Abstract
With the depletion of crude oil reserves, the ever-increasing global energy consumption encourages the efforts to find alternative renewable sources for production of biofuels and value-added chemicals. The conversions of lignocellulosic biomass into biofuels and commodity chemicals via the biotechnological pathway have been the recent trend. Specifically, these products can be obtained through fermentation of reducing sugars, which are the main but basic derivatives from the biomass. In order to overcome the recalcitrant structure of the biomass for effective reducing sugar recovery, a pretreatment stage is normally required. Currently, one of the most novel forms of biomass pretreatment is using energy irradiation methods such as electron beam, gamma ray, pulsed electrical field, microwave and ultrasound. In general, these technologies are often used together with other more conventional chemical and/or biological pretreatment techniques for enhancing sugar recovery. Nevertheless, energy irradiation offers significant improvement in terms of possible cost reduction opportunities and reduced toxicity. Hence, this review highlights the recent studies of using energy irradiation for pretreating biomass as well as the industrial applications of reducing sugars in biotechnological, chemical and fuel sectors. In short, more research needs to be done at the scientific, engineering and economic levels to make energy irradiation one of the front runners in the field of biomass pretreatment.
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Introduction
Lignocellulosic biomass is one of the most abundant bioresources in the world. According to the Union of Concerned Scientists (2012), in the US alone, the production rate of biomass was projected to reach nearly 680 million tons per year by 2030. In order to overcome the recalcitrance and alter the structural hindrance of biomass for effective digestibility and component utilization, a pretreatment stage is often required. Basically, the stage of biomass pretreatment is considered to be the most expensive stage within a biorefining facility, taking up to 20–48 % of the total operational cost (Ofori-Boateng and Lee 2014a). Mechanical communition techniques such as chipping, milling and grinding have been used to increase the surface area of biomass to render it more amenable to enzymatic hydrolysis (Chen et al. 2012b; Zheng et al. 2009). However, these typical techniques are also energy intensive and time consuming, making the process uneconomic and seldom used as an exclusive pretreatment method (Kim et al. 2011; Zheng et al. 2009). As such, both constraints of excessive energy consumption and low effectiveness prevent the application of most mechanical pretreatment systems to be used widely in industries (Bak et al. 2009). Only conventional chemical and biological pretreatments have been effectively applied at reasonable cost. On the other hand, some of the more novel energy irradiation methods not only require less energy, but they are also known to limit the production of inhibitors during the pretreatment process (Kim et al. 2011). Recently, advanced technologies such as gamma ray (Hong et al. 2014), electron beam (Karthika et al. 2012; Sundar et al. 2014), pulsed electrical field (Zbinden et al. 2013), microwave (Darji et al. 2015; Karunanithy et al. 2014) and ultrasound (Ninomiya et al. 2013; Rehman et al. 2014) have been gaining attention because of their fast and effective results in pretreatment of lignocellulosic biomass. Thus, this review re-evaluates the uses of reducing sugars obtained from the biomass and, most importantly, provides an overview on the recent use of high-intensity energy irradiation as a form of biomass pretreatment technique.
Current and future trends of biomass valorization
High energy demand around the globe has exerted excessive stress over the usage of depleting non-renewable resources such as fossil fuels and various minerals. Due to its renewable nature and abundant availability, the utilization of lignocellulosic biomass could be a potential sustainable solution to the aforementioned issue. The conversion of biomass into various value-added biochemicals is generally termed as biomass valorization (Iqbal et al. 2013). Over the past decades, active research is ongoing in exploring innovative and effective processes to improve the present bioconversion processes.
Complete transformation of biomass into value-added products can be divided into two stages, consisting of pretreatment of biomass, followed by either thermochemical (liquefaction, combustion, gasification, pyrolysis and torrefaction) or biological processing (fermentation) of biomass. The pretreatment of biomass is particularly vital in the biomass valorization process as it serves to break down the resistance of biomass because of the presence of hemicellulose (20–40 %), lignin (20-30 %) and extractives in large quantities, which serve as a protective layer (Lam et al. 2015). By applying an appropriate pretreatment stage, a more energy-efficient and simpler downstream process can be ensured. The type of biomass pretreatments can be further broken down into three major approaches, which are biological, chemical and physical/mechanical pretreatments (Loow et al. 2015).
The history of the pretreatment process for biomass valorization began with acid hydrolysis and steam explosion, which were developed in the 1920s (Kurian et al. 2013). As a practice to improve the existing method, different solvents and chemicals have since been developed and deployed as catalysts for the pretreatment process. Until now, various pretreatment techniques such as supercritical water treatment, alkaline hydrolysis, ozonolysis, densification and fungal digestion have been explored (Lam et al. 2015). Recently, the advances in energy irradiation have given a new impetus to the exhaustive research in this area, with methods such as electron beam, gamma ray, ultrasound, pulsed electrical field and microwave garnering attention across the research field. According to Grewell and Montalbo-Lomboy (2013), energy irradiation improved mass transport by enhancing mixing and improving the surface area for greater reaction sites. As the benefits associated with energy irradiation in the pretreatment process are significant, one of the future trends in biomass valorizations may involve the integration between energy irradiation and more conventional pretreatment methods for improving reducing sugar recovery from the lignocellulosic biomass.
