release/food-grade-l-arabinose-market-demand-by-2030-2023-04-06 (accessed on 10 April 2023).
  12. Lane, S.; Xu, H.; Oh, E.J.; Kim, H.; Lesmana, A.; Jeong, D.; Zhang, G.; Tsai, C.S.; Jin, Y.S.; Kim, S.R. Glucose repression can be alleviated by reducing glucose phosphorylation rate in Saccharomyces cerevisiae. Sci. Rep. 2018, 8, 2613. [Google Scholar] [CrossRef]
  13. Mohamed, E.T.; Mundhada, H.; Landberg, J.; Cann, I.; Mackie, R.I.; Nielsen, A.T.; Herrgard, M.J.; Feist, A.M. Generation of an E. coli platform strain for improved sucrose utilization using adaptive laboratory evolution. Microb. Cell Fact. 2019, 18, 116. [Google Scholar] [CrossRef] [PubMed]
  14. Ceroni, F.; Carbonell, P.; François, J.M.; Haynes, K.A. Editorial–Synthetic biology: Engineering complexity and refactoring cell capabilities. Front. Bioeng. Biotechnol. 2015, 3, 120. [Google Scholar] [CrossRef] [PubMed]
  15. Kim, H.M.; Park, J.H.; Choi, I.S.; Wi, S.G.; Ha, S.; Chun, H.H.; Hwang, I.M.; Chang, J.Y.; Choi, H.-J.; Kim, J.-C.; et al. Effective approach to organic acid production from agricultural kimchi cabbage waste and its potential application. PLoS ONE 2018, 13, e0207801. [Google Scholar] [CrossRef] [PubMed]
  16. Schneider, J.; Eberhardt, D.; Wendisch, V.F. Improving putrescine production by Corynebacterium glutamicum by fine-tuning ornithine transcarbamoylase activity using a plasmid addiction system. Appl. Microbiol. Biotechnol. 2012, 95, 169–178. [Google Scholar] [CrossRef] [PubMed]
  17. Venkateswar Rao, L.; Goli, J.; Gentela, J.; Koti, S. Bioconversion of lignocellulosic biomass to xylitol: An overview. Bioresour. Technol. 2016, 213, 299–310. [Google Scholar] [CrossRef]
  18. Safian, M.T.-U.; Sekeri, S.H.; Yaqoob, A.A.; Serra, A.; Jamudin, M.D.; Ibrahim, M.N.M. Utilization of lignocellulosic biomass: A practical journey towards the development of emulsifying agent. Talanta 2022, 239, 123109. [Google Scholar] [CrossRef]
  19. Gírio, F.; Fonseca, C.; Carvalheiro, F.; Duarte, L.; Marques, S.; Bogel-Łukasik, R. Hemicelluloses for fuel ethanol: A review. Bioresour. Technol. 2010, 101, 4775–4800. [Google Scholar] [CrossRef]
  20. Fehér, C. Novel approaches for biotechnological production and application of L-arabinose. J. Carbohydr. Chem. 2018, 37, 251–284. [Google Scholar] [CrossRef]
  21. Kennedy, M.; List, D.; Lu, Y.; Foo, L.Y.; Newman, R.H.; Sims, I.M.; Bain, P.J.S.; Hamilton, B.; Fenton, G. Apple pomace and products derived from apple pomace: Use, composition and analysis. In Modern Methods of Plant Analysis, Analysis of Plant Waste Materials; Linskens, H.F., Jackson, J.F., Eds.; Springer-Verlag: Berlin, Germany, 1999; Volume 20, pp. 75–119. [Google Scholar]
  22. Doran, J.B.; Cripe, J.; Sutton, M.; Foster, B. Fermentations of pectin rich biomass with recombinant bacteria to produce fuel ethanol. Appl. Biochem. Biotechnol. 2000, 84, 141–152. [Google Scholar] [CrossRef]
  23. Mohnen, D. Pectin structure and biosynthesis. Curr. Opin. Plant Biol. 2008, 11, 266–277. [Google Scholar] [CrossRef]
  24. Zhou, W.; Widmer, W.; Grohmann, K. Developments in ethanol production from citrus peel waste. Proc. Fla. State Hort. Soc. 2008, 121, 307–310. [Google Scholar]
  25. Edwards, M.; Doran-Peterson, J. Pectin-rich biomass as feedstock for fuel ethanol production. Appl. Microbiol. Biotechnol. 2012, 95, 565–575. [Google Scholar] [CrossRef]
  26. Seiboth, B.; Metz, B. Fungal arabinan and L-arabinose metabolism. Appl. Microbiol. Biotechnol. 2011, 89, 1665–1673. [Google Scholar] [CrossRef] [PubMed]
  27. Hollmann, J.; Lindhauer, M. Pilot-scale isolation of glucuronoarabinoxylans from wheat bran. Carbohydr. Polym. 2005, 59, 225–230. [Google Scholar] [CrossRef]
  28. Fehér, C. Integrated process of arabinose biopurification and xylitol fermentation based on the diverse action of Candida boidinii. Chem. Biochem. Eng. Q. 2016, 29, 587–597. [Google Scholar] [CrossRef]
  29. Kühnel, S.; Schols, H.; Gruppen, H. Aiming for the complete utilization of sugar-beet pulp: Examination of the effects of mild acid and hydrothermal pretreatment followed by enzymatic digestion. Biotechnol. Biofuels 2011, 4, 14. [Google Scholar] [CrossRef] [PubMed]
  30. Treimo, J.; Westereng, B.; Horn, S.J.; Forssell, P.; Robertson, J.A.; Faulds, C.B.; Waldron, K.W.; Buchert, J.; Eijsink, V.G.H. Enzymatic solubilization of brewers’ spent grain by combined action of carbohydrases and peptidases. J. Agric. Food Chem. 2009, 57, 3316–3324. [Google Scholar] [CrossRef]
  31. Gottschalk, L.; Oliveira, R.; Bon, E. Cellulases, xylanases, β-glucosidase and ferulic acid esterase produced by Trichoderma and Aspergillus act synergistically in the hydrolysis of sugarcane bagasse. Biochem. Eng. J. 2010, 51, 72–78. [Google Scholar] [CrossRef]
  32. Sakdaronnarong, C.; Jonglertjunya, W. Rice straw and sugarcane bagasse degradation mimicking lignocellulose decay in nature: An alternative approach to biorefinery. ScienceAsia 2012, 38, 364. [Google Scholar] [CrossRef]
  33. Sabiha-Hanim, S.; Siti-Norsafurah, A.M. Physical properties of hemicellulose films from sugarcane bagasse. Procedia Eng. 2012, 42, 1390–1395. [Google Scholar] [CrossRef]
  34. Tsigie, Y.; Wang, C.; Truong, C.; Ju, Y. Lipid production from Yarrowia lipolytica Po1g grown in sugarcane bagasse hydrolysate. Bioresour. Technol. 2011, 102, 9216–9222. [Google Scholar] [CrossRef] [PubMed]
  35. Yang, S.; Zhang, Y.; Yue, W.; Wang, W.; Wang, Y.-Y.; Yuan, T.-Q.; Sun, R.-C. Valorization of lignin and cellulose in acid-steam-exploded corn stover by a moderate alkaline ethanol post-treatment based on an integrated biorefinery concept. Biotechnol. Biofuels. 2016, 9, 238. [Google Scholar] [CrossRef]
  36. Cellulosic Biofuel Process Can also Improve Ruminant Forage Digestibility. MSU Extension. Available online: https://www.canr.msu.edu/news/cellulosic_biofuel_process_can_also_improve_ruminant_forage_digestibility. (accessed on 28 April 2022).
