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Lignocellulose to bio-hydrogen: An overview on recent developments
international journal of hydrogen energy xxx (xxxx) xxx
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Lignocellulose to bio-hydrogen: An overview on recent developments Monika Yadav, Kunwar Paritosh, Vivekanand Vivekanand* Centre for Energy and Environment, Malaviya National Institute of Technology Jaipur, JLN Marg, Jaipur, Rajasthan, 302017, India
highlights Lignocellulose to biohydrogen production has been reviewed. Pretreatment strategies to improve biohydrogen have been discussed. Recent trends in research for biomass to hydrogen conversion have been summarized.
article info
abstract
Article history:
Production of hydrogen from lignocellulosic biomass using biological methods is an
Received 25 April 2019
alluring approach to generate green and clean energy. However, the challenges levied by
Received in revised form
structural and compositional aspects of lignocellulosic biomass block the way to harness
27 September 2019
their complete energy potential. The review revisits the available methods of pretreatment
Accepted 2 October 2019
to augment the accessibility of carbon source required for microorganism to perform
Available online xxx
biomass to hydrogen conversion. The fermentation methods that have been employed for years for bio-hydrogen production are discussed in brief to provide the background of
Keywords:
biological routes of hydrogen production. The review further highlights the latest research
Lignocellulosic biomass
trends and upgrades in technologies including the identified novel microbial strains,
Pretreatment
reactor configurations, integrated schemes of fermentations, nanocatalysts addition and
Bio-hydrogen
the genetic engineering tactics to enhance the competence of hydrogen producing bacteria.
Dark fermentation
© 2019 Hydrogen Energy Publications LLC. Published by Elsevier Ltd. All rights reserved.
Photo fermentation
Introduction Developing countries like India, are struggling to have clean energy sources to fulfil gross energy demand [1]. Conventional sources such as coal and petroleum are exhausting day by day and search for non-conventional alternatives is stressed for uninterrupted supply of energy. Renewable sources (viz. Solar, wind, biomass, ocean and small hydro), on the other hand, may be helpful to meet the gross energy demand and may
create a sustainable cum circular economy [2]. However, in the context of transportation fuel from renewable sources, only biomass-based fuels may replace the petroleum-based transportation industry as solar and wind are intended to other energy applications. In transportation sector, hydrogen is now a days considered as a potential fuel. Automobile companies in different countries are putting effort for hydrogen driven vehicle to curb environmental pollution and degradation. Most of the world-renowned companies in vehicle are shifting towards hydrogen-based
* Corresponding author. E-mail address: [email protected] (V. Vivekanand). https://doi.org/10.1016/j.ijhydene.2019.10.027 0360-3199/© 2019 Hydrogen Energy Publications LLC. Published by Elsevier Ltd. All rights reserved. Please cite this article as: Yadav M et al., Lignocellulose to bio-hydrogen: An overview on recent developments, International Journal of Hydrogen Energy, https://doi.org/10.1016/j.ijhydene.2019.10.027
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economy in terms of transportation fuel. The burning of hydrogen as a fuel only releases water vapour as coproduct which makes it attractive option for sustainable approach. Also, 1 g of hydrogen possess around 142 kJ of energy which is further alluring for fuel application [3]. However, the world needs alternative for hydrogen production as most of the hydrogen is being produced from nonrenewable sources. The carbon rich non-biodegradable matters exploited for production of hydrogen are non-desirable option for sustainable city, society and economy. Hence, the focus needs to be shifted on degradable and renewable resources for hydrogen production. There are various ways by which bio-hydrogen may be produced. Some of notable processes are dark fermentation (DF), photo fermentation (PF), bio photolysis and indirect bio photolysis. From all the processes to produce hydrogen, DF is reported to be an efficient one as it does not require additional energy to operate [3]. However, the major obstructions associated with DF for hydrogen production are high operational cost and production efficiency. Being a carbon neutral substrate, lignocellulosic biomass is an attractive feedstock for production of bio-hydrogen. Since the food or fuel debate dominates the use of first-generation biomass for fuel production, employing non-edible second generation biomass is recommended [4]. Second generation biomass is consisting of lignin rich feedstock such as stalks, stover and residues of crops, forestry waste, wood chips and clippings, twigs and fallen leaves. The second-generation biomass is rich in various fermentable sugars (pentoses and hexoses) along with the existence of lignin. These fermentable polysaccharide sugar such as hexose and pentose could be advantageous for bio-hydrogen production [5]. However, lignin, a polymer, encircles the physical structure of lignocellulosic biomass, the holocellulose (cellulose þ hemicellulose) which makes its hydrolysis an energy intense process and tedious. To expose the fermentable sugar existing in the lignocellulose for hydrolysis, pretreatment is required. The next section of the review
summarizes the structural arrangement of biomass and the pretreatment approaches to improve its degradability for hydrogen production. The review further confers the fermentation approaches and the recent trends in research and technologies to enhance the bio-hydrogen yield in the subsequent sections.