Applications of reducing sugars
Any sugar that acts as a reducing agent because of the presence of free aldehyde or ketone groups can be defined as a reducing sugar. The diverse applications of reducing sugars in various industries have encouraged innovations in extracting the simplest form of sugar carbohydrates such as glucose, xylose and arabinose from the lignocellulosic biomass. Some of the major derivatives of reducing sugars as well as their applications in the industry are shown in Table 1. Therefore, the wide applications of reducing sugars for industrial purposes warrant the continuous development of more efficient and sustainable biomass pretreatment technologies.
Energy irradiation pretreatment of lignocellulosic biomass
Electron beam
Electron beam (EB) is a multi-stage process that is widely applied for polymer degradation and modification in which the pretreatment effects are caused by irradiation alone via minimization of temperature effects at high doses (Gryczka et al. 2014). As compared to gamma rays, EB is usually used at higher dosages but offers very limited penetration into materials whereby the high energy electrons are deposited in relatively thin layers of material (Duarte et al. 2012). This ionizing radiation technique has been successfully applied in the treatment of industrial effluents because the species produced from the radiation and water reaction (OH radicals, e-aq and H) were able to remove organic pollutants (Duarte et al. 2012). In the field of biomass pretreatment, EB was effective in removing the hemicellulose and lignin content, as these components retained a greater chance to be hit by the beam (Bak et al. 2009). This mode of pretreatment focused on the changes in internal structure of the substrates through the action of chain scission due to electron bombardment (Bak 2014; Shin and Sung 2008).
Generally, the dosage of EB radiation plays a significant role in pretreatment efficiency. Radiation-induced chain scission of the glucoside bond by β-cleavage of radicals was found to be proportional to the irradiation dose (Shin and Sung 2008). It is worth highlighting that the lower dosage was insufficient for effective breakage of bonds, but excessive dosage might lead to the decrease in glucose recovery since the glucose monomer was further decomposed by the excess energy (Kim et al. 2011; Xin and Kumakura 1993). For instance, Gryczka et al. (2014) reported that radiation effects were visible at 25 kGy, but severe destruction of the surface structure and breakage of cell walls was more apparent at 300 kGy as shown in Fig. 1. Using the same enzymatic hydrolysis duration, 450 kGy of radiation imposed a more profound effect on glucose yield than 150 kGy, with an increase in sugar recovery of 6.2 and 3.4 %, respectively, over the control (Shin and Sung 2008). The partial tearing that occurred at the fibers and cell walls caused the increase of the total wall area, whereas the pores progressively expanded and agglomerated into larger structures during the pretreatment process (Gryczka et al. 2014). The performance of EB-assisted sugar recoveries from various lignocellulosic biomasses is summarized in Table 2.
The ionizing radiation from EB had the capability of altering the lignocellulose structure within a short exposure time (Karthika et al. 2013). Besides, the pretreatment also increased the crystallinity index (CrI) because of the transformation of the intermediate para-crystalline phase of cellulose polymer between the diverse forms of crystalline and amorphous cellulose (Karthika et al. 2013). Bak et al. (2009) increased the intensity of the crystalline region from 54.5 to 58.0 % when EB was radiated at 80 kGy, attributed to the removal of hemicellulose and lignin amorphous regions. Kim et al. (2011) concurred with the result that the increase in beam dosage promoted the crystalline surface modification of biomass into the rugged surface, resulting in an increase of CrI. However, Karthika et al. (2012) and Sundar et al. (2014) observed contradictory results in which the CrI decreased along with the molecular weight, but the surface area was increased. The longitudinal fibers and vessels of the wood external layer were partially destroyed (Gryczka et al. 2014), coupled with the formation of degraded cracks and non-spherical protrusions (Bak 2014) after undergoing EB radiation. Hence, the reduction in the degree of polymerization (Shin and Sung 2008; Sung and Shin 2011) and disruption of the recalcitrant structure facilitated the reagents' accessibility as well as enzymatic saccharification (Karthika et al. 2013; Sundar et al. 2014). For instance, Sundar et al. (2014) successfully increased the overall glucose recovery by approximately fourfold when EB was applied before enzymatic hydrolysis.
Using mild radiation doses, the content of hemicellulose showed a decreasing trend with increases in dosage from 0 to 150 kGy, even though cellulose and lignin were not affected (Karthika et al. 2013). The loss of hemicellulose implied that it has been partially depolymerized and cleaved from its linkages with cellulose and lignin, rendering it easier to be solubilized (Sundar et al. 2014). Interestingly, the pretreatment effects were more pronounced when EB was integrated with other conventional methods. For instance, Karthika et al. (2013) reported that the cellulose was more sensitive to radiation with an addition of mild acid (1 % of H2SO4) or alkali (1 % of NaOH). Also, rice straw showed a remarkable improvement of glucose recovery after combining EB irradiation and 4 % of NaOH, with approximately 200 % higher yield than the pretreatment process consisting of alkali soaking alone (Xin and Kumakura 1993). On the other hand, Chosdu et al. (1993) improved the glucose yield of corn stalk from 20 to 43 % by incorporating both 500 kGy of EB and 2 % of NaOH. As such, the modification in structural state and mechanical strength promoted biomass hydrolysis. Nevertheless, a huge variation was observed for the sugar extraction because of the cleavage of macromolecules into soluble fractions, as well as the possible formation of intermolecular bonds (Karthika et al. 2013). Thus, high doses of EB have been reported to cause both polymerization and depolymerization in macromolecules (Karthika et al. 2013).