  37. Fehér, A. Combined approaches to xylose production from corn stover by dilute acid hydrolysis. Chem. Biochem. Eng. Q. 2017, 31, 77–87. [Google Scholar] [CrossRef]
  38. Jiang, M.; Zhao, M.; Zhou, Z.; Huang, T.; Chen, X.; Wang, Y. Isolation of cellulose with ionic liquid from steam exploded rice straw. Ind. Crops Prod. 2011, 33, 734–738. [Google Scholar] [CrossRef]
  39. Pinzi, S.; Dorado, M. Vegetable-based feedstocks for biofuels production. In Handbook of Biofuels Production: Processes and Technologies; Luque, R., Campelo, J., Clark, J., Eds.; Woodhead Publishing Ltd.: Cambridge, UK, 2011; pp. 61–94. [Google Scholar]
  40. Roberto, I.; Mussatto, S.; Rodrigues, R. Dilute-acid hydrolysis for optimization of xylose recovery from rice straw in a semi-pilot reactor. Ind. Crops. Prod. 2003, 17, 171–176. [Google Scholar] [CrossRef]
  41. Nigam, J.N. Bioconversion of water-hyacinth (Eichhornia crassipes) hemicellulose acid hydrolysate to motor fuel ethanol by xylose-fermenting yeast. J. Biotechnol. 2002, 97, 107–116. [Google Scholar] [CrossRef] [PubMed]
  42. Alfaro, J.R.; Daza, L.T.; Lindado, G.; Peláez, H.C.; Córdoba, Á.P. Acid hydrolysis of water hyacinth to obtaining fermentable sugars. Cienc. Tecnol. Futuro. 2013, 5, 101–112. [Google Scholar] [CrossRef]
  43. Carvalheiro, F.; Silva-Fernandes, T.; Duarte, L.C.; Gírio, F.M. Wheat straw autohydrolysis: Process optimization and products characterization. Appl. Biochem. Biotechnol. 2009, 153, 84–93. [Google Scholar] [CrossRef]
  44. Farhat, W.; Venditti, R.; Hubbe, M.; Taha, M.; Becquart, F.; Ayoub, A. A review of water-resistant hemicellulose-based materials: Processing and applications. Chem. Sus. Chem. 2016, 10, 305–323. [Google Scholar] [CrossRef]
  45. Tozluoğlu, A.; Özyurek, Ö.; Çöpür, Y.; Özdemir, H. Integrated production of biofilm, bioethanol, and papermaking pulp from wheat Straw. Bioresour. 2015, 10, 7834–7854. [Google Scholar] [CrossRef]
  46. Olmos, J.C.; Hansen, M.Z. Enzymatic depolymerization of sugar beet pulp: Production and characterization of pectin and pectic-oligosaccharides as a potential source for functional carbohydrates. Chem. Eng. J. 2012, 192, 29–36. [Google Scholar] [CrossRef]
  47. Saric, L.; Filipcev, B.; Simurina, O.; Plavsic, D. Sugar beet molasses: Properties and applications in osmotic dehydration of fruits and vegetables. Food Feed Res. 2016, 43, 135–144. [Google Scholar] [CrossRef]
  48. Dinand, E.; Chanzy, H.; Vignon, M. Parenchymal cell cellulose from sugar beet pulp: Preparation and properties. Cellulose 1996, 3, 183–188. [Google Scholar] [CrossRef]
  49. Eveleigh, D.E. Comprehensive biotechnology: The principles, applications and regulations of biotechnology in industry, agriculture and medicine. In The Principles of Biotechnology: Scientific Fundamentals; Moo-Young, M., Bull, A.T., Dalton, H., Eds.; Pergamon Press: Oxford, UK, 1985; Volume 1, p. 688. [Google Scholar]
  50. Gama, R.; Dyk, J.V.; Pletschke, B. Optimisation of enzymatic hydrolysis of apple pomace for production of biofuel and biorefinery chemicals using commercial enzymes. 3 Biotech 2015, 5, 1075–1087. [Google Scholar] [CrossRef] [PubMed]
  51. Ayala, J.R.; Montero, G.; Coronado, M.A.; García, C.; Curiel-Alvarez, M.A.; León, J.A.; Sagaste, C.A.; Montes, D.G. Characterization of orange peel waste and valorization to obtain reducing sugars. Molecules 2021, 26, 1348. [Google Scholar] [CrossRef]
  52. Torrado, A.M.; Cortés, S.; Salgado, J.M.; Max, B.; Rodríguez, N.; Bibbins, B.P.; Converti, A.; Domínguez, J.M. Citric acid production from orange peel wastes by solid-state fermentation. Braz. J. Microbiol. 2011, 42, 394–409. [Google Scholar] [CrossRef]
  53. Nawirska, A.; Kwaśniewska, M. Dietary fibre fractions from fruit and vegetable processing waste. Food Chem. 2005, 91, 221–225. [Google Scholar] [CrossRef]
  54. Szymańska-Chargot, M.; Chylińska, M.; Gdula, K.; Kozioł, A.; Zdunek, A. Isolation and characterization of cellulose from different fruit and vegetable pomaces. Polymers 2017, 9, 495. [Google Scholar] [CrossRef]
  55. Kheiralla, Z.H.; El-Gendy, N.S.; Ahmed, H.A.; Shaltout Th, H.; Hussein, M.M.D. Upgrading of Tomato (Solanum lycopersicum) Agroindustrial Wastes. J. Microb. Biochem. Technol. 2018, 10, 46–48. [Google Scholar] [CrossRef]
  56. Del Valle, M.; Cámara, M.; Torija, M. Chemical characterization of tomato pomace. J. Sci. Food Agric. 2006, 86, 1232–1236. [Google Scholar] [CrossRef]
  57. Song, C.W.; Park, J.M.; Chung, S.C.; Lee, S.Y.; Song, H. Microbial production of 2,3-butanediol for industrial applications. J. Ind. Microbiol. Biotechnol. 2019, 46, 1583–1601. [Google Scholar] [CrossRef]
  58. Ma, C.; Wang, A.; Qin, J.; Li, L.; Ai, X.; Jiang, T.; Tang, H.; Xu, P. Enhanced 2, 3-butanediol production by Klebsiella pneumoniae SDM. Appl. Microbiol. Biotechnol. 2009, 82, 49–57. [Google Scholar] [CrossRef] [PubMed]