Lignocellulosic biomass structure, pretreatment and inhibitions Structure of lignocellulosic biomass Lignocelluloses are the most abundant raw material on earth [6]. The lignocellulosic biomass comprises of wood (hardwood and softwood), grass, leaves, agricultural stubble, crop residues, forestry waste and organic fraction of municipal solid waste. The production of lignocellulosic biomass is stated to be around 0.22 trillion tonnes [7]. The lignocellulosic biomass is composed of cellulose and hemicellulose collectively known as holocellulose (Fig. 1). This combination of cellulose and hemicellulose is encircled with a recalcitrant material, lignin. For bio-hydrogen production, holocellulose is needed as it consists of C6 and C5 linear and branched polysaccharides. For example, glucose, mannose, xylose and arabinose are common example of sugar present in lignocellulosic biomass. However, lignin shows recalcitrant nature in bio-hydrogen production and decreases the conversion efficiency and effectiveness of lignocellulosic biomass into bio-hydrogen. The sturdy nature of lignin is responsible for low performance of direct conversion of lignocellulosic biomass to biohydrogen.
Cellulose Cellulose is the most ample and highly stable polymer in nature. The lignocellulosic biomass comprises of nearly 40e45% of cellulose having both crystalline and amorphous structure.
Fig. 1 e Structural arrangement of plant cell wall. Please cite this article as: Yadav M et al., Lignocellulose to bio-hydrogen: An overview on recent developments, International Journal of Hydrogen Energy, https://doi.org/10.1016/j.ijhydene.2019.10.027
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Most of the cellulose is well assembled and crystalline in nature while the rest of it is amorphous. Amorphous cellulose is preferred for degradation over crystalline cellulose as crystallinity makes the degradation difficult [4]. The bonds present in cellulose molecules are hydrogen and covalent with Vander-wall force. Hydrogen bonding present in cellulose is responsible for its straight nature whereas interchain hydrogen bonds presents in the cellulose decides the structural arrangement. Inter and intramolecular hydrogen bonds existing in the cellulose makes it rigid in nature. This rigid nature of cellulose opposes any solubilization in organic solvent and shows resistant to it.
Hemicellulose Hemicellulose which is the second most abundant polymer in nature, shares around 30% of lignocellulosic biomass. The molecular weight of hemicellulose is around 30000 g/mol. Unlike cellulose, hemicellulose is made of heterogeneous polymers which mainly consist of lateral chains of various sugars such as pentoses, hexoses and uronic acids. Composition of hemicellulose varies in lignocellulosic biomass. Grass and agricultural stubbles are mainly consisting of xylan while glucomannan is main constituent of softwoods. Extraction of xylan is responsive to mild acid or alkali treatment whereas glucomannan requires strong environment of alkali [6]. It was also reported that hemicellulose is very sensitive to thermochemical treatment as compared to cellulose and lignin [3]. In lignocellulosic biomass, hemicellulose covers cellulose from outside and to expose cellulose for enzymatic actions, 50% of hemicellulose should be displaced. However, if the disruption of hemicellulose is severe and not controlled, degradation products of hemicellulose such as furfural and hydroxymethyl furfural (5 e HMF) may hamper the biomass degradation process. Furthermore, severity condition of biomass treatment may be compromised to dodge the generation of inhibiting by-product of hemicellulose degradationand to increase the sugar availability [6].