Gamma ray
The gamma ray (γ-ray) mechanism involves the generation of phenoxy radical intermediates, offering an efficient way to permit access of enzymes to cellulose (Chung et al. 2012). In the presence of water, γ-ray irradiation promoted the degradation of polysaccharides via breakage of glycosidic bonds in the biomass (Orozco et al. 2012; Yoon et al. 2012). High activity radicals were produced through the rapid delocalization of the absorbed energy within the molecules of cellulosic materials. Chemical reactions such as chain scission caused secondary degradation of these materials (Yoon et al. 2012) by breaking down the crystalline cellulose regions and modifying the lignin structure (Hong et al. 2014). Thus, the generation of phenoxy radicals via ionizing radiation, which are important radical intermediates in lignin formation, would subsequently transform into lignin O-quinonoid structures (Chunping et al. 2008). This structure might enable enzymes to access the biomass more easily. Orozco et al. (2012) argued that γ-rays degraded lignocellulose components via three mechanisms, namely (1) weakening of van der Waals force, (2) production of free radicals through cleavage of hydrogen bonds and (3) hydrolysis of glycoside bonds. Consequently, cell wall degradation was assisted by the weakening of cell wall constituents, as well as fiber depolymerization and delignification (Yoon et al. 2012). Even after the termination of radiation, some of the radicals that were trapped in crystalline and semi-crystalline regions of the cellulose could decay over time to cause further biomass degradation (Hong et al. 2014).
Surface morphology studies indicated that the even and smooth surface of wheat straw became rugged with a broken structure after undergoing γ-ray radiation. In fact, the effect was further enhanced when γ-ray radiation was combined with dilute acid pretreatment in which the surface appeared to be severely damaged with leaf split up to many pieces as shown in Fig. 2 (Hong et al. 2014). Wang et al. (2012) also observed a similar change in lignocellulosic structure after undergoing γ-ray radiation, as the rough surface indicated destructuralization of fibers and hence an increase in cellulose reactive area. Furthermore, small droplets were observed on the uneven surface, ascribed to the melting and wider distribution of lignin at 1000 kGy of γ-ray irradiation (Wang et al. 2012).
Previous studies showed that the recovery of sugars increased with γ-ray dosage, especially when γ-ray irradiation was integrated with other pretreatment systems, particularly dilute acid hydrolysis. For instance, the reducing sugar concentration experienced a steady rise from 0.017 (without γ-ray) to 0.048 g/l (500 kGy of γ-ray), which was further enhanced to 0.235 g/l when γ-ray irradiation was implemented with dilute acid pretreatment (Yoon et al. 2012). In another study conducted by Hong et al. (2014), a cellulose-enriched solid portion was produced because of the complete removal of xylose content, promoting more efficient enzymatic hydrolysis. When γ-ray irradiation was increased from 0 to 1000 kGy, the glucose yield improved from 24.9 to 40.2 %. However, when 1000 kGy of γ-ray was combined with 3 % of (w/w) H2SO4, 69.7 % of sugar recovery could be achieved because of the faster and greater release of soluble glucose (Hong et al. 2014). The combination of 1000 kGy and 3 % (w/w) of γ-ray and H2SO4, respectively, showed a remarkable fermentable sugar yield of 83.0 %, which was greater than the individual pretreatment of γ-rays (51.5 %) or dilute acid pretreatment (56.1 %) (Chung et al. 2012). The enhancement in sugar recovery was correlated with the greater disruption of cellulose crystalline structure, alteration in polymeric lignin structures as well as removal of hemicellulose (Hong et al. 2014). Furthermore, the integration of γ-rays with dilute acid pretreatment drastically decreased the CrI of poplar bark, reaching the lowest value of 4.5 % at 1000 kGy (Chung et al. 2012). However, excessive irradiation caused a decrease in the total reducing sugar concentration, as proven by Wang et al. (2012), when the radiation dosage was increased from 800 to 2000 kGy. Orozco et al. (2012) stated that the biomass degradation was irrelevant at a low dosage of <600 kGy, but further increased beyond 1800 kGy causing glycolytic degradation of sugars. Hence, the results implied that excessive γ-ray dosage above a certain threshold could have an adverse effect on sugar recovery because of monomeric sugar degradation. The performance of γ-rays in assisting sugar recoveries from various lignocellulosic biomass sources is summarized in Table 3.
