Synergistic benefits from a lignin-first biorefinery of poplar via coupling acesulfamate ionic liquid followed by mild alkaline extraction

Bioresource Technology 303 (2020) 122888

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Synergistic benefits from a lignin-first biorefinery of poplar via coupling acesulfamate ionic liquid followed by mild alkaline extraction

T

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Jikun Xua,b, , Lin Daic, Yang Guia, Lan Yuana, Chuntao Zhanga, Yang Leid a

School of Chemistry and Chemical Engineering, Wuhan University of Science and Technology, Wuhan 430081, China School of Environmental Science & Engineering, Huazhong University of Science and Technology, Wuhan 430074, China c Tianjin Key Laboratory of Pulp and Paper, Tianjin University of Science and Technology, Tianjin 300457, China d Center for Energy Resources Engineering, Department of Chemistry, Technical University of Denmark, Lyngby 2800, Denmark b

G R A P H I C A L A B S T R A C T

A R T I C LE I N FO

A B S T R A C T

Keywords: Lignin-first biorefinery Ionic liquid Alkaline pretreatment Hemicellulose Enzymatic hydrolysis

A novel mind-set, termed lignin-first biorefinery, is bewitching to synchronously boost lignin output for entirely lignocellulosic utilization. A lignin-first fractionation, using a food-additive derived ionic liquid (1-ethyl-3-methylimidazolium acesulfamate, emimAce) and mild alkaline pretreatments, was formed for the purposely isolating poplar lignin, whilst delivering a cellulose-rich substrate that can be easily available for enzymatic digestion. The emimAce-driven lignin, alkali-soluble lignin and hemicellulose, and accessible cellulose were sequentially gained. We introduce a lignin-first approach to extract the amorphous fractions, destroy the robust architecture, and reform cellulose-I to II, thereby advancing the cellulose bioconversion from 15.4 to 90.5%. A harvest of 70.7% lignin, 52.1% hemicellulose, and 330.1 mg/g glucose was fulfilled from raw poplar. A structural ‘‘beginning-to-end’’ analysis of lignin inferred that emimAce ions are expected to interact with lignin β-arylether due to their aromatic character. It was reasonable to derive benefits from lignin-first technique that can substantially augment the domain of biorefinering.

1. Introduction Irritated by resource scarcity and environmental issues, a surge of key shift towards a closed-loop, bio-driven economics is on the horizon (Renders et al., 2019). This inevitable innovation will hinge on the deployment of renewable energy that are able to meet the requirements of humankind in a sustainable way. In this vein, a critical technique

should be drafted in the frame of lignocellulosic biorefining, thus offering an entrance to renewable chemicals, energy and materials. In reality, the effort associated with facile biorefining has been long-term hindered by certain factors, such as biomass recalcitrance, natural variation, versatile chemistry, process waste streams (Renders et al., 2019; Yang et al., 2019). As one of the most abundant renewable biopolymers, cellulose is already widely used in the fields of bioenergy and

⁎ Corresponding author at: School of Chemistry and Chemical Engineering, Wuhan University of Science and Technology, 947 Heping Avenue, Qingshan District, Wuhan 430081, China. E-mail address: [email protected] (J. Xu).

https://doi.org/10.1016/j.biortech.2020.122888 Received 10 December 2019; Received in revised form 20 January 2020; Accepted 21 January 2020 Available online 23 January 2020 0960-8524/ © 2020 Elsevier Ltd. All rights reserved.

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Fig. 1. Synthesis roadmap (a) of 1-ethyl-3-methylimidazolium acesulfamate (emimAce). The recovery yield and chemical compositions (b) of poplar wood. Control: raw poplar wood; ILP: emimAce-pretreated poplar wood; CRM: carbohydrate-rich poplar wood after emimAce and mild alkaline pretreatments.

sulfate (bmimHSO4) and 1-butyl-3-methylimidazolium chloride (bmimCl), in which about 17–57% of delignification was achieved (Sorn et al., 2019). Li et al. also declared the credible capacity of IL polyoxometalates for the scission of β-O-4′, α-O-4′, and 4-O-5′ bonds in three types of lignin models, as well as, for the efficient conversion of native lignocellulose (Li et al., 2019b). The facile dissolution and regeneration pathways usually come with highly efficient decrystallization of cellulose and fractionation of lignin, therefor, leading to a high grade of accessible pulp available for bioethanol precursor. To date, it is hard to retrieve lignin in its natural form, owing to the chemical alternation of its 3D network during the fractionation step. How to fully exert the selective ILs-induced fractionation is the linchpin of biomass chemistry that asserts a lignin-first biorefinery. For a targeted extraction of lignin, therefore, a good situation to fabricate a controllable IL with a desired set of features ignites the enthusiasm from the scientific views. Herein, we report on a synthesized IL (1-ethyl-3-methylimidazolium acesulfamate, emimAce) from a low-cost food-additive (acesulfamate potassium, Ace K) with the directed characteristic of an aromatic anion. This task-tailored manner of emimAce endows its ability to selectively separate and recover poplar lignin, while preserving the structural integrality and potential value of leftover cellulose. To the best of our knowledge, there was barely report for a coupled pretreatment of selfmade emimAce followed by mild alkaline extraction to pursue a ligninfirst deconstruction of poplar. A critical “beginning-to-end” analysis of lignin structure is conducive to provide a clue for the plausible mechanism of emimAce-drived lignin fractionation. In brief, we built a lignin-first protocol for the assistant of complete biomass valorization by the alliance between selective emimAce and mild alkaline extraction.