Lignin After cellulose and hemicellulose, lignin is the third most abundant polymer in nature. Cross linkages of phenolic monomers make lignin a complex and large molecule. The phenolic monomers which make impermeable structure of lignin are coniferyl, sinapyl and coumaryl alcohols [8]. These phenolic monomers are linked together by alkyl-alkyl, arylalkyl and aryl e aryl ether bonds [6]. The complex and sturdy nature of lignin acts as a barrier to the plant cell wall degradation and oxidative stress caused by microbes. Generally, the grasses are reported to have lower percentage of lignin while softwood has higher percentage. Lignin often makes lignin-cellulose complex (LCC) with cellulose microfibrils which makes biomass deterrent to the microbial activity and hydrolysis. The percentage of lignin in lignocellulosic biomass mainly depends on the origin and type of the biomass [8].
Extractives Extractives are chemicals that are non-polymeric part of lignocellulosic biomass which can be extracted with the help of solvents [7]. Solvents such as acetone, water, toluene,
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hexane etc. may be employed for extraction of extractives. In general, biomass consists various extractives such as proteins, pectin, waxes, essential oils, phenolics, flavonoids etc. Based on solubility, extractives may be classified as water soluble, ether soluble and toluene/ethanol soluble extractives. Bark of the hardwood consists phenolic extractives. These phenolic extractives protect the plant cell wall against microbial attack.
Pretreatment of lignocellulosic biomass Pretreatment of lignocellulosic biomass is intended for enhanced hydrolysis rate and a smoother process stability for hydrogen production. Pretreatment helps to alleviate the enzymatic activity by breaking the lignocellulosic structure and rupturing the lignin cellulose complex [9]. The plant cell wall lysis is often increased by delignification of biomass which consecutively boosts the increase the hydrolysis.
Chemical pretreatment Use of chemicals and reagents for removing the lignin barrier in lignocellulosic biomass is called as chemical pretreatment. Alkalis, acids, organic solvents, ionic liquids and chlorides of metal ions are commonly employed chemicals for pretreatment of biomass. Alkalis and acid pretreatment are most explored and economical pretreatment strategy among all the chemical pretreatment. Alkalis generally targets the ester bonding between the lignin and hemicellulose which help to solubilize the hemicellulose as well as expose the cellulose for hydrolysis. NaOH, KOH and CaOH2 are the most commonly used alkalis for pretreatment of lignocellulosic biomass to produce bio-hydrogen. However, higher concentration of alkalis may dissolve substantial hemicellulose which might be a loss of useful product for hydrolysis [10]. Lime, on the other hand, is a safe and economically competitive alternative to sodium hydroxide. Cao et al. [11] employed lime to pretreat corn stalk for bio-hydrogen production. It was reported that 38% higher bio-hydrogen yield was obtaines as compared to untreated corn stalk at the loading of 0.1 g of lime for 1 g of corn stalk. Also, the characterization of corn stalk showed that 23% of lignin was removed. It was also reported that kiln technique may help to recover the lime which could be an economical and effective approach for enhanced bio-hydrogen production. Pretreatment of sweet sorghum bagasse with sodium hydroxide for enhanced bio-hydrogen yield was performed by Panagiotopoulos et al. [12]. It was observed that at 10% of NaOH (w/w of dry matter) showed maximum delignification (46%) and maximum biohydrogen yield (10.2 mmol/(L h)). For acid pretreatment of lignocellulosic biomass, Sulphuric acid, hydrochloric acid, boric acid and nitric acid are common examples. In acid pretreatment, lignin gets solubilized which expose the holocellulose for better and improved hydrolysis. The degree of solubilization of lignin depends on the strength of acid whether the acid is dilute or strong. Cao et al. [13] employed dilute hydrochloric acid for the pretreatment of corn stover for enhance bio-hydrogen production. The H2SO4 concentration was selected as 0.25e4% v/v for the pretreatment of corn stover at 121 C for 30e180 min.