Pulsed electrical field
Pulsed electrical field (PEF) is a form of electroporation or electropermeabilization in which the cell suspensions are basically subjected to high electric fields over a short period of time to increase the membrane permeability of the cells (Zbinden et al. 2013). A very short burst (~100 µs) of high voltage is applied from electrodes in order to induce the critical electrical potential, leading to rapid electrical breakdown and local structural changes of the plant tissue (Kumar et al. 2011). This technology is relatively established in the fields of biology, biotechnology and medicine for microorganism access. The application of an external electrical field above the transmembrane potential created very evident signs of cell polarity and produced charge separation as well as a dipole moment parallel to the external field (Zbinden et al. 2013). The formation of pores was even more visible using PEF at short duration pulses, whereas above the critical applied field, irreversible pore formation might result from dielectric rupture because of high electrocompressive forces (Zbinden et al. 2013). Field strength, pulse duration, number of pulses and type of electrical pulses (rectangular or exponential decay) were identified as several important parameters during PEF operation (Zbinden et al. 2013).
To date, PEF has not been directly used to recover sugars from lignocellulosic biomass. Instead, it was used as a pretreatment strategy for intensifying lipid extraction from the biomass (Zbinden et al. 2013) as well as algae on an industrial scale (Eckelberry et al. 2011; Kempkes et al. 2011). Nevertheless, PEF has the potential to be used as an alternative irradiation pretreatment of biomass for recovering sugars. This is because the phospholipids and peptidoglycan, which make up cell membranes and walls, contain polar molecules that give a net negative charge on the outer surface of cells (Stumm and Morgan 1996). Hence, the polar nature of the cell membranes and walls could make them more susceptible to the action of strong electrical fields. Zbinden et al. (2013) found that PEF was able to disrupt cells in the biomass to provide better access of enzymes to the biomass structure to improve sugar conversion. To prove this, Kumar et al. (2011) investigated the rate of colored dye in PEF-treated wood chips and switchgrass caused by the change of porosity during the pretreatment. The permeabilization of wood chips and switchgrass was significantly improved when the lignocellulosic biomass was pretreated with PEF at 8 and 10 kV/cm, respectively (Kumar et al. 2011). Thus, high PEF strengths in the range of 5–20 kV/cm might be able to facilitate the transportation of chemicals or enzymes into the lignocellulose structure for more efficient degradation, resulting in more desirable enzymatic or acid hydrolysis rates (Kumar et al. 2011).
Microwave
A microwave (MW) is defined as an electromagnetic wave that interacts with polar molecules such as water (Xia et al. 2013) and ions in a material to drive reactions (Diaz et al. 2015; Pang et al. 2012). MW energy is able to couple with the molecules in a pretreatment mixture in order to provide more volumetric and energy-efficient internal heating of a substrate. The polar molecules and disordered ions are spun by the oscillating electric field component in MW, dissipating heat via molecular friction for uniform and rapid heating (Chen et al. 2012b; Xia et al. 2013). Besides, materials containing dielectrics that were heated by electromagnetic energy could create non-thermal effects that enhanced the degradation of lignocellulose, which is more efficient than superficial heat transfer in conventional heating systems (Chen et al. 2012a; Xia et al. 2013). According to Lai and Idris (2013), MW irradiation did not cause local overheating, which might decompose the product, substrate or reagent during the pretreatment process.
When MW was used for lignocellulose pretreatment, MW radiation selectively heated the more polar regions of the biomass, generating “hot spots” to create explosion effects among the heterogeneous material particles. Subsequently, the crystalline structure in lignocellulose was disrupted (Vani et al. 2012). In a study conducted by Marx et al. (2014), pretreatment with MW heating was able to convert up to 100 % cellulose and 58.5 % hemicellulose into hexose and pentose sugars, respectively. Besides, MW could be easily combined with chemicals such as acid, alkali or other reagents for enhancing reaction rates (Binod et al. 2012). For example, remarkable results were achieved when MW was integrated with alkali, as the electrolyte solution acted as a microwave sensitizer for energy absorption (Tsubaki and Azuma 2013). The use of 2.5 M of NaOH with MW enabled the cleavage of inter- and intra-molecular hydrogen bonds within the lignin and hemicellulose matrix of biomass (Lai and Idris 2013). Higher sugar recovery was also achieved via MW acid (36.84 %) in comparison with ultrasonic acid (30.76 %) because of more effective lignocellulose degradation during MW heating (Gabhane et al. 2014a). Moreover, MW was used to intensify the fractionation of rice straw components in a FeCl3 solution, resulting in 2.9-fold reducing sugar production (Lu and Zhou 2011). Darji et al. (2015) and Mai et al. (2014) also successfully implemented ionic liquid with MW heating as the highly ionic and polar nature of the medium promoted rapid and effective dissolution during MW heating. As a result, the collision frequency between anions and cations of ionic liquid and biomass macromolecules intensified the breakage of hydrogen bonds within the biomass matrix (Darji et al. 2015). The performance of MW-assisted sugar recoveries from various lignocellulosic biomass sources is summarized in Table 4.