electronics (Dutta et al., 2017a). To impart desired energy specialty of cellulose, this is of great significance for the rational design of advanced pretreatments by exploring high-purity cellulose with the sacrifice of lignin. Meanwhile, a shrewd pretreatment step is indispensable to simultaneously satisfy the demand of biomass recalcitrance mitigation and whole lignocellulose valorization. An inherent drawback of classical biorefinery is to valorize the carbohydrate part of lignocellulose with lignin either released as a waste or burnt to generate power (Renders et al., 2017). Due to the nonproductive inhibition and physical block of enzymes by lignin, an ocean of pretreatments intend to remove lignin in-depth for largely improving the recovery of fermentable sugars. With respect to high-energy density fuels, lignin seems to be more attractive than cellulose and hemicellulose because of its high carbon content (60 vs 44 wt%), as well as, its reduced oxygen content (32 vs 49 wt%) (Cao et al., 2018). It is worth mentioning that lignin, as the third major part, reaches up to approximately 20–35 wt% of dry lignocellulose and 40% of its potential fuel value (Cao et al., 2018; Gazi, 2019). The above standpoints provide a powerful evidence of the prospective benefits available from a lignin-tofuels strategy. On this account, to boost the feasibility of bioenergy, much recent effort has been gradually put into utilizing efficiently all of three building blocks of lignocellulose including lignin that holds the great promise for the alternative source of renewable aromatics and drop-in fuels (Cao et al., 2018; Wu et al., 2018). Prior to the regulation of individual motif, the plant matrix should be fractionated into main branches via a valid strategy. During the past several years, one of the fascinating approaches laid at the core field of lignocellulosic fractionation is lignin-first approach. The lignin-first regime is the exploitation of lignin isolation that mainly focused on the preservation of lignin β-O4′ bonds by avoiding the consumption of carbohydrates (Den Bosch et al., 2017), offering an opportunity to utilize the whole lignocellulose in a more efficient-manner. The employment of particular solvents such as ammonia (Mittal et al., 2017; Sousa et al., 2016), ionic liquids (ILs) (Kim et al., 2017; Sathitsuksanoh et al., 2014) or γ-valerolactone (Luterbacher et al., 2015; Luterbacher et al., 2014) could satisfy the needs for partially extracting the quasi-crude lignin under a relatively moderate environment. Thereinto, ILs-driven pretreatment has emerged as one of the most efficient route, thanking to their unparalleled aspects, e.g. superior thermal stability, low volatility, modifiable ions, excellent biomass solubility, and etc. (Brandt et al., 2013). An environmentally benign procedure was proposed for the deconstruction of rice straw by using 1-butyl-3-methylimidazolium hydrogen

2. Materials and methods 2.1. Materials and reagents The directed synthesis of emimAce was relied on a one-pot reaction (Pinkert et al., 2011). The synthetic pathway (Fig. 1a) of emimAce and its 1H NMR spectrum are displayed. Triploid of Populus tomentosa Carr., a fast-growing poplar serving as the raw material of biomass, was reaped from a breeding base of Beijing, China. Leaves and barks were abandoned, then the dried stems were ground to sieve through a 40–60 mm mesh. All the chemical reagents used were of analytical grade or the best available. 2

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2.2. The lignin-first pretreatment and cellulose enzymatic hydrolysis

3.1. Characterization of lignin towards a lignin-first biorefinering

We briefly showed the sequential procedure of a lignin-first fractionation for poplar by using emimAce followed by mild alkaline extraction. Firstly, we immersed poplar wood of 5 g in 100 g of emimAce. The IL/poplar mixture was subsequently heated by a hot plate (IKA, Germany) with vigorous magnetic stirring at 110 °C for 4 h. The regeneration of the dissolved wood was carried out by pouring the mixed solution into about 1000 mL deionized water under vigorous stirring. Then, the resulting mixture was filtered under the reduced pressure to obtain the regenerated wood particles (ILP). The liquid fraction was concentrated and then poured into a beaker loaded with 30 mL of anhydrous acetone. Afterwards, the IL-extracted lignin (ILL) could be facilely precipitated and separated. To recycle emimAce, the residual acetone need to be distilled after the recovery of lignin. To extended isolation of lignin (AL) and hemicellulose (AH), the IL-emimAce pretreated poplar wood (ILP) was sequentially extracted with 1 mol/L aqueous NaOH with a solid-to-liquid ratio of 1:15 (g/mL) at 75 °C for 3 h. The leftover solid was of a carbohydrate-rich material (CRM) that will be used as the substrate for the subsequent enzymatic hydrolysis at the cellulase loading of 15 FPU/g.