Please cite this article as: Yadav M et al., Lignocellulose to bio-hydrogen: An overview on recent developments, International Journal of Hydrogen Energy, https://doi.org/10.1016/j.ijhydene.2019.10.027
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As per results, 1.69% of acid showed maximum hydrogen yield (3305 ml H2/L medium) at the time of 117 min. Unlike separate alkali and acid pretreatment of lignocellulosic biomass, combined ammonia and dilute acid pretreatment of rice straw was attempted by Nguyen et al. [14]. The digestibility of rice straw was increased up to 85% in the case of combined pretreatment (10% ammonia and 1% dilute sulphuric acid). It was also reported that 72% of glucose and 95% of xylose was converted to bio-hydrogen. Chong et al. [15] studied the effect of acid pretreatment on palm oil fruit brunch for bio-hydrogen production. 6% of sulphuric acid yielded maximum bio-hydrogen which was 690 mL/L medium for palm oil fruit brunch. The sugar production was also increased by 78% with acid pretreatment.
Physical pretreatment Physical pretreatment refers to the use of mechanical instruments to disrupt the tough lignocellulosic structure for accessible holocellulose. Mechanical instruments such as grinder, ball milling, screw press, microwave and sonication are commonly used for physical pretreatment of biomass. These instruments reduce or change the surface area of lignocellulosic biomass making it amenable for digestion and solubilization. Silva et al. [16] reported that yield of glucose was more in case of ball milling pretreatment as compared to steam explosion. Also, the size reduction by physical pretreatment help to reduce the crystallinity of cellulose as crystalline cellulose is less accessible as compared to amorphous one. Zhao et al. [17] reported that ball milling helped to reduce the crystallinity of a e cellulose. One of the drawbacks of physical pretreatment is that the method is energy intense and may distort the equation of net energy gain. It was suggested to combine the physical pretreatment with chemical or biological pretreatment for positive net energy gain [17]. Microwave and sonication use electromagnetic wave to disrupt the ester and ether linkages in lignin cellulose complex. Leano et al. [18] employed ultrasonication for the pretreatment of palm oil mill effluent in bio-hydrogen production. Results showed that the bio-hydrogen productivity and COD removal was 38 and 20% more as compared to untreated one at ultrasonication dose of 195 J/ml. The maximum biohydrogen produced was 0.7 mmol H2/g COD. It was also reported that lower dose of ultrasonic waves (91 J/ml) showed negligible effect on biohydrogen production but increasing the frequency showed positive results. Apart from ultrasonication, microwave assisted acid pretreatment of corn stover for improved biohydrogen production was performed by Liu and Cheng [19]. A microwave with rated power 700 W was selected for acid assisted pretreatment. The time of microwave pretreatment was selected as 5, 15, 30, 45, 60 and 90 min. Results showed that maximum hydrogen production was observed at 45 min which was 1.53 mol H2/mol glucose. Coupling the microwave pretreatment with other pretreatment may have fruitful impact on biohydrogen production. Also, coupling acid assisted microwave pretreatment has been reported to have short pretreatment duration, higher sugar yield and no or less inhibitor formation [20]. Palm oil trunk was pretreated with microwave irradiation (450 W)
assisted with sulphuric acid for improved hydrolysis and it was observed that 1.56% of sulphuric acid (w/v) at 450 W and 7.5 min reaction time in microwave showed maximum hydrolysis of glucose, xylose and arabinose. The yield of glucose, xylose and arabinose was 8.95, 8.29 and 4.57 g/L respectively. Increasing the concentration of sulphuric acid from 1 to 3% w/v showed increment in sugar yield. However, increasing the concentration of sulphuric acid in above reported study did increase the inhibitors as HAc. Maximum HAc (3.97 g/L) as inhibitor was observed at 3% of sulphuric acid (w/v).