  59. Yang, Z.; Zhang, Z. Recent advances on production of 2, 3-butanediol using engineered microbes. Biotechnol. Adv. 2019, 37, 569–578. [Google Scholar] [CrossRef]
  60. Saha, B.C.; Bothast, R.J. Production of 2,3-butanediol by newly isolated Enterobacter cloacae. Appl. Microbiol. Biotechnol. 1999, 52, 321–326. [Google Scholar] [CrossRef]
  61. Białkowska, A.M. Strategies for efficient and economical 2, 3-butanediol production: New trends in this field. World J. Microbiol. Biotechnol. 2016, 32, 1–14. [Google Scholar] [CrossRef] [PubMed]
  62. Leuchtenberger, W.; Huthmacher, K.; Drauz, K. Biotechnological production of amino acids and derivatives: Current status and prospects. Appl. Microbiol. Biotechnol. 2005, 69, 1–8. [Google Scholar] [CrossRef] [PubMed]
  63. Hahn-Hagerdal, B.; Karhumaa, K.; Fonseca, C.; Spencer-Martins, I.; Gorwa-Grauslund, M.F. Towards industrial pentose-fermenting yeast strains. Appl. Microbiol. Biotechnol. 2007, 74, 937–953. [Google Scholar] [CrossRef] [PubMed]
  64. Gopinath, V.; Meiswinkel, T.M.; Wendisch, V.F.; Nampoothiri, K.M. Amino acid production from rice straw and wheat bran hydrolysates by recombinant pentose-utilizing Corynebacterium glutamicum. Appl. Microbiol. Biotechnol. 2011, 92, 985–996. [Google Scholar] [CrossRef]
  65. Sasaki, M.; Jojima, T.; Kawaguchi, H.; Inui, M.; Yukawa, H. Engineering of pentose transport in Corynebacterium glutamicum to improve simultaneous utilization of mixed sugars. Appl. Microbiol. Biotechnol. 2009, 85, 105–115. [Google Scholar] [CrossRef]
  66. Jojima, T.; Omumasaba, C.; Inui, M.; Yukawa, H. Sugar transporters in efficient utilization of mixed sugar substrates: Current knowledge and outlook. Appl. Microbiol. Biotechnol. 2009, 85, 471–480. [Google Scholar] [CrossRef]
  67. Chiang, C.; Knight, S.G. L-Arabinose metabolism by cell-free extracts of Penicillium chrysogenum. Biochim. Biophys. Acta 1961, 46, 271–278. [Google Scholar] [CrossRef] [PubMed]
  68. Witteveen, C.F.B.; Busink, R.; van de Vondervoort, P.; Dijkema, C.; Swart, K.; Visser, J. L-Arabinose and D-xylose catabolism in Aspergillus niger. J. Gen. Microbiol. 1989, 135, 2163–2171. [Google Scholar] [CrossRef]
  69. Umai, D.; Kayalvizhi, R.; Kumar, V.; Jacob, S. Xylitol: Bioproduction and applications-A Review. Front. Sustain. 2022, 3, 826190. [Google Scholar] [CrossRef]
  70. Jin, Y.; Cruz, J.; Jeffries, T. Xylitol production by a Pichia stipitis D-xylulokinase mutant. Appl. Microbiol. Biotechnol. 2005, 68, 42–45. [Google Scholar] [CrossRef]
  71. Dahms, A.S. 3-Deoxy-D-pentulosonic acid aldolase and its role in a new pathway of D-xylose degradation. Biochem. Biophys. Res. Commun. 1974, 60, 1433–1439. [Google Scholar] [CrossRef] [PubMed]
  72. Weimberg, R. Pentose oxidation by Pseudomonas fragi. J. Biol. Chem. 1961, 236, 629–635. [Google Scholar] [CrossRef] [PubMed]
  73. Sato, T.; Atomi, H. Novel metabolic pathways in Archaea. Curr. Opin. Microbiol. 2011, 14, 307–314. [Google Scholar] [CrossRef] [PubMed]
  74. McClintock, M.K.; Wang, J.; Zhang, K. Application of nonphosphorylative metabolism as an alternative for utilization of Lignocellulosic Biomass. Front Microbiol. 2017, 8, 2310. [Google Scholar] [CrossRef]
  75. Burley, S.; Bonanno, J. Structural genomics of proteins from conserved biochemical pathways and processes. Curr. Opin. Struct. Biol. 2002, 12, 383–391. [Google Scholar] [CrossRef]
  76. Liu, J.; Rost, B. Comparing function and structure between entire proteomes. Protein Sci. 2001, 10, 1970–1979. [Google Scholar] [CrossRef]
  77. Vermersch, P.S.; Tesmer, J.J.; Lemon, D.D.; Quiocho, F.A. A Pro to Gly mutation in the hinge of the arabinose-binding protein enhances binding and alters specificity. Sugar-binding and crystallographic studies. J. Biol. Chem. 1990, 265, 16592–16603. [Google Scholar] [CrossRef] [PubMed]
  78. deGroot, M.; Prathumpai, W.; Visser, J.; Ruijter, G. Metabolic control analysis of Aspergillus niger L-arabinose catabolism. Biotechnol. Prog. 2005, 21, 1610–1616. [Google Scholar] [CrossRef] [PubMed]
  79. de Vries, R.P.; Flipphi, M.J.; Witteveen, C.F.; Visser, J. Characterization of an Aspergillus nidulans L-arabitol dehydrogenase mutant. FEMS Microbial. Lett. 1994, 123, 83–90. [Google Scholar] [CrossRef]
  80. Fonseca, C.; Spencer-Martins, I.; Hahn-Hägerdal, B. L-arabinose metabolism in Candida arabinofermentans PYCC 5603T and Pichia guilliermondii PYCC 3012: Influence of sugar and oxygen on product formation. Appl. Microbiol. Biotechnol. 2007, 75, 303–310. [Google Scholar] [CrossRef] [PubMed]