To selectively isolate lignin with slight degradation of carbohydrate, the first entry point is to seek a moderate extraction using a purposive solvent that has no significant side-reaction with cellulose. It is worth pointing that this solvent need to be green, innoxious, noncorrosive, thermally stable, and recyclable. For the selective separation of poplar lignin, the design of IL-emimAce with an aromatic-like acesulfamate anion was formed with the assistance of following considerations: a) Ace K can be adopted as anion source for emimAce synthesis via a metathesis of anion, which is an industrial food-additive with the unique properties of low cost and nontoxic; b) the empirical point of view indicated that the poorly dissolving ability of cellulose was highly depended on the bulky anion of ILs with delocalized charge, for instance, Ace anion (Pinkert et al., 2011); and c) due to the aromatic character of emimAce ions, it is believed that lignin can be dissolved and/or extracted by emimAce under the guidance of parallel aromaticity. The reaction roadmap and 1H NMR (DMSO‑d6) pattern of emimAce are displayed. IL-emimAce can be readily synthesized from a low-cost food additive Ace K and imidazolium cation by one-pot displacement reaction (Fig. 1a). The 1H NMR spectrum of emimAce showed six classical types of chemical shifts stemming from imidazolium cation, such as 9.20 ppm (1H, H-a), 7.80 and 7.75 ppm (2H, H-b/H-b′), 4.20 ppm (2H, H-1), 3.90 ppm (3H, H-1′), 1.50 ppm (3H, H-2). The chemical shifts at 1.92 ppm (3H, H-3) and 5.30 ppm (1H, H-5) were located as the information of protons from Ace anion, confirming the successful coalescent of emimAce ions by replacing food-additive acesulfamate anion (Ace−). In addition, traces of residual water in the emimAce was proved by the location of 3.39 ppm. As compared with the common IL acetate, a greater thermal stability and viscosity of the as-prepared emimAce is due to the nature of the anion. The existence of tiny amounts of water might reduce the dynamic viscosity of emimAce, which always be profitable to the wood dissolution and also has a slight negative impact on the lignin extraction (Brandt et al., 2011; Pinkert et al., 2011). A recent report inferred that the appropriate addition of water into IL could improve the hydrolysis efficiency of lignin (Sun & Xue, 2018). Poplar lignin contains a large number of aromatic structures and hydroxyl groups. The hydroxyl groups also divide into aliphatic and phenolic hydroxyl groups. Non-covalent π–π interactions between the aromatic structures are the primary forces that hold lignin subunits together and contribute to the aggregation of lignin. Inspired by this natural intermolecular force in lignin, we designed and prepared a food additive-derived IL (emimAce) with aromatic anion for a specific fractionation of poplar lignin. To frame an IL-driven pretreatment resembling the deep lignin-first biorefinery, the virtues of a food-additive rooted emimAce can be summarized in this work: 1) it is crucial that the selective extraction of lignin was accomplished at the slight expense of cellulose (4.47%); 2) during the regeneration process, the facile recovery of lignin from emimAce was actualized by using acetone as the anti-solvent; 3) an obvious drop in CrI (34.7 vs 41.9%) was resulted from the cellulose transition under emimAce environment; 4) the robust recalcitrance of hardwood was easily tackled by the emimAce deconstruction; 5) the swelling and reconstitution of plant cell wall under the emimAce environment was conducive to the extended alkaline isolation of lignin. An important aspect for the lignin-first process is the extraction efficiency of wood lignin. A common 1-ethyl-3-methylimidazolium acetate (emimOAc) was also adopted to fractionate poplar, in which about 10.7% of lignin and 29.8% of hemicelluloses were co-dissolved in the emimOAc (Yuan et al., 2013). The unique aromatic character of emimAce anion was responsible for the relatively higher extraction of lignin and lower degradation of carbohydrates. For ILs pretreatment, the elimination of lignin was also reported to be between 17% and 65%, while hemicellulose removal varied between 0% and 83% (Brandt et al., 2013). Although ILs have been used extensively for lignocellulose deconstruction, it has been witnessed that the efficient isolation of

2.3. Analytic procedure The chemical composition of the raw and pretreated poplar was analyzed by using acid hydrolysis procedure. For poplar, the content of hemicelluloses (xylan) was calculated on the basis of xylose using 0.88 as anhydro corrections for xylose. The concentration of lignin was calculated on the sum of Klason and acid-soluble lignin. A high-performance anion exchange chromatography (HPAEC) system (Dionex ICS3000, US) was conducted to quantify the content of neutral sugars. An instrument of gel permeation chromatography (GPC) was applied to determine the molecular weights of lignin and hemicellulose. The indepth structure of lignin and hemicellulose was evaluated by an in-situ NMR technique on a Bruker AVIII 400 MHz spectrometer at 25 °C. An Xray diffractograms instrument (XRD-6000, Shimadzu, Japan) was worked to acquire the XRD pattern of powder samples. Scanning electron microscopy (SEM) was employed to detect the morphologic changes of the original and pretreated poplar. 3. Results and discussion The lignin-first standpoint offers an opportunity to obtain valuable lignin in the light of using the whole lignocellulose efficiently. A sequential fractionation allows each step to preserve the worth of lignin and hemicellulose as well as to generate an accessible cellulose at the end of process. Herein, we present a designed IL/emimAce-driven lignin-first approach for the deconstruction of poplar into individual building-blocks. The tentative idea of using emimAce was to selectively fractionate lignin without the expenditure of cellulose for creating partial pores and/or channels in the fiber cell walls, thus allowing the expedite penetration of alkali to cleave ester and/or lignin-carbohydrate complex (LCC). We proposed that the synthesized bmimAce purposely cleaves the β-O-4′ linkage of lignin by Ace anion attack. The lignin-first concept would become more viable if the carbohydrate part can survive after lignin extraction and can be incorporated into the available biorefinery system. Thus, the mild alkaline extraction offers a medium to extend the isolation of lignin and hemicellulose, thus preserving an easily accessible cellulose for enzymatic hydrolysis. The overall lignin-first fractionation led to the splitting of poplar into three main motifs as following: a) emimAce-extracted lignin (ILL); b) alkalisoluble lignin (AL) and hemicellulose (AH); c) an accessible cellulose substrate (CRM). The present work not only delivers a promising tool to precisely dissociate lignin, but also opens an avenue for the complete utilization of lignocellulose via the lignin-first regime under moderate environment. 3