MW heating had the capability to form cracks and tiny cavities on the initially smooth, compact and rigid fibrils of raw biomass (Lai and Idris 2013; Vani et al. 2012). It was also able to damage and remove the silica waxy surface (Lu and Zhou 2011; Xia et al. 2013) of biomass, but changes were more significant when MW was used together with acid, whereby many channels and various sizes of pores were formed after undergoing the combined pretreatments (Xia et al. 2013). Chen et al. (2012b) claimed that an MW temperature of ≥130 °C caused the swelling of biomass when MW was assisted with ammonia, but the effects were barely noticeable below 130 °C. Lai and Idris (2013) also added that the exposure of the cellulose structure allowed for better enzyme accessibility, indicated by the enhanced CrI in oil palm trunks (42.07–56.08 %) and oil palm fronds (37.21–44.20 %). Similar trends were observed by Lu and Zhou (2011) and Vani et al. (2012), whereby the CrI of the biomass increased from 28.3 to 43.0 % and 45.3 to 60.0 %, respectively, after the removal of amorphous components that prevented the non-productive binding of enzymes and intensified cellulose digestion. According to Chen et al. (2011), the destruction of biomass structure became increasingly pronounced when the MW temperature was increased from 130 to 190 °C. Fragmentation and swelling were observed on the bagasse surface at 130 °C, while more severe disruptions were reported at 160 °C as shown in Fig. 3 (Chen et al. 2011). However, the effect of MW radiation seemed to be more apparent on the amorphous regions of the biomass rather than the crystalline regions (Binod et al. 2012).
High MW power and time favored the dissolution of extractives in the biomass, along with the condensation of lignin (Pang et al. 2012). Likewise, increases in these parameters improved glucose and xylose yields. For example, Janker-Obermeier et al. (2012) recorded greater removals of hemicellulose (80 %) and lignin (90 %) with higher power input due to the cleavage of inter-unit linkages in lignin that formed smaller molecular compounds, leading to a significant reduction in pretreatment time as compared to using alkaline pretreatment at ambient conditions. However, Rodrigues et al. (2013) confirmed the reduction of glucose recovery from 355 to 307 mg/g glucan when the power was raised excessively from 600 to 900 W. According to Xia et al. (2013), the hydrolysis of hemicellulose also markedly increased with temperature, as the biomass attained a low residual hemicellulose content of 16.93 % at 120 °C and complete degradation at 160 °C. On the other hand, a temperature of 180 °C assisted crystalline structure degradation and cellulose hydrolysis to achieve maximum glucose recovery of 8.74 g/100 g biomass, but the glucose was found to be degraded beyond 180 °C (Xia et al. 2013). Short pretreatment durations could be compensated with higher MW power. For instance, maximum reducing sugar yield was obtained using 3 and 24 min of pretreatment at 850 and 100 W, respectively (Binod et al. 2012). Nonetheless, Pang et al. (2012) affirmed that lower power and shorter times were recommended in pretreatment of lignocellulosic biomass because less severe conditions reduced both energy consumption and potential generation of degradation products because of localized overheating (Pang et al. 2012; Vani et al. 2012).
Ultrasound
An application of energy in the form of sound waves is known as ultrasonication, usually applied with a frequency of >20 kHz for the intention of cell disruption (Ofori-Boateng and Lee 2014b). Depending on the frequency, ultrasound (US) can be generally categorized into three classes, namely power (16–100 kHz), high frequency (0.1–1 MHz) and diagnostic (1–10 MHz) (Kang et al. 2013). US ranging from 20 to 100 kHz is usually used in chemically important systems in which chemical and physical changes are desired as it has the ability to cause cavitation of bubbles (Wu et al. 2013). During US, energy is simultaneously provided by means of cavitation, turbulence, agitation as well as heating (Rehman et al. 2014). When US is applied to liquid slurry, 4–300 micron bubbles can be generated (Luo et al. 2014). As a result, nearby particles are disintegrated for improved diffusivity or mass transfer because of vigorous hydromechanical shear forces (Luo et al. 2014; Rehman et al. 2014), which depolymerize the macropolymers in lignocellulosic biomass (Velmurugan and Muthukumar 2011). US has been used to assist many thermo- and biochemical reactions with increased sugars, bioethanol and gas products up to 10–300 % when US was combined with the proper solvents (Luo et al. 2014). However, the difficulty in calculating acoustic properties induced by US leads to very few studies being conducted to evaluate the effect of US pretreatment on the biomass (Hodnett and Zeqiri 1997).
Even though US alone was incapable of hydrolyzing polysaccharides to monomeric sugars (Villa-Velez et al. 2015; Yunus et al. 2010), it could assist the breaking of lignocellulosic linkages while producing fewer impurities in the process (Kang et al. 2013). As such, similar to enzymatic hydrolysis, US did not obtain remarkable recoveries when used on its own, but only when US was used as an auxiliary or before other pretreatments (Placido et al. 2013). Biomass pretreated by US was more easily hydrolyzed for extraction of cellulose, hemicellulose and lignin compounds (Luo et al. 2014) because of the increased accessible surface area and improved mass transfer of reactants (Kang et al. 2013; Placido et al. 2013). Gabhane et al. (2014b) successfully recovered more reducing sugars (59.56 %) via US-assisted alkali pretreatment, which was more than alkali alone (32.76 %). Also, Subhedar and Gogate (2014) reported that US caused a twofold increase in the extent of biomass delignification as compared to only using alkaline pretreatment. US was used to facilitate the diffusion of 1-allyl-3-methylimidazolium chloride ionic liquid into the structure of biomass (Liu et al. 2013). When the transient cavitation bubbles shrank or collapsed, high local temperatures and compressed air were formed to generate violent shock waves and jet streams to promote the binding of 1-allyl-3-methylimidazolium chloride to the biomass cellulose structures as shown in Fig. 4 (Liu et al. 2013). Moreover, the conversion of cellulose to glucose reached a maximum of 95.48 % when 1-methyl-3-methylimidazolium dimethylphosphate was used in conjunction with US (Yang et al. 2010). Hence, the result from the ionic liquid-US integrated pretreatment was significantly higher than the control (42.77 %) and cellulose treated with mere conventional heating (75.57 %). Velmurugan and Muthukumar (2011) found that US also facilitated contact between reactants during acid hydrolysis, subsequently hydrolyzing significant amounts of cellulose in a shorter period of time. Better catalyst-reactant contact during US was contributed by the phenomenon of micro-streaming, thereby improving mass and heat transfer (Luo et al. 2014). Therefore, faster reactions or a change of kinetics due to disengagement of heterogeneous reactants, intermediates and products could be achieved (Luo et al. 2014). The performance of US-assisted sugar recoveries from various lignocellulosic biomass sources is summarized in Table 5.