Biological and biochemical pretreatment In biological pretreatment, enzymes or microbes perform the depolymerization of lignocellulosic biomass. Enzymes or microbes act as a precursor to the hydrolysis of biomass in biological pretreatment. Fungus is commonly used biological entity to perform biological pretreatment for its exclusive lignolytic and delignification property [4,9]. Fungus such as brown rot, white rot and soft rot are common example of fungal species employed for biological pretreatment. During biological pretreatment with fungus, depolymerization of biomass generally happens outside the plant cell wall due to insolubility of biomass. In this regard, lignolytic enzymes are required in the pretreatment process for efficient lignin disruption. Peroxidase of lignin and manganese and laccase are the enzymes secreted by fungus which are responsible for oxidative stress in lignin. Zhao et al. [21] employed Phanerochaete chrysosporium for pretreatment of corn stalk for biohydrogen production. The corn stalk was pretreated at 29 C for 15 days with Phanerochaete chrysosporium and delignification was reported to be 34%. It was also observed that in pretreated corn stalk enzymatic saccharification was 20% higher as compared to the untreated corn stalk. Though depolymerization of lignin with the help of fungi is reported supportive, selectivity of fungi for lignin degradation is of utter importance to prevent loss of hemicellulose. Enzymes may reduce the time of biological pretreatment process and may provide better delignification. In enzymes, cellulase, endoxylanase, amylase and bromelain are common example for biochemical pretreatment of lignocellulosic me neur et al. [22] performed biochemical prebiomass. Que treatment by adding exogenous enzymes in fermentation of wheat straw for bio-hydrogen production. Results showed that addition of 1e5 mg of enzyme for per g of wheat straw yielded maximum bio-hydrogen. While untreated showed 10.5 ml of hydrogen per g of volatile solid, enzyme addition enhanced the bio-hydrogen production up to 19.6 ml/g VS. Although enzymatic pretreatment saves time, cost of the enzyme and its synergy with chemical mediators for oxidative stress are still an explorable concern [23].
Physiochemical pretreatment Other than chemical, physical and biological, pretreatment of lignocellulosic biomass is also performed under steam explosion, ammonia fibre explosion (AFEX) and liquid hot water. These pretreatment methods are termed as physiochemical pretreatment of biomass. In steam explosion, which is one of the oldest techniques, biomass is exposed to high pressure and temperature and left for some time before quickly
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decompressing it. Huang et al. [24] performed steam explosion pretreatment cotton stalk in 1% sulphuric acid solution for enhanced enzymatic saccharification. High conversion rate of sugar to biofuel from cotton stalk with no or less inhibition was observed as per the results. Vivekanand et al. [25] demonstrated the effect of severity on birch after steam explosion at 13 combinations of temperature (170 - 230 C) and time (5e15 min). The study reported xylan degradation and generation of pseudo-lignin caused by the increased severity of steam explosion pretreatment. All types of pretreatment and the relevant studies regarding their impact on bio-hydrogen yield and lignin removal discussed in this section are summarized in Table 1.
Inhibition in pretreatment Pretreatment may be considered as a promising route to rise the production of bio-hydrogen from lignocellulosic biomass. However, degradation products formed in different pretreatment approaches may hamper the improved bio-hydrogen production. The degradation products or the inhibitors may be classified in to two categories, furan compounds and weak acids [3]. Furfural and 5 - hydroxymethyl furfural (5 - HMF) are called furan compounds while acetic and formic acids are called weak acids. It is noteworthy that production of degradation products and inhibitors may rupture the microbial cell wall and hinder the microbial and biochemical activity for biohydrogen production. Toxic substances such as furan derivatives may change the pH level in the reactor if present by shifting carboxylic acids into intracellular space and may puncture the cell wall. Weak acids may disturb the optimum acid concentration in the process which also disturb the optimum pH level. Monlau et al. [26] studied the effect of dilute acid hydrolysate on formation of inhibitors while pretreating sunflower stalk for biohydrogen production. Sunflower stalk hydrolysate was prepared by mixing 4 g of HCL in 100 g total solid (TS) of stalks at 170 C for 1 h duration. It was observed that furan derivatives and weak acids were also released besides fermentable sugar from sunflower stalk. The concentration of acetic and formic acid were 0.6 and 0.8 g/L and concentration of furfural and 5 e HMF were 1.15 and 0.13 g/L respectively in the hydrolysate of sunflower stalks. After preparing the hydrolysates, it was mixed in the ratio of 0, 3.5, 7.5, 15 and 35% v/v with glucose as carbon source which was 5 g VS/L of
concentration. A sharp decline was noticed in biohydrogen yield at 15% concentration of hydrolysate þ glucose (0 mol of hydrogen per mole equivalent hexose consumed) compared to glucose only which was 2.04 mol of hydrogen per mole equivalent hexose consumed. Similar results were also reported by Arisht et al. [27] in acid hydrolysate of coconut husk. Pretreatment with phosphoric acid resulted in 0.19, 0.23 and 0.65 g/L of furfural at 1, 5 and 10% v/v concentration. The acetic acid at 1, 5 and 10% concentration of phosphoric acid was 0.36, 0.43 and 0.75 g/L respectively. However, the accumulation of 5 e HMF was minimal (0.0048, 0.0164 and 0.0189 g/L) at various concentration of phosphoric acid (1, 5 and 10%). Also, the bio-hydrogen production was 0.68, 0.52 and 0.45 mol hydrogen/mol sugar consumed from acid hydrolysates (1, 5 and 10% respectively). The extent of the inhibition strongly depends on the concentration of degradation products in the system as well as tolerance capacity of specific microorganisms. Detoxification process of acid hydrolysates may reduce the adverse effect on biohydrogen production. Ion exchange and oxidation processes may be adopted prior to fermentation to reduce ill effects of inhibitors.