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linkages (β-O-4′, A), resinol (β-β′, B), phenylcoumaran (β-5′, C), and minor structural units of Iγ (p-hydroxycinnamyl alcohol end groups), can be well separated from the side-chain region of lignin (Wang et al., 2019). The correlation for spirodienone structure Dα (δC/δH 59.5/ 2.86, Cβ-Hβ) and Dβ (δC/δH 60.1/2.76, Cβ-Hβ) was located in AL rather than ILL, inferring that the instability of spirodienone motif (D) and its cleavage in weak acid environment was induced by emimAce. Hallac et al. also reported a similar result by probing lignin evolution under an acidic enviroment (Hallac et al., 2010). However, the longterm existence of the correlations of β-5′ and β-β′ bonds in the spectra of ILL and AL was mainly due to the fact that the carbon-carbon bonding was relatively stable during the IL and mild alkaline stages. The signal of 65–68/3.5–3.8 ppm in ILL was triggered by the appearance of β-D-xylopyranoside unit, suggesting the depolymerization of xylan and its association with ILL. Furthermore, the cross-signals from syringyl (S), guaiacyl (G) and p-hydroxyphenyl (H) lignin units were sharply differentiated in the aromatic regions (Yang et al., 2016). From the HSQC spectra of ILL and AL, the common S-type lignin motifs exhibited an obvious C2,6–H2,6 correlation at δC/δH 104.2/6.70, whereas the C2,6–H2,6 signal of Cα-oxidized S units was located at δC/ δH 106.4/7.25. The different correlations of C2–H2, C5–H5, and C6–H6 for typical G units were presented at δC/δH 111.5/6.97, 114.8/ 6.73–6.91, and 119.5/6.74 ppm, respectively (Sun et al., 2019). It is reasonable to deduce that the two adjacent signals at C5 were triggered by the distinct substituents at C4 position. Note that the signal of phydroxybenzoate substructures (PB) was detected from AL while it disappeared in ILL, inferring that the ester alliance between lignin and PB was partially disrupted in emimAce. Also, the PB structure was still adhered to AL from the mild alkaline extraction. The 31P NMR, a precise and facile technique, is usually employed to quantify the major hydroxyl groups (–OH) that can be regarded as the important medium in lignin valorization (Eraghi Kazzaz et al., 2019). To follow the disparity of main hydroxyl groups, the classical 31P NMR spectra of phosphitylated ILL and AL as well as the content of hydroxyl groups in lignin are shown, respectively. Note that, the aliphatic –OH content of ILL (2.89 mmol/g) was relatively lower than that of AL (3.65 mmol/g), indicating the scission of the γ-methylol group as formaldehyde, the oxidation of Cα − OH groups to ketones, the exfoliation of whole side-chains to form β-1′ linkages, and the occurrence of dehydration in lignin side-chain during emimAce deconstruction (Dutta et al., 2017b). Since the absence of associated carbohydrates in AL, therefore, the aliphatic –OH of AL was mainly stemmed from the sidechain of lignin. By contrast, the phenolic –OH content of ILL (1.43 mmol/g) was slightly higher than that of AL (1.20 mmol/g), which was closely related to the selective dissociation of lignin by the aromatic character of emimAce anion. Generally, the partial cracking of

lignin from ILs is still a big hindrance to be faced. Note that, the dominate merit of emimAce can be defined as the facile recovery of lignin from IL and the negligible consumption of cellulose. About 37.56% and 33.11% of the total lignin was extracted by emimAce and mild alkali, respectively. Most of the lignin (˃70%) in the biomass was extracted by emimAce and subsequent alkaline process. It was found that the yield of ILL was slightly higher than that of AL, which was probably ascribed to the efficient disruption of the inter- and intramolecular hydrogen bonding, the selective cleavage of lignin β-O-4′ linkage, and the swelling of plant cell wall. During the mild alkaline extraction, this would give the chance for lignin to escape from compact plant matrix as well as for the acceleration of extended dissolution of lignin and hemicellulose. The content of the linked sugars was 1.27% for ILL and 0.76% for AL, indicating that the bonds between lignin and hemicellulose in the cell walls of poplar were evidently disrupted upon the alkaline environment. Of particular interest, the formation of cracks and holes on the surface of ILP was inspired by emimAce, indicating the liberation of accessible regions and active sites for the sake of improving lignin dissolution in mild alkaline extraction. The molecular weight (weight-average Mw and number-average Mn) and polydispersity (Mw/Mn) of ILL and AL are given. It can be concluded that the molecular weight of lignin was strongly affected by emimAce pretreatment, which was likely ascribed to the lignin dissociation initiated by the cleavage of its sensitive bonds. The occurrence of lignin depolymerization during IL pretreatment can also be affirmed by a lower Mw for ILL (2800 vs 3250 g/mol) together with the higher content of phenolic OH. The Mw of lignin is positively relied on its content of β-O4′ bonds that could be partially cleaved by emimAce. The previous reports also declared that emimOAc pretreatment led to the release of lignin subunits via depolymerization, thus reducing the molecular size and shape of lignin (Cheng et al., 2012; George et al., 2011). In addition, a relatively low polydispersity of all the lignin fractions (1.41 for ILL and 1.22 for AL) provided a good evidence for their relatively narrow molecular weight distributions. The gentle treatment conditions might serve as a factor for the low polydispersity of lignin, which be conducive to its extended use. The extracted lignin (ILL and AL) had a higher purity (˃90%) and a moderate molecular weight, which could be adapted to add value for lignin-first biorefinery. To gain the fine structure of lignin, the 2D HSQC NMR spectra of ILL and AL were also summarized in Fig. 2. We also presented the primary motifs of lignin. The assignment of 1H–13C cross-signals for the mainly basic structure is displayed. The location of inter-unit linking patterns can be found from the side-chain region (δC/δH 50–90/2.5–6.0), and the appearance of lignin aromatic regions (δC/δH 100–140/6.0–8.0) units with an excellent resolution can be easily recognized. The evident signals, e.g. methoxyls (–OCH3), the substructures of β-aryl ether

Fig. 2. 2D HSQC NMR spectra of lignin ILL (a/c) and AL (b/d) from the whole process. Side-chain (a-b) and aromatic regions (c-d) in the HSQC NMR spectrum, δC/δH 50–90/ 2.5–6.0 and δC/δH 100–140/6.0–8.0, respectively. ILL: ionic liquid (emimAce) isolated lignin; AL: alkali-soluble lignin. Main classical structures of lignin: (A) β-O-4′ linkages; (B) resinol structures formed by β-β′/ α-O-γ′/γ-O-α′ linkages; (C) phenylcoumarane structures formed by β-5′/α-O-4′ linkages; (D) spirodienone structures formed by β-1′ linkages; (I) p-hydroxycinnamyl alcohol end groups; (PB) p-hydroxybenzoate units; (S) syringyl unit; (S′) oxidized syringyl unit linked a carbonyl or carboxyl group at Cα (phenolic); (G) guaiacyl unit; (G′) oxidized guaiacyl units with a Cα ketone; (H) phydroxyphenyl units.