  81. Lee, Y.-J.; Lee, S.-J.; Kim, S.-B.; Lee, S.J.; Lee, S.H.; Lee, D.-W. Structural insights into conserved L-arabinose metabolic enzymes reveal the substrate binding site of a thermophilic L-arabinose isomerase. FEBS. Lett. 2014, 588, 1064–1070. [Google Scholar] [CrossRef]
  82. Ye, S.; Kim, J.; Kim, S. Metabolic engineering for improved fermentation of L-arabinose. J. Microbiol. Biotechnol. 2019, 29, 339–346. [Google Scholar] [CrossRef]
  83. Hahn-Hägerdal, B.; Karhumaa, K.; Jeppsson, M.; Gorwa-Grauslund, M. Metabolic engineering for pentose utilization in Saccharomyces cerevisiae. Biofuels 2007, 108, 147–177. [Google Scholar] [CrossRef]
  84. Wisselink, H.W.; Toirkens, M.J.; del Rosario Franco Berriel, M.; Winkler, A.A.; van Dijken, J.P.; Pronk, J.T.; van Maris, A.J.A. Engineering of Saccharomyces cerevisiae for efficient anaerobic alcoholic fermentation of l-arabinose. Appl. Environ. Microbiol. 2007, 73, 4881–4891. [Google Scholar] [CrossRef]
  85. Servinsky, M.D.; Germane, K.L.; Liu, S.; Kiel, J.T.; Clark, A.M.; Shankar, J.; Sund, C.J. Arabinose is metabolized via a phosphoketolase pathway in Clostridium acetobutylicum ATCC 824. J. Ind. Microbiol. Biotechnol. 2012, 39, 1859–1867. [Google Scholar] [CrossRef]
  86. Dien, B.; Kurtzman, C.; Saha, B.; Bothast, R. Screening for L-arabinose fermenting yeasts. Appl. Biochem. Biotechnol. 1996, 57-58, 233–242. [Google Scholar] [CrossRef]
  87. McMillan, J.D.; Boynton, B.L. Arabinose utilization by xylose-fermenting yeasts and fungi. Appl. Biochem. Biotechnol. 1994, 45-46, 569–584. [Google Scholar] [CrossRef]
  88. Lucas, C.; van Uden, N. Transport of hemicellulose monomers in the xylose-fermenting yeast Candida shehatae. Appl. Microbiol. Biotechnol. 1986, 23, 491–495. [Google Scholar] [CrossRef]
  89. Kordowska-Wiater, M. Production of arabitol by yeasts: Current status and future prospects. J. Appl. Microbiol. 2015, 119, 303–314. [Google Scholar] [CrossRef] [PubMed]
  90. Hong, K.-K.; Nielsen, J. Metabolic engineering of Saccharomyces cerevisiae: A key cell factory platform for future biorefineries. Cell. Mol. Life Sci. 2012, 69, 2671–2690. [Google Scholar] [CrossRef]
  91. Chen, X.; Zhou, L.; Tian, K.; Kumar, A.; Singh, S.; Prior, B.A.; Wang, Z. Metabolic engineering of Escherichia coli: A sustainable industrial platform for bio-based chemical production. Biotechnol. Adv. 2013, 31, 1200–1223. [Google Scholar] [CrossRef] [PubMed]
  92. Nielsen, J.; Larsson, C.; Maris, A.V.; Pronk, J. Metabolic engineering of yeast for production of fuels and chemicals. Curr. Opin. Biotechnol. 2013, 24, 398–404. [Google Scholar] [CrossRef] [PubMed]
  93. Rogers, P.L.; Jeon, Y.J.; Lee, K.J.; Lawford, H.G. Zymomonas mobilis for fuel ethanol and higher value products. Biofuels 2007, 108, 263–288. [Google Scholar] [CrossRef]
  94. Wallace-Salinas, V.; Gorwa-Grauslund, M. Adaptive evolution of an industrial strain of Saccharomyces cerevisiae for combined tolerance to inhibitors and temperature. Biotechnol. Biofuels 2013, 6, 151. [Google Scholar] [CrossRef]
  95. Çakar, Z.; Turanlı-Yıldız, B.; Alkım, C.; Yılmaz, Ü. Evolutionary engineering of Saccharomyces cerevisiae for improved industrially important properties. FEMS Yeast Res. 2011, 12, 171–182. [Google Scholar] [CrossRef]
  96. Demeke, M.M.; Dietz, H.; Li, Y.; Foulquié-Moreno, M.R.; Mutturi, S.; Deprez, S.; Abt, T.D.; Bonini, B.M.; Liden, G.; Dumortier, F.; et al. Development of a D-xylose fermenting and inhibitor tolerant industrial Saccharomyces cerevisiae strain with high performance in lignocellulose hydrolysates using metabolic and evolutionary engineering. Biotechnol. Biofuels 2013, 6, 89. [Google Scholar] [CrossRef]
  97. Dhar, R.; Sägesser, R.; Weikert, C.; Yuan, J.; Wagner, A. Adaptation of Saccharomyces cerevisiae to saline stress through laboratory evolution. J. Evol. Biol. 2011, 24, 1135–1153. [Google Scholar] [CrossRef]
  98. Hua, Q.; Joyce, A.R.; Palsson, B.Ø.; Fong, S.S. Metabolic characterization of Escherichia coli strains adapted to growth on lactate. Appl. Environ. Microbiol. 2007, 73, 4639–4647. [Google Scholar] [CrossRef]
  99. Lee, D.-H.; Palsson, B.Ø. Adaptive evolution of Escherichia coli K-12 mg1655 during growth on a non-native carbon source, l-1,2-propanediol. Appl. Environ. Microbiol. 2010, 76, 4158–4168. [Google Scholar] [CrossRef]
  100. Agrawal, M.; Wang, Y.; Chen, R. Engineering efficient xylose metabolism into an acetic acid-tolerant Zymomonas mobilis strain by introducing adaptation-induced mutations. Biotechnol. Lett. 2012, 34, 1825–1832. [Google Scholar] [CrossRef] [PubMed]
  101. Sootsuwan, K.; Thanonkeo, P.; Keeratirakha, N.; Thanonkeo, S.; Jaisil, P.; Yamada, M. Sorbitol required for cell growth and ethanol production by Zymomonas mobilis under heat, ethanol, and osmotic stresses. Biotechnol. Biofuels 2013, 6, 180. [Google Scholar] [CrossRef]