Some of the important parameters during US include the temperature and concentration of the medium (Ofori-Boateng and Lee 2014b). For example, US was proven to work well at low temperature ranges in any concentration of NaOH (Kang et al. 2013). Specifically, the enzymatic digestibility of biomass after undergoing NaOH pretreatment increased by 27 % when the pretreatment was coupled with US at a low temperature of 30 °C, but the effects were diminished at high temperature of around 80 °C (Kang et al. 2013). Yang and Fang (2014) observed comparable trends in which the total sugar yields reached a peak of 65.05 % at 50 °C. At lower temperature, cavitational effects were dominant in assisting the diffusion of enzymes into substrate networks. Furthermore, Villa-Velez et al. (2015) mentioned that the biomass could behave like a liquid to allow the spread of shock waves from bubble collapse throughout the entire volume of medium at low biomass concentration. High solid-to-liquid ratios could be detrimental to US effects, as proven by Bussemaker et al. (2013). They reported that the cavitation was hindered at 1:15 (g/ml) concentration of wheat straw, leading to inefficient physico-chemical effects. The concentrations of solid substrates were ranged between 2 and 5 wt%, as 5–10 wt% would require the addition of acid/base to improve the efficiency of US (Luo et al. 2014).
More importantly, the frequency, time and power of US also play significant roles in ultrasonication efficiency (Ofori-Boateng and Lee 2014b). Jiang et al. (2011) found that biomass exposure to low-intensity US for longer duration was similar to that of high intensity for shorter duration. According to Ofori-Boateng and Lee (2014b), low-intensity US could facilitate the disintegration of the biomass cell wall. Ashokkumar et al. (2008) highlighted that low- (20–100 kHz) and high-frequency (>100 kHz) US favored physical disruption and radical generation, respectively. High frequency US could be unsuitable for cavitation because of insufficient time, radial motion and bubble collapse (Luo et al. 2014). Besides, the smaller volume change of bubbles also contributed to rapid decay of acoustic energy (Luo et al. 2014). For example, US caused significant physical damage such as pits and cracking at 40 kHz and major carbohydrate solubilization due to enhanced radical attacks at 995 kHz (Bussemaker et al. 2013). In a detailed investigation conducted by Suresh et al. (2014), it was concluded that the contribution of US through micro-streaming was more significant for increasing sugar content as opposed to micro-turbulence and acoustic waves generated by the cavitation (Suresh et al. 2014). US at spatial and temporal scales was ineffective in opening biomass structure, and the US only facilitated the transport of monosaccharides out from the biomass matrix (Suresh et al. 2014). Basically, the majority of the US was beneficial in extracting carbohydrates within the first 20–30 min of pretreatment (Bussemaker et al. 2013). Rehman et al. (2014) enhanced the sugar yields by twofold when the sonication time was increased from 30 to 50 min. On the other hand, Yunus et al. (2010) attained a maximum xylose yield of 52 %, as compared to the control (22 %), when 90 % amplitude was applied for 45 min. However, contradictory results were reported by Subhedar and Gogate (2013), whereby lower sonication time was recommended for minimizing energy consumption and lignin condensation. Glucose recovery from starchy materials was improved using US for 5–10 min, while 10–20 min was more suitable for lignocellulosic materials (Subhedar and Gogate 2013). Pejin et al. (2012) also added that while US for short periods might be effective in destroying amorphous regions, the compact crystalline regions could not be degraded easily even at longer sonication durations. In addition, US power greatly affected the number and lifetime of cavitation bubbles as well as the cavitation intensity. Particularly, bubbles that were formed at the transducer during US at high power levels might obstruct the transfer of energy to the medium, adversely affecting the cavitational effects (Subhedar and Gogate 2014). Villa-Velez et al. (2015) found that the morphology of the biomass changed in accordance with the power: the cellulose structure was altered at 300 W; a homogeneous structure with compact and shorter fibrils was formed at 900 W; cellulose microstructure particle size was significantly reduced at 1500 W. Regardless, yields were found to be proportional to the power, but the US power and time were inversely related (Imai et al. 2004). Stirring during US was not recommended as it could interrupt the cavitation field around the solid surface in the solid–liquid system, causing the liquid jet force to be abated and thus decreasing the radical production (Bussemaker et al. 2013).