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β-O-4′ bonds would lead to the increase of phenolic –OH, whereas the dehydration reaction can be a blasting fuse to reduce aliphatic –OH (Wen et al., 2014). The ratio of total phenolic OH to aliphatic OH content of ILL (0.49) was relatively higher than that of AL (0.33), indicating a high degree of aryl ether dissociation, condensation and/or C–C coupling during the emimAce dissolution (Dutta et al., 2017b). However, the relatively stable and/or slightly decreased carboxyl (–COOH) in lignin (0.35 vs 0.37 mmol/g) under emimAce dissolution was observed, which was probably due to the naissance of weak oxidation. This phenomenon could shed substantial light on the preferential reactivity of dehydration rather than oxidation during the lignin fractionation by emimAce (Wen et al., 2014). As compared with AL, ILL exhibited a slight higher content of non-condensed G-OH (0.62 vs 0.49 mmol/g) and S-OH (0.52 vs 0.45 mmol/g), suggesting the obvious scission of β-O-4′ bonds under emimAce environment. A recent survey also reported that the preferential degradation of S-type lignin in both switchgrass and eucalyptus took place in ILs, which is ascribed to that the largely existence of β-O-4′ bonding in S-type lignin motifs (Varanasi et al., 2012). The methoxyl (–OCH3) content of AL was slightly higher than that of ILL (1.76/Ar vs 1.55/Ar), inferring that demethoxylation occurred in the processing of emimAce pretreatment. It was potentially deduced that the demethoxylation preferentially took place in G units as a consequence of a relatively higher S/G ratio of ILL from 2D-HSQC NMR. Even if the happening of demethoxylation reaction, the ignorable difference of non-condensed H-OH content between ILL and AL (0.14 vs 0.15 mmol/g) deduced that the basic structure of demethoxylation products from G-type lignin was incompletely analogous to that of common H units (Wen et al., 2014). It is witnessed that the association of free phenolic OH groups of lignin is crucial for its reactivity and antioxidant capacity, thereby leading to its potentials for the extended utilization, e.g. antioxidant reagents (Zhang et al., 2019), lignin filler (Dai et al., 2019), and adhesive (Bajwa et al., 2019). The exploration of lignin fractionation by ILs process is a promising direction for lignin-first biorefinery that also shed light on its large-scale. The degradation of lignin model compounds in acidic ILs was conducted in a recent research, inferring a catalytic manner for lignin depolymerization interacted with the IL anion (Cox et al., 2011). From a previous report, the IL pretreatment selectively degraded the G-type units of lignin under a relatively gentle environment (110 and 120 °C). However, an abnormal tendency was observed at a higher temperature (160 °C), that is, it is easier to peel off the S-type lignin than the G-type lignin (Varanasi et al., 2012). An analogous study has deduced that lignin could be selectively permeated into aqueous ILs, and the S-motif of lignin was believed to suffer preferential collapse under the environment of IL-water mixture (Sun and Xue, 2018). A mechanistic survey on the cleavage of β-O-4′ interunit bond, by immersing lignin model compounds into hydrogen sulfate-based acidic ILs, was carried out in depth, which proposed a pathway that initiates a dehydration reaction followed by generation of enol-ether and consequent hydrolysis to yield guaiacol and Hibbert ketones (De Gregorio et al., 2016). The depolymerization products of lignin are also found to be a function of the especially chemical nature of IL. Herein, the plausible mechanism of lignin structural changes during emimAce fractionation is depicted in Fig. 3a. In short, the following pathway could be tentatively involved with lignin extraction by emimAce: 1) the reactivity of lignin with emimAce due to the specifically aromatic nature of acesulfamate anion (Ace−) which presents a close analogy with the basic structure unit of lignin, whereas the poor capacity of emimAce for cellulose dissolution has been confirmed. The hydrogen donating ability of IL allows for a solvolytic cleavage of the interunit linkages in lignin, primarily the β-O4′ bonds. We propose the possibly selective cleavage of β-O-4′ aryl ether bond between phenylpropane subunits of lignin, allowing the impaction of the IL anion into the degradation product. The damage of aryl ether led to a decline size of lignin macromolecule in conjunction with the loss of G-typical lignin monomer and β-β′/β-5′ bonds (Sun et al., 2019); 2) it is reasonable to deduce that the demethoxylation reaction