  102. Zhang, M.; Eddy, C.; Deanda, K.; Finkelstein, M.; Picataggio, S. Metabolic engineering of a pentose metabolism pathway in ethanologenic Zymomonas mobilis. Science 1995, 267, 240–243. [Google Scholar] [CrossRef]
  103. Deanda, K.; Zhang, M.; Eddy, C.; Picataggio, S. Development of an arabinose-fermenting Zymomonas mobilis strain by metabolic pathway engineering. Appl. Environ. Microbiol. 1996, 62, 4465–4470. [Google Scholar] [CrossRef]
  104. Zhang, M.; Chou, Y.-C.; Picataggio, S.K.; Finkelstein, M. Single Zymomonas mobilis Strain for Xylose and Arabinose Fermentation. US Patent 5843760, 1 December 1998. [Google Scholar]
  105. Mohagheghi, A.; Evans, K.; Chou, Y.; Zhang, M. Cofermentation of glucose, xylose, and arabinose by genomic DNA-integrated xylose/arabinose fermenting strain of Zymomonas mobilis AX101. Appl. Biochem. Biotechnol. 2002, 98–100, 885–898. [Google Scholar] [CrossRef] [PubMed]
  106. He, M.X.; Wu, B.; Qin, H.; Ruan, Z.Y.; Tan, F.R.; Wang, J.L.; Shui, Z.X.; Dai, L.C.; Zhu, Q.L.; Pan, K.; et al. Zymomonas mobilis: A novel platform for future biorefineries. Biotechnol. Biofuels 2014, 7, 101. [Google Scholar] [CrossRef] [PubMed]
  107. Wang, H.H.; Isaacs, F.J.; Carr, P.A.; Sun, Z.Z.; Xu, G.; Forest, C.R.; Church, G.M. Programming cells by multiplex genome engineering and accelerated evolution. Nature 2009, 460, 894–898. [Google Scholar] [CrossRef] [PubMed]
  108. Cong, L.; Ran, F.A.; Cox, D.; Lin, S.; Barretto, R.; Habib, N.; Hsu, P.D.; Wu, X.; Jiang, W.; Marraffini, L.A.; et al. Multiplex genome engineering using CRISPR/Cas Systems. Science 2013, 339, 819–823. [Google Scholar] [CrossRef] [PubMed]
  109. Kolb, A. Genome engineering using site-specific recombinases. Cloning Stem Cells 2002, 4, 65–80. [Google Scholar] [CrossRef] [PubMed]
  110. Wirth, D.; Gama-Norton, L.; Riemer, P.; Sandhu, U.; Schucht, R.; Hauser, H. Road to precision: Recombinase-based targeting technologies for genome engineering. Curr. Opin. Biotechnol. 2007, 18, 411–419. [Google Scholar] [CrossRef]
  111. Zhang, Y.; Perry, K.; Vinci, V.; Powell, K.; Stemmer, W.; del Cardayré, S. Genome shuffling leads to rapid phenotypic improvement in bacteria. Nature 2002, 415, 644–646. [Google Scholar] [CrossRef] [PubMed]
  112. Carroll, D. Genome engineering with zinc-finger nucleases. Genetics 2011, 188, 773–782. [Google Scholar] [CrossRef]
  113. Becker, J.; Boles, E. A modified Saccharomyces cerevisiae strain that consumes L-arabinose and produces ethanol. Appl. Environ. Microbiol. 2003, 69, 4144–4150. [Google Scholar] [CrossRef]
  114. Sedlak, M.; Ho, N. Expression of E. coli araBAD operon encoding enzymes for metabolizing L-arabinose in Saccharomyces cerevisiae. Enzyme Microb. Technol. 2001, 28, 16–24. [Google Scholar] [CrossRef]
  115. Wiedemann, B.; Boles, E. Codon-optimized bacterial genes improve L-arabinose fermentation in recombinant Saccharomyces cerevisiae. Appl. Environ. Microbiol. 2008, 74, 2043–2050. [Google Scholar] [CrossRef]
  116. Wang, C.; Shen, Y.; Zhang, Y.; Suo, F.; Hou, J.; Bao, X. Improvement of L-arabinose fermentation by modifying the metabolic pathway and transport in Saccharomyces cerevisiae. Biomed. Res. Int. 2013, 2013, 1–9. [Google Scholar] [CrossRef]
  117. Richard, P.; Verho, R.; Putkonen, M.; Londesborough, J.; Penttila, M. Production of ethanol from L-arabinose by containing a fungal L-arabinose pathway. FEMS Yeast Res. 2003, 3, 185–189. [Google Scholar] [CrossRef] [PubMed]
  118. Bera, A.; Sedlak, M.; Khan, A.; Ho, N. Establishment of L-arabinose fermentation in glucose/xylose co-fermenting recombinant Saccharomyces cerevisiae 424A(LNH-ST) by genetic engineering. Appl. Microbiol. Biotechnol. 2010, 87, 1803–1811. [Google Scholar] [CrossRef] [PubMed]
  119. Wang, C.; Zhao, J.; Qiu, C.; Wang, S.; Shen, Y.; Du, B.; Ding, Y.; Bao, X. Co-utilization of D-glucose, D-xylose, and L-arabinose in Saccharomyces cerevisiae by co expressing the metabolic pathways and evolutionary engineering. BioMed. Res. Int. 2017, 2017, 1–8. [Google Scholar] [CrossRef]
  120. Verho, R.; Putkonen, M.; Londesborough, J.; Penttilä, M.; Richard, P. A novel NADH-linked L-xylulose reductase in the L-arabinose catabolic pathway of yeast. J. Biol. Chem. 2004, 279, 14746–14751. [Google Scholar] [CrossRef] [PubMed]
  121. Kim, S.; Park, Y.; Jin, Y.; Seo, J. Strain engineering of Saccharomyces cerevisiae for enhanced xylose metabolism. Biotechnol. Adv. 2013, 31, 851–861. [Google Scholar] [CrossRef]
  122. Jansen, M.L.A.; Bracher, J.M.; Papapetridis, I.; Verhoeven, M.D.; de Bruijn, H.; de Waal, P.P.; van Maris, A.J.A.; Klaassen, P.; Pronk, J.T. Saccharomyces cerevisiae strains for second-generation ethanol production: From academic exploration to industrial implementation. FEMS Yeast Res. 2017, 17, fox044. [Google Scholar] [CrossRef]