Approaches for bio-hydrogen production Classification on the basis of process configuration The fermentation process for hydrogen production can be categorized on the basis of arrangement of pretreatment, hydrolysis and fermentation steps, which can be performed simultaneously in same reactor or sequentially in separate vessels. The three approaches for hydrogen production from lignocellulosic biomass are summarized in the following subsections and Table 2:
Separate hydrolysis and fermentation The conventional approach of producing hydrogen from lignocellulosic biomass comprises of performing hydrolysis and fermentation processes separately in two different reactors [28]. The optimum conditions for hydrolysis and fermentation can be different. Therefore, separate hydrolysis and fermentation (SHF) can enhance the hydrogen production efficiency by carrying out hydrolysis and fermentation at desired optimum conditions in two separate apparatus [7]. Since the ease of fermentation relies upon the efficient
Table 1 e Pretreatment for improved bio-hydrogen production. Feedstock Corn stalk Sweet sorghum Corn stover Rice straw Palm oil fruit brunch Palm oil mill effluent Corn stover Corn stalk Wheat straw Cotton stalk
Pretreatment
Lignin removal (%)
Bio-hydrogen yield
References
Alkali (Lime) Alkali (NaOH) Acid (HCL) Combined (alkali þ acid) Acid (H2SO4) Physical (Ultrasonication) Physical (Microwave) Biological Biochemical Physiochemical (Steam explosion þ H2SO4)
23 53 e 66 e e e 34 e 3
38% increment Maximum 3 mol H2/mol sugar Maximum yield 2.24 mol H2/mol sugar Maximum yield of 0.0027 mol H2/g straw Maximum yield 1.98 mol H2/mol xylose 20% 1.5 mol H2/mol glucose 20% 96%
[11] [12] [13] [14] [15] [18] [20] [21] [22] [24]
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Table 2 e Advantages and disadvantages of bio-hydrogen production methods on the basis of process configurations. S.No.
Type of process
Advantages
1.
Separate hydrolysis and fermentation
Possible to maintain optimize conditions for both processes separately
2.
Simultaneous saccharification and fermentation
Save the reactor cost, shorten the time duration
3.
Consolidated bioprocessing
High mass transfer rates and conversion efficiency due to chosen cultures
conversion of lignocellulosic biomass to soluble sugars, adopting pretreatment prior to hydrolysis may enhance the hydrogen yield by many folds. However, accumulation of monomeric sugars after hydrolysis is the major bottleneck associated of this approach [28]. To remove this hurdle, the accumulated sugars need to be processed further by employing microorganisms capable of fermenting both hexose and pentose sugars [7]. In this regard, performing hydrolysis and fermentation simultaneously in a single apparatus would be an appropriate solution where the converted soluble sugars can be utilized for fermentation [29].
Simultaneous saccharification and fermentation As discussed above, simultaneous saccharification and fermentation (SSF) is an integrated concept in which saccharification of biomass and fermentation of the soluble sugars is performed simultaneously in a single apparatus. SSF improves the hydrogen production efficiency by mitigating the inhibition imposed accumulating sugars during hydrolysis. Apart from rectifying the operational drawback of SHF, SSF also reduce the operational cost by lowering the operation time and apparatus requirements. However, it requires the adjustment of optimum conditions to work for both processes rather than being specific for the individual processes. Li and Chen [30] carried out SSF of corn straw pretreated with steam explosion. After 72 h of SSF, the process achieved the highest cumulative hydrogen yield of 68 mL/g corn straw. Zhao