According to Ninomiya et al. (2013), the biomass became rougher after introducing choline acetate pretreatment, but was further disordered with the implementation of US. Alkali pretreatment that was assisted with US showed that the surface of sugarcane bagasse became rough and porous because of the combined effects of NaOH swelling and free radicals formed by US (Velmurugan and Muthukumar 2011). The effect of US on biomass surface morphology is shown in Fig. 5 (Kim and Han 2012). In addition, the physicochemical effects induced by dilute acid microbubbles during US created a microporous surface that enabled easier access to the biomass interior structure (Rehman et al. 2014). The cavitation phenomenon during US even caused surface pitting with severe surface erosion (Luo et al. 2014) and bumps on the surface, along with the reduced silica content from 5.94 to 0.94 %, which promoted hydrolysis (Yang and Fang 2014). Yunus et al. (2010) deduced that the perforation of the silica crater contributed to better penetration of water molecules into the biomass during US-assisted acid hydrolysis. Also, acid hydrolysis increased the CrI of sugarcane bagasse from 50 to 66 % and was further enhanced to 70.7 % when the pretreatment was integrated with US (Velmurugan and Muthukumar 2011). Gabhane et al. (2014b) reported a decrease in the degree of biomass polymerization after undergoing US irradiation, exhibited by an increase of CrI from 72.9 to 82.8 %. In comparison with MW irradiation, which formed fragmentation at 200 °C, US caused fibrillation to the biomass surface, in which the cellulose fibrils appeared as forks and fine fibrils with major cracks on the cell wall, as shown in Fig. 6 (Gabhane et al. 2014b). In this aspect, US appeared to be more advantageous as the fibrillation would ease enzymatic hydrolysis, whereas the complete tissue collapse after undergoing MW resulted in less space for microbial activities (Gabhane et al. 2014b). Also, US energy was capable of causing particle size reduction for improving solubilization (Bussemaker et al. 2013). For instance, when US was used with hot water, the surface area was enhanced with a reduction of average particle size of biomass from 1000 to 10 μm (Imam and Capareda 2012).
Prospect of energy irradiation pretreatment
Advantages of energy irradiation
One of the main advantages of energy irradiation is the reduced toxicity during biomass pretreatment as the use of reagents is not essential, though the combination between energy irradiation and chemicals usually gives higher sugar recovery. Thus, the need to set up a wastewater treatment system for the spent chemicals may be eliminated, which is economically viable especially in large-scale operations. Furthermore, according to Karthika et al. (2012) and Sundar et al. (2014), certain ionizing radiation methods such as EB had the advantage of disrupting complex lignocellulosic structures without forming any inhibitory components since extreme temperature was not required during the energy irradiation pretreatment (Bak et al. 2009). The negligible production of major inhibitors such as acetic acid, furfural and HMF content contributed to better bioconversion rates in the later stages (Bak 2014). Duarte et al. (2012) confirmed that the combination of energy irradiation and enzymatic hydrolysis managed to decrease pretreatment severity, preventing both excessive sugar degradation and generation of toxic by-products.
Additionally, some irradiation technologies offer vast opportunities for cost reduction during biomass pretreatment because of less severe operating conditions and ease of operation. For example, PEF could be carried out under ambient conditions with low energy usage, since processing could be done at relatively short pulse times as well as at ambient temperature (25 °C) and pressure (1 atm) (Kumar et al. 2011). PEF is a very energy-efficient technique, as the rupturing of cells is contributed by the presence of the electrical field and not temperature effects. Particularly, PEF showed remarkable energy savings of 50, 80 and 95 % in comparison with traditional mechanical, enzymatic and thermal pretreatment technologies, respectively (Zbinden et al. 2013). In addition, no moving part is involved in the equipment, which simplifies the equipment operation. On the other hand, MW irradiation offers lower process energy and time requirements, consistent processing, better control and flexibility in process operation, high reaction rates as well as reductions of equipment size and waste reagents (Darji et al. 2015; Rodrigues et al. 2011). Kannan et al. (2013) claimed that the energy input using MW pretreatment contributed to only 7 % of the total energy needed during bioethanol production from sago barks. Moreover, the energy consumption of MW-alkali pretreatment was reported to be approximately 108 kJ, which was five times less than using high pressure pretreatment (Vani et al. 2012). Thus, MW is a cost-effective and easy alternative that may offer better yields than conventional pretreatments at a commercial level (Binod et al. 2012; Kannan et al. 2013). Moreover, the reduction in energy demands for γ-ray irradiation ($ 0.48/kg) led to lower pretreatment costs than traditional physical pretreatments such as ball milling ($ 5.82/kg) and roller milling ($ 14.0/kg) (Fan et al. 1981).