  123. Leandro, M.; Fonseca, C.; Gonasalves, P. Hexose and pentose transport in ascomycetous yeasts: An overview. FEMS Yeast Res. 2009, 9, 511–525. [Google Scholar] [CrossRef]
  124. Subtil, T.; Boles, E. Improving L-arabinose utilization of pentose fermenting Saccharomyces cerevisiae cells by heterologous expression of L-arabinose transporting sugar transporters. Biotechnol. Biofuels 2011, 4, 38. [Google Scholar] [CrossRef]
  125. Verhoeven, M.D.; Bracher, J.M.; Nijland, J.G.; Bouwknegt, J.; Daran, J.-M.G.; Driessen, A.J.M.; van Maris, A.J.A.; Pronk, J.T. Laboratory evolution of a glucose-phosphorylation-deficient, arabinose-fermenting S. cerevisiae strain reveals mutations in GAL2 that enable glucose-insensitive L-arabinose uptake. FEMS Yeast Res. 2018, 18, foy062. [Google Scholar] [CrossRef]
  126. Li, J.; Xu, J.; Cai, P.; Wang, B.; Ma, J.Y.; Benz, P.; Tian, C. Functional analysis of two L-Arabinose transporters from filamentous fungi reveals promising characteristics for improved pentose utilization in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 2015, 81, 4062–4070. [Google Scholar] [CrossRef]
  127. Fonseca, C.; Romão, R.; de Sousa, H.R.; Hahn-Hägerdal, B.; Spencer-Martins, I. L-Arabinose transport and catabolism in yeast. FEBS J. 2007, 274, 3589–3600. [Google Scholar] [CrossRef]
  128. Bettiga, M.; Bengtsson, O.; Hahn-Hägerdal, B.; Gorwa-Grauslund, M.F. Arabinose and xylose fermentation by recombinant Saccharomyces cerevisiae expressing a fungal pentose utilization pathway. Microb. Cell Factories 2009, 8, 40. [Google Scholar] [CrossRef] [PubMed]
  129. Madhavan, A.; Tamalampudi, S.; Srivastava, A.; Fukuda, H.; Bisaria, V.S.; Kondo, A. Alcoholic fermentation of xylose and mixed sugars using recombinant Saccharomyces cerevisiae engineered for xylose utilization. Appl. Microbiol. Biotechnol. 2009, 82, 1037–1047. [Google Scholar] [CrossRef]
  130. Hamacher, T.; Becker, J.; Gárdonyi, M.; Hahn-Hägerdal, B.; Boles, E. Characterization of the xylose-transporting properties of yeast hexose transporters and their influence on xylose utilization. Microbiology 2002, 148, 2783–2788. [Google Scholar] [CrossRef] [PubMed]
  131. Subtil, T.; Boles, E. Competition between pentoses and glucose during uptake and catabolism in recombinant Saccharomyces cerevisiae. Biotechnol. Biofuels 2012, 5, 14. [Google Scholar] [CrossRef]
  132. Ye, S.; Jeong, D.; Shon, J.C.; Liu, K.-H.; Kim, K.H.; Shin, M.; Kim, S.R. Deletion of PHO13 improves aerobic l-arabinose fermentation in engineered Saccharomyces cerevisiae. J. Ind. Microbiol. Biotechnol. 2019, 46, 1725–1731. [Google Scholar] [CrossRef] [PubMed]
  133. Lin, C.; Hsieh, P.; Mau, J.; Teng, D. Construction of an intergeneric fusion from Schizosaccharomyces pombe and Lentinula edodes for xylan degradation and polyol production. Enzyme Microb. Technol. 2005, 36, 107–117. [Google Scholar] [CrossRef]
  134. Kordowska-Wiater, M.; Kubik-Komar, A.; Targoński, Z. Optimization of arabitol production by karyoductant SP-K 7 of S. cerevisiae V30 and P. stipitis CCY 39501 using response surface methodology. Pol J Microbiol. 2012, 61, 291–297. [Google Scholar] [CrossRef]
  135. Akinterinwa, O.; Khankal, R.; Cirino, P. Metabolic engineering for bioproduction of sugar alcohols. Curr. Opin. Biotechnol. 2008, 19, 461–467. [Google Scholar] [CrossRef] [PubMed]
  136. Dien, B.S.; Hespell, R.B.; Wyckoff, H.A.; Bothast, R.J. Fermentation of hexose and pentose sugars using a novel ethanologenic Escherichia coli strain. Enzyme Microb. Technol. 1998, 23, 366–371. [Google Scholar] [CrossRef]
  137. Bothast, R.; Saha, B.; Flosenzier, A.; Ingram, L. Fermentation of L-arabinose, D-xylose and D-glucose by ethanologenic recombinant Klebsiella oxytoca strain P2. Biotechnol. Lett. 1994, 16, 401–406. [Google Scholar] [CrossRef]
  138. Xiong, X.; Wang, X.; Chen, S. Engineering of an L-arabinose metabolic pathway in Rhodococcus jostii RHA1 for biofuel production. J. Ind. Microbiol. Biotechnol. 2016, 43, 1017–1025. [Google Scholar] [CrossRef] [PubMed]
  139. Kawaguchi, H.; Sasaki, M.; Vertès, A.; Inui, M.; Yukawa, H. Identification and functional analysis of the gene cluster for L-arabinose utilization in Corynebacterium glutamicum. Appl. Environ. Microbiol. 2009, 75, 3419–3429. [Google Scholar] [CrossRef] [PubMed]
  140. Saha, B.; Sakakibara, Y.; Cotta, M. Production of D-arabitol by a newly isolated Zygosaccharomyces rouxii. J. Ind. Microbiol. Biotechnol. 2007, 34, 519–523. [Google Scholar] [CrossRef] [PubMed]
  141. Saha, B.; Bothast, R. Production of L -arabitol from L -arabinose by Candida entomaea and Pichia guilliermondii. Appl. Microbiol. Biotechnol. 1996, 45, 299–306. [Google Scholar] [CrossRef]
Processes 11 01516 g001 550
Figure 1. Production of value-added products from LCB-derived L-Ara.