was occurred preferentially in guaiacyl pattern. Moreover, the extent of lignin demethoxylation was relied on the nature of the anion (Hossain et al., 2019); 3) we introduce that the increased phenolic OH was roughly initiated through the disruption of β-O-4′ linkages, while the reduced aliphatic OH was potentially stemmed from the dehydration reaction. We attribute the biomass deconstruction and its synergistic benefits to the unique role of emimAce. It also should be noted that the selectively IL-induced lignin-first fractionation is a rapidly rising field in current biorefinery to meet the demands of waste-free standpoint. 3.2. Chemical composition, structure and enzymatic hydrolysis of poplar One of the compelling features of acesulfamate ILs is their capacity to obviously dissolve lignin under a gentle condition, owing to the aromatic identity of acesulfamate anion (Pinkert et al., 2011). Herein, it is requisite brought to light the impact of pretreatment on the change of poplar chemical compositions (Fig. 1b). As illustrated, the extraction of lignin was a primary phenomenon as a function of emimAce-aided fractionation, however, the synergistic output of lignin and hemicellulose was a direct proof for the occurrence of mass loss. The recovery yield of leftover poplar declined from 80.1% for ILP to 55.6% for CRM roughly due to the removal of main components. The content of lignin, cellulose and hemicellulose in raw poplar was 25.4, 43.1 and 18.2%, respectively. The content of lignin was decreased from 25.4 to 19.8% (ILP), which was ascribed to the selective dissociation of lignin aryl ether linkages by emimAce. The slight loss of xylan (17.8 vs 18.2%) during IL pretreatment was clearly referred to the weak ability of carbohydrate degradation for emimAce. Note that, only 4.47% cellulose was degraded into emimAce, also confirming the poor cellulose dissolving power of emimAce. The content of lignin and hemicellulose was further declined to 13.4 and 8.6% respectively, which potentially indicated that the alkali might disrupt the bonds between lignin and polysaccharides to a large extend, and/or between lignin and hydroxyl cinnamic acid, e.g. ferulic and p-coumaric acids (Martinez et al., 2016). The result also indicated that the increase of glucan content for ILP (51.4%) and CRM (65.6%), suggesting the weak depolymerization of cellulose during the global pretreatment. This phenomenon was also stemmed from the substantial elimination of lignin and hemicellulose during the overall lignin-first fractionation, which led to the relative enrichment of main cellulose portion. To pursue the renaissance of lignin-first fractionation, a great deal of effort has been aimed at the feasible technique for isolation and conversion of lignin and cellulose. Wherein, the facile recovery of hemicellulose can be integrated with the novel lignin-first biorefinery for boosting its overall economics. The alkali treatment acting on lignocellulose could snip the α-ether linkages between hemicellulose and lignin (Deepa et al., 2011), as well as, the swelling of plant cell wall can be initially promoted by ILs, thus leading to the substantial release of hemicellulose. To laterally determine the polymerization degree of hemicellulose, the Mw, Mn, and the polydispersity (Mw/Mn) of AH was also analyzed by GPC. The Mw of 54,000 g/mol and PI of 1.81 was observed for AH, inducing that the strong penetration capacity of emimAce could be of help to the swelling of the poplar cell wall. Hence, a high molecular weight of hemicellulose with relatively uniform structure (PI, 1.81) was delivered exactly into alkaline medium. Chemically heterogeneous hemicelluloses are consisted of pentose and hexose, therefore, the molecular structure and sugar composition of AH should be analyzed to facilitate the subsequent use. As shown, the immediate correlations between carbon and hydrogen of glycosyl motifs from hemicellulose can be identified by the characteristic overlapping resonances in the HSQC spectra. The appearance of (1 → 4)linked-β-D-xylopyranosyl (A) units was clearly detected from its location of C1–H1 (anomeric), C2–H2, C3–H3, C4–H4, C5–H5ax and C5–H5eq correlations at δC/δH 102.5/4.28, 73.2/3.16, 75.0/3.35, 76.1/3.65, 63.1/3.95 (axial proton), and 63.1/4.40 (equatorial proton), respectively (Li et al., 2018). The appearance of correlations at δC/δH 5

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Fig. 3. (a) Plausible integration of the acesulfamate anion of emimAce during cleavage of β-O-4′ linkages, elimination of methoxy group, and dehydration. (b) Cellulose enzymatic hydrolysis of triploid poplar. Poplar: raw poplar wood; ILP: IL (emimAce)-pretreated poplar wood; CRM: the carbohydrate-rich material via the integration of emimAce and mild alkaline extraction.

lignin and hemicellulose) was extremely conducive to the extended bioconversion of cellulose. To set up a bridge between physical morphology and enzymatic hydrolysis, SEM was always applied to view the exterior surface of lignocellulose. In a few words, the accessible area and porous structure of the treated poplar was promoted by the elimination of both lignin and hemicellulose, which made a positive effect on the cellulose bioconversion (Sorn et al., 2019). The virgin poplar wood presented an intact and flatness structure of virgate fiber, wherein cellulosic fiber is highly wrapped by hemicellulose and lignin. However, the continuously rodlike fiber of poplar was severely disrupted into oddments with irregular cracks and pores via the emimAce penetration and swelling of plant cell wall. After the two-stage pretreatment, the external and inner configurations were destroyed to a large extent. A rough surface and some agglomeration could still be observed at the edges of the fibers. This is usually triggered by lignin droplets that are formed by polymerization and relocation during the delignification process (Ferrini et al., 2016). The lignin-first biorefining aims to substantially augment the value of both lignin and cellulose. Efficiently enzymatic saccharification of cellulose into glucose is the first entry point required for cellulose valorization. The effect of lignin-first fractionation on the enzymatic digestion of poplar is plotted in Fig. 3b. The carbohydrate pulp derived from the lignin-first process is a suitable substrate for enzymatic hydrolysis because of the favorable delignification and high hexose retention. The positive effect of lignin-first fractionation via the combination of emimAce and mild alkali on improving the glucose yield of poplar. The released sugar can also be upgraded by known biological and chemical catalytic process that have been developed independently for pure carbohydrates (Huber et al., 2005; Parsell et al., 2015). For enzymatic hydrolysis of raw poplar cellulose, a ratio as low as 15.4%. This is mainly triggered by the synergistic action of the non-productive binding of lignin as well as the presence of xylan coating in the cell wall, which resulted in a serious impediment to bioconversion (Jin et al., 2019; Liu et al., 2017). By contrast, the cellulose digestibility of ILP and CRM were sharply enhanced to 70.8 and 90.5% respectively, which are 4.6- and 5.9-fold higher than that of original poplar. Enabled by the demolishment of lignin and hemicelluloses, the enzymatic efficiency of poplar reached up to 50.4% after alkaline pretreatment alone. For the IL pretreated sample, the digestibility of ILP was apparently higher than that of alkali pretreated poplar (70.8 vs 50.4%), which was mainly due to the expansion of cellulose I lattice and fibrous surface area. The results suggested that the global lignin-first process led to the alternation of cellulose crystal, removal of xylan and lignin, and morphological disruption, which formed a cooperative mechanism for sharply promoting the cellulose digestibility.