In fact, the process time required for biomass pretreatment and enzymatic saccharification could be reduced significantly when energy irradiation is coupled with other conventional pretreatments such as dilute acid and alkali hydrolysis. A case in point, hydrolysis of rice straw was 22 times faster when 1-ethyl-3-methylimidazolium acetate-dimethlysulfoxide was used together with MW, resulting in four times higher sugar productions than untreated rice straw (Mai et al. 2014). The carbon-rich biomass also acted as a good MW energy absorber and required less energy to generate hydrothermic conditions for polysaccharide hydrolysis (Diaz et al. 2015; Tsubaki and Azuma 2013). In fact, MW could selectively heat polar molecules after penetrating into the inner particles, resulting in reduced heating time by a factor of over ten as compared to conventional heating, which usually utilizes conduction and convection (Xia et al. 2013). Bak (2014) further demonstrated the potential for energy/time saving during the subsequent fermentation process, as the fermentability of biomass treated with EB was around 2.1 times higher than the untreated biomass. The sugar yield from rice straw radiated with EB achieved 65.5 % after 10 days of biodegradation, which was similar to that of unradiated rice straw (64.8 %), which took a longer biodegradation period of 15 days to achieve similar results (Bak 2014).
Challenges faced in energy irradiation
One of the major bottlenecks for most energy irradiation technologies lies in the scaling-up of irradiation systems for industrial application. This may be due to the difficulty in handling and inefficient irradiation at large volumes, such as the scaling up of MW technology (Zheng et al. 2014, Vani et al. 2012). In addition, MW irradiation cannot be carried out indefinitely without a loss of liquid at atmospheric pressure, since the pretreatment time is only limited to the boiling point of the sugar broth (Marx et al. 2014). In order to minimize the loss of sugar broth, the duration of MW at atmospheric pressure could be limited, but with lower liberation of sugars from the biomass. Therefore, Diaz et al. (2015) have successfully implemented the use of high-boiling-point glycerol as the hydrolysis medium so that it could be maintained at liquid state during MW heating. US also faces some challenges as the use of an incorrect sonochemical reactor and parameter choices could cause poor sonification and unfavorable economics, leading to low efficiency especially in scaled equipment (Luo et al. 2014). According to Kim and Han (2012), the sonication effect may sometimes be insufficient to warrant the use of US for biomass pretreatment, since the improved digestibility could be attributed to the temperature rise instead of the physical and chemical changes due to the US itself. Nevertheless, Bussemaker and Zhang (2013) insisted that the use of US to pretreat biomass in biorefinery and biofuel applications promised significant benefits, possibly in the form of reduced energy requirements and higher accessibility of microorganisms during enzymatic hydrolysis and fermentation. Hence, irradiation technologies such as US in biomass pretreatment provide various opportunities for cost reduction in other aspects, such as reduction in enzyme loading as well as shorter treatment times (Sabarez et al. 2014).
Furthermore, the efficiency of energy irradiation strongly depends on the type of biomass sample. In the case of MW heating, polarizable components were preferred for dipole orientation in the electrical field (Janker-Obermeier et al. 2012). Hence, a modification of the direction and strength of the electrical field would be essential to rotate the dipoles and induce effective biomass heating. Also, Wang et al. (2012) highlighted that γ-rays appeared to be strongly selective toward certain biomass species, working more favorably for pretreatment of cellulosic materials for ethanol conversion purposes. Moreover, the efficiency of PEF was also largely dependent on the type of biomass used during the pretreatment process, as the degree of electropolaration was observed to be lower for biomass with higher lignin content since it was harder to be broken down (Kumar et al. 2011). Therefore, even if an irradiation technique was proven to be effective in pretreating a certain type of biomass, it might not be suitable for another biomass.
Conclusion
Generally, irradiation is free of toxicity since reagents or additives are not required, making it more environmentally friendly and simpler in comparison with conventional pretreatment methods such as dilute acid and alkaline hydrolysis (Yoon et al. 2012). Additionally, radiation has the capability to cause polymer degradation reproducibly and quantitatively (Orozco et al. 2012). However, the high intensity of energy associated with the majority of irradiation methods contradicts the main purpose of the pretreatment, which is to induce a cost reduction for an effective downstream transformation process. As such, the increasing demand for environmental sustainability warrants more research efforts to be done in utilizing energy irradiation for biomass pretreatment, despite concerns regarding the cost in technology. The use of reducing sugars as building blocks for value-added products holds great promise for sustainable development. Therefore, improvements need to be done at a scientific level to fully understand the mechanism involved during radiation pretreatment. Studies at the tissue and cellular scale will hence be pivotal so that better optimization works can be done for the development of cost-effective pretreatments (Loow et al. 2016). Also, more studies need to be conducted at the engineering level in terms of reactor design and process optimization as well as the economic level via cost reduction and improvement in energy efficiency.
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Acknowledgments
The funding of this study is supported by the Ministry of Higher Education, Malaysia, under the Long Term Research Grant Scheme (LRGS/2013/UKM-UKM/PT/01) and University of Malaya Research Grant (RP002D-13AET). In addition, the authors would like to thank Monash University Malaysia for providing Y.-L. Loow with a postgraduate scholarship.
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Loow, YL., Wu, T.Y., Yang, G.H. et al. Role of energy irradiation in aiding pretreatment of lignocellulosic biomass for improving reducing sugar recovery. Cellulose 23, 2761–2789 (2016). https://doi.org/10.1007/s10570-016-1023-x
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DOI: https://doi.org/10.1007/s10570-016-1023-x