Figure 1. Production of value-added products from LCB-derived L-Ara.
Processes 11 01516 g001
Processes 11 01516 g002 550
Figure 2. Native metabolic pathways for assimilation of L-Ara. ADP: Adenosine Diphosphate; ATP: Adenosine Triphosphate; L-ribulose-5-P: L-ribulose-5-Phosphate, D-xylose-5-P: D-xylose-5-Phosphate; NAD(P)H: Nicotinamide Adenine Dinucleotide Phosphate Hydrogen; NAD(P)+: Nicotinamide Adenine Dinucleotide Phosphate; NADH: Nicotinamide Adenine Dinucleotide Hydrogen; NAD: Nicotinamide Adenine Dinucleotide, KDA dehydratase: 2-Keto-3-Deoxy-l-Arabinonate; KDPG aldolase: 2-Keto-3-Deoxy-6-Phospho Gluconate aldolase; αKGSA dehydrogenase: αKeto Glutarate Semialdehyde Dehydrogenase; Fructose-6-P: Fructuose-6-Phosphate; GAP: Glyceraldehylde-3-Phosphate; CoaSH: Coenzyme A; Pi: inorganic phosphate; TCA: tricarboxylic acid.
Figure 2. Native metabolic pathways for assimilation of L-Ara. ADP: Adenosine Diphosphate; ATP: Adenosine Triphosphate; L-ribulose-5-P: L-ribulose-5-Phosphate, D-xylose-5-P: D-xylose-5-Phosphate; NAD(P)H: Nicotinamide Adenine Dinucleotide Phosphate Hydrogen; NAD(P)+: Nicotinamide Adenine Dinucleotide Phosphate; NADH: Nicotinamide Adenine Dinucleotide Hydrogen; NAD: Nicotinamide Adenine Dinucleotide, KDA dehydratase: 2-Keto-3-Deoxy-l-Arabinonate; KDPG aldolase: 2-Keto-3-Deoxy-6-Phospho Gluconate aldolase; αKGSA dehydrogenase: αKeto Glutarate Semialdehyde Dehydrogenase; Fructose-6-P: Fructuose-6-Phosphate; GAP: Glyceraldehylde-3-Phosphate; CoaSH: Coenzyme A; Pi: inorganic phosphate; TCA: tricarboxylic acid.
Processes 11 01516 g002
Processes 11 01516 g003 550
Figure 3. Schematic representation of L-Ara utilization pathway of Z. mobilis and its metabolic engineering strategies. XylA: Xylose isomerase; XylB: Xylulose-5-P kinase; AraA: Arabinose isomerase; AraB: Arabinose-5-P kinase; AraD: L-Arabinonate dehydratase; ED Pathway: Entner–Doudoroff pathway; Glyceraldehyde-3-P: Glyceraldehyde-3-Phosphate; Pdc: Pyruvate dehydrogenase complex; AdhA/B: Alcohol dehydrogenase genes; LdhA: Lactate dehydrogenase gene.
Figure 3. Schematic representation of L-Ara utilization pathway of Z. mobilis and its metabolic engineering strategies. XylA: Xylose isomerase; XylB: Xylulose-5-P kinase; AraA: Arabinose isomerase; AraB: Arabinose-5-P kinase; AraD: L-Arabinonate dehydratase; ED Pathway: Entner–Doudoroff pathway; Glyceraldehyde-3-P: Glyceraldehyde-3-Phosphate; Pdc: Pyruvate dehydrogenase complex; AdhA/B: Alcohol dehydrogenase genes; LdhA: Lactate dehydrogenase gene.
Processes 11 01516 g003
Processes 11 01516 g004 550
Figure 4. Construction of a recombinant S. cerevisiae strain for L-arabinose assimilation through metabolic engineering. gap: glyceraldehyde-3-phosphate promoter; araA: L-arabinose isomerase; araB: L-ribulokinase; araD: L-ribulose 5-phosphate 4-epimerase; Peno: enolase promoter; tktA: transketolase; talB: transaldolase; NAD(P)H: Nicotinamide Adenine Dinucleotide Phosphate Hydrogen; NAD(P)+: Nicotinamide Adenine Dinucleotide Phosphate; araA: arabinose isomerase; araB: arabinose-5-P kinase; araD: L-arabinonate dehydratase; AR: Aldose Reductase; ArDH; D-Arabitol Dehydrogenase; permease Gal2: permease Galactose2; RPE: Ribulose-5-Phosphate Epimerase; RPI: Ribulose-5-Phosphate Isomerase; TKL: Transketolase; TAL1: Transaldolase 1; GND: 6-phosphogluconate dehydrogenase; Glyceraldehyde-3-P: Glyceraldehyde-3-Phosphate; D-Ribose-5-P: D-Ribose-5-Phosphate; D-Ribulose-5-P: D-Ribulose-5-Phosphate; Fructose-6-P: Fructose-6-Phosphate; Erythrose-4-P: Erythrose-4-Phosphate; Pseudoheptulose-7-P: Pseudoheptulose-7-Phosphate; D-Xylulose-5-P: D-Xylulose-5-Phosphate; L-Ribulose-5-P: L-Ribulose-5-Phosphate.