59.5/3.31 (–OCH3), 97.2/5.12 (C1–H1), 71.8/3.36 (C2–H2), 82.5/3.05 (C4–H4), and 72.1/4.12 (C5–H5) was an initiate of 4-O-methyl-α-glucuronic acid units (C, 4-OMe-α-D-GlcpA). Hence, the presence of branched β-D-Xylp units (B) was highly announced by the location of δC/δH 100.1/4.46 (C1–H1), 76.5/3.25 (C2–H2), and 72.1/3.57 (C3–H3), owing to the launch of linked side-chain (C, 4-OMe-α-DGlcpA) (Li et al., 2018). In addition, the signals of (1 → 4)-linked-β-Dglucopyranose (G) from low molecular-weight glucan can be determined by their correlations of C1–H1 (δC/δH 102.8/4.25, anomeric) and C6–H6 (δC/δH 61.1/3.65), suggesting the slight degradation of cellulose during emimAce penetration and alkaline extraction (Yuan et al., 2013). This phenomenon can also be confirmed by the result of chemical composition, which directly indicated that about 10.9% of cellulose was degraded into aqueous NaOH. Xylose was the dominant monosaccharide of hemicellulose, taking up to 72.38%. The content of glucose was 20.19% corresponding to be the secondary major sugar. Besides, small amounts of glucuronic acid (4.52%), galactose (1.23%), rhamnose (0.94%) and arabinose (0.74%) were detected. In short, a linear backbone of (1 → 4)-linked-β-D-xylopyranosyl residues decorated with the branch at O-2 of 4-O-methyl-α-glucuronic acid motif can be deduced as the main framework of alkali-soluble hemicellulose (AH). It is commonly known that cellulose generally comprises crystalline and amorphous regions. The strong hydrogen linking force within crystalline domain of cellulose makes it more recalcitrant to enzymatic saccharification than the amorphous region (Li et al., 2019a). XRD profile of lignocellulose delivers an excellent instruction of crystalline status, such as intact, distorted, swollen, of cellulose upon lignin-first fractionation (Yang et al., 2019). The XRD patterns and crystalline index (CrI) of poplar wood are provided. The crystalline structure of original poplar cellulose can be classified as cellulose I crystal type in virtue of the peaks at around 16° (110 planes) and 22° (200 planes) (Sharma et al., 2019). Note that, an obvious drop in CrI (34.7 vs 41.9%) was resulted from the initial emimAce environment via the disruption of hydrogen and/or hydroxyl bonds as well as the embedding of IL ions. It can be authenticated by the migration of diffraction angle from 22 to 20° as well as the loss of resolution at 16.0° for proving the transition of cellulose I to II (Xu et al., 2017). During emimAce treatment, the alternation of cellulose led to the exposure of accessible cellulose and random orientation of the crystallites, which are favorable for improving the efficiency of enzymatic conversion. An obvious increase in CrI of 45.3% was resulted from the single alkali-pretreated poplar that exhibited typical diffraction patterns of cellulose I. Moreover, the CrI of CRM (39.8%) was higher than that of ILP (34.7%), involving the removal of amorphous components in terms of partial lignin and hemicellulose. Except for the alternation of cellulose crystals, the CrI of cellulose generally exhibits a positive correlation with the degree of delignification (Parsell et al., 2015). In brief, the damage of cellulose crystallites and/or the elimination of mainly amorphous elements (i.e., 6

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pretreatment that harvested a majority of 71% lignin, evolved cellulose crystallinity, and destroyed poplar structure.

3.3. Process overall mass balance The lignin-first fractionation delivers an efficient chance to pursue the entire utilization of lignocellulose with the focus of lignin. The precise determination of process streams of three building blocks is extremely imperative to boost the feasibility of lignin-first biorefiney. The process mass balance of the emimAce and mild alkali pretreatments, and enzymatic digestion was assessed. The yield of leftover poplar was decreased from 100 to 80.1 g after IL pretreatment, in which a portion of poplar lignin (9.54 g, delignification of 37.56%) as well as a small quantity of xylan (3.94 g, 21.65%) and glucan (1.93 g, 4.47%) were dissolved into emimAce. For 100 g of original poplar, the content of cellulose and hemicellulose was 43.1 and 18.2 g, respectively. After IL-emimAce process, a portion of amorphous lignin and hemicellulose was degraded into emimAce, whereas the residue (ILP) preserved the amount of carbohydrates with 41.17 g of cellulose and 14.26 g of hemicellulose. It is foresaw that the depolymerization of lignin outpaced carbohydrates under a synthetically selective emimAce environment. Mild alkali-directed lignin removal was carried out with 33.11% delignification (removal of 8.41 g), in which led to a leftover solid (CRM) remaining 36.47 g cellulose, 4.78 g hemcielluloses and 7.45 g lignin. It should be emphasizing that the elimination of hemicellulose (52.09%) was higher than that of lignin (33.11%) under mild alkaline environment, implying that the removal ability of hemicellulose could outstrip that of lignin. This is ascribed to the pleasurable capacity of alkali for the cleavage of glucosidic and ester bonds (Farhat et al., 2017), which ultimately led to an obvious xylan removal and its recovery. These substances were stably preserved in the residue (CRM) that subsequently hydrolyzed by cellulose enzymes. Notably, we can successfully extract 70.67% (w/w) of lignin (total yield of 17.95 g) that has the latent capacity for the candidate of aromatics and biopolymers. Additionally, about 9.48 g of hemicellulose (AH) was isolated from mild alkaline process that can be used for platform chemicals. The overall lignin-first biorefinering ultimately delivered a yield of glucose as high as 33.01 g. In particular, the synergistic benefits of lignin and hemicellulose fractionation provided opportunities for more efficient downstream conversion. The benefits of outputting the lignin and xylan as well as enhancing cellulose enzymatic hydrolysis are responsible for the synergistic performance of lignin-first biorefinery. The valorization of lignocellulose in a direct fashion using the catalytic amount of Brønsted acidic ILs was reported to weigh against the high-cost of ILs, which was the economic detriment for the large-scale application (Matsagar & Dhepe, 2017). Herein, this drawback of ILs for biomass pretreatment can be obviously ameliorated via the effective recycle of emimAce. On the other hand, the highlight of emimAce was the efficient recovery of lignin, which could also substantially break the tradeoff between lignin fractionation and IL price. This logical placement of appropriate emimAce enables lignin valorization without the need for any additional bias or sacrificial agent and allows the protection of cellulose. The current research delivers a lignin-first fractionation with the aid of selective emimAce to pave the avenue for the improvement of cellulose digestibility as well as the output of lignin and xylan. The structure of lignin might also be tailored for downstream products, which be beneficial to the scale-up of lignin-first technique.

CRediT authorship contribution statement Jikun Xu: Conceptualization, Methodology, Validation, Investigation, Writing - original draft, Funding acquisition. Lin Dai: Formal analysis, Project administration. Yang Gui: Writing - review & editing. Lan Yuan: Writing - review & editing. Chuntao Zhang: Resources. Yang Lei: Resources. Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgements The authors would like to express their gratitude for the financial support from the National Natural Science Foundation of China (31700511) and the Project funded by China Postdoctoral Science Foundation (2018T110770). Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.biortech.2020.122888. References Bajwa, D.S., Pourhashem, G., Ullah, A.H., Bajwa, S.G., 2019. A concise review of current lignin production, applications, products and their environmental impact. Ind. Crops Prod. 139, 111526. Brandt, A., Gräsvik, J., Hallett, J.P., Welton, T., 2013. Deconstruction of lignocellulosic biomass with ionic liquids. Green Chem. 15 (3), 550–583. Brandt, A., Ray, M.J., To, T.Q., Leak, D.J., Murphy, R.J., Welton, T., 2011. Ionic liquid pretreatment of lignocellulosic biomass with ionic liquid–water mixtures. Green Chem. 13 (9), 2489–2499. Cao, Z., Dierks, M., Clough, M.T., Daltro de Castro, I.B., Rinaldi, R., 2018. A convergent approach for a deep converting lignin-first biorefinery rendering high-energy-density drop-in fuels. Joule 2 (6), 1118–1133. Cheng, G., Kent, M.S., He, L., Varanasi, P., Dibble, D.C., Arora, R., Deng, K., Hong, K., Melnichenko, Y.B., Simmons, B.A., 2012. Effect of ionic liquid treatment on the structures of lignins in solutions: molecular subunits released from lignin. Langmuir 28 (32), 11850–11857. Cox, B.J., Jia, S., Zhang, Z.C., Ekerdt, J.G., 2011. Catalytic degradation of lignin model compounds in acidic imidazolium based ionic liquids: hammett acidity and anion effects. Polym. Degrad. Stab. 96 (4), 426–431. Dai, L., Cao, Q., Wang, K., Han, S., Si, C., Liu, D., Liu, Y., 2019. High efficient recovery of L-lactide with lignin-based filler by thermal degradation. Ind. Crops Prod., 111954. De Gregorio, G.F., Weber, C.C., Gräsvik, J., Welton, T., Brandt, A., Hallett, J.P., 2016. Mechanistic insights into lignin depolymerisation in acidic ionic liquids. Green Chem. 18 (20), 5456–5465. Deepa, B., Abraham, E., Cherian, B.M., Bismarck, A., Blaker, J.J., Pothan, L.A., Leao, A.L., de Souza, S.F., Kottaisamy, M., 2011. Structure, morphology and thermal characteristics of banana nano fibers obtained by steam explosion. Bioresour. Technol. 102 (2), 1988–1997. Den Bosch, S.V., Renders, T., Kennis, S., Koelewijn, S., Den Bossche, G.V., Vangeel, T., Deneyer, A., Depuydt, D., Courtin, C.M., Thevelein, J.M., 2017. Integrating lignin valorization and bio-ethanol production: on the role of Ni-Al2O3 catalyst pellets during lignin-first fractionation. Green Chem. 19 (14), 3313–3326. Dutta, S., Kim, J., Ide, Y., Ho Kim, J., Hossain, M.S.A., Bando, Y., Yamauchi, Y., Wu, K.C.W., 2017a. 3D network of cellulose-based energy storage devices and related emerging applications. Mater. Horiz. 4 (4), 522–545. Dutta, T., Isern, N.G., Sun, J., Wang, E., Hull, S., Cort, J.R., Simmons, B.A., Singh, S., 2017b. Survey of lignin-structure changes and depolymerization during ionic liquid pretreatment. ACS Sustainable Chem. Eng. 5 (11), 10116–10127. Eraghi Kazzaz, A., Hosseinpour Feizi, Z., Fatehi, P., 2019. Grafting strategies for hydroxy groups of lignin for producing materials. Green Chem. 21 (21), 5714–5752. Farhat, W., Venditti, R.A., Quick, A., Taha, M., Mignard, N., Becquart, F., Ayoub, A., 2017. Hemicellulose extraction and characterization for applications in paper coatings and adhesives. Ind. Crops Prod. 107, 370–377. Ferrini, P., Rezende, C.A., Rinaldi, R., 2016. Catalytic upstream biorefining through hydrogen transfer reactions: understanding the process from the pulp perspective. ChemSusChem 9 (22), 3171–3180.

4. Conclusion IL-mediated lignin-first fractionation of lignocellulose is a burgeoning biorefinery that integrates lignin retrieve with entire lignocellulose utilization. An emimAce-aided two-stage poplar pretreatment was efficiently constructed to advance the lignin-first concept. An initial food-additive emimAce led to the selective separation of 37.56% lignin with a slight cellulose loss as a result of the uniquely aromatic nature of acesulfamate anion, meanwhile, a second step of mild alkaline extraction was applied to further collect lignin and xylan. A cellulose digestibility of 90.5% was realized after the overall lignin-first 7

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