Figure 4. Construction of a recombinant S. cerevisiae strain for L-arabinose assimilation through metabolic engineering. gap: glyceraldehyde-3-phosphate promoter; araA: L-arabinose isomerase; araB: L-ribulokinase; araD: L-ribulose 5-phosphate 4-epimerase; Peno: enolase promoter; tktA: transketolase; talB: transaldolase; NAD(P)H: Nicotinamide Adenine Dinucleotide Phosphate Hydrogen; NAD(P)+: Nicotinamide Adenine Dinucleotide Phosphate; araA: arabinose isomerase; araB: arabinose-5-P kinase; araD: L-arabinonate dehydratase; AR: Aldose Reductase; ArDH; D-Arabitol Dehydrogenase; permease Gal2: permease Galactose2; RPE: Ribulose-5-Phosphate Epimerase; RPI: Ribulose-5-Phosphate Isomerase; TKL: Transketolase; TAL1: Transaldolase 1; GND: 6-phosphogluconate dehydrogenase; Glyceraldehyde-3-P: Glyceraldehyde-3-Phosphate; D-Ribose-5-P: D-Ribose-5-Phosphate; D-Ribulose-5-P: D-Ribulose-5-Phosphate; Fructose-6-P: Fructose-6-Phosphate; Erythrose-4-P: Erythrose-4-Phosphate; Pseudoheptulose-7-P: Pseudoheptulose-7-Phosphate; D-Xylulose-5-P: D-Xylulose-5-Phosphate; L-Ribulose-5-P: L-Ribulose-5-Phosphate.
Processes 11 01516 g004
Table
Table 1. Value-added products and their corresponding yields.
Table 1. Value-added products and their corresponding yields.
ValueAdded ProductsYieldMicrobe‘C’ Source Reference
Organic acidsLactic Acid: 12.1 g/L
Fumaric Acid: 7.4 g/L
Acetic Acid: 4.5 g/L		Lactobacillus sakei WiKim31Kimchi cabbage waste[15]
Putrescine19 g/LClostridium glutamicum PUT21Glucose[16]
Amino acidsL-Lysine: 9.9 g/L
L-Ornithine: 25.8 g/L
L-Arginine: 8.4 g/L		C. glutamicum ARG1Glucose and L-Ara[6]
Table
Table 2. Different sources of L-Ara and its applications.
Table 2. Different sources of L-Ara and its applications.
FeedstockLignin (%)Hemicellulose (%)Cellulose (%)Pre-Treatment Method Used to Obtain L-AraApplicationsReferences
Sugarcane bagasse25–3219–24 32–43Acid hydrolysis resulted in 2.78 g/L of L-AraFood coatings, hydrogels, packaging films, cationic biopolymers, and other biomedical uses[32,33,34]
Corn stover192236Acid hydrolysis resulted in 38.2% L-Ara yield in 8 h reaction timeAdvanced biofuels and livestock feed[35,36,37]
Rice straw151835Combined pre-treatment methods resulted in 2.7–4.5% of L-ArayieldBiofuel and ethanol production[38,39,40]
Water hyacinth103525Sulphuric acid treatment resulted in 33.3 g/L yield of L-AraBiothanol production using Pichia stipitis[41,42]
Wheat straw16–2523–2428–39Hot water and NaOH treatment resulted in 2.37 ± 0.09% of L-AraAdsorbents, packing materials, bioplastic industry, and several other industries[43,44,45]
Sugar beet molasses63022–24Acid alkali pretreatment along with ultrafiltration resulted in 92% recovery of L-AraFood industry, as a bakery or confectionery product, apart from being utilized as a ruminant feed[46,47]
Apple pomace191012Sulphuric acid treatment resulted in 90% yield of L-AraBioethanol, animal feed, citric acid, and several other applications[48,49,50]
Orange peels20969Acid alkali treatment to extract L-AraBioethanol, essential oils, and biogas[51,52]
Carrot pomace17728Acid treatment to extract L-AraFertilizer, feed for livestock, dietary fiber, and production of biofuels[53,54]
Tomato pomace73138Acid treatment to extract L-AraFertilizer, feed for livestock, dietary fiber, and production of biofuels[54,55,56]
Table
Table 3. L-Arabitol from L-Ara metabolizing yeast, fusants, and recombinants.
Table 3. L-Arabitol from L-Ara metabolizing yeast, fusants, and recombinants.
Type of OrganismName of Organism/StrainProduct
Produced		Product Yield (g g−1) References
YeastDebaryomyces nepalensis NCYC 3413L-Arabitol0.48[140]
P. guilliermondii0.54[80]
C. entomeae0.77[141]
Intergeneric fusantS. pombe and
L. edodes hybrid		L-Arabitol0.80[133]
RecombinantS. cerevisiae AH22L-Arabitol0.62[114]
S. cerevisiae TMB 36640.48[128]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Jacob, S.; Dilshani, A.; Rishivanthi, S.; Khaitan, P.; Vamsidhar, A.; Rajeswari, G.; Kumar, V.; Rajak, R.C.; Din, M.F.M.; Zambare, V. Lignocellulose-Derived Arabinose for Energy and Chemicals Synthesis through Microbial Cell Factories: A Review. Processes 2023, 11, 1516. https://doi.org/10.3390/pr11051516

AMA Style

Jacob S, Dilshani A, Rishivanthi S, Khaitan P, Vamsidhar A, Rajeswari G, Kumar V, Rajak RC, Din MFM, Zambare V. Lignocellulose-Derived Arabinose for Energy and Chemicals Synthesis through Microbial Cell Factories: A Review. Processes. 2023; 11(5):1516. https://doi.org/10.3390/pr11051516

Chicago/Turabian Style

Jacob, Samuel, Aswin Dilshani, Srinivasan Rishivanthi, Pratham Khaitan, Adhinarayan Vamsidhar, Gunasekaran Rajeswari, Vinod Kumar, Rajiv Chandra Rajak, Mohd Fadhil Md. Din, and Vasudeo Zambare. 2023. "Lignocellulose-Derived Arabinose for Energy and Chemicals Synthesis through Microbial Cell Factories: A Review" Processes 11, no. 5: 1516. https://doi.org/10.3390/pr11051516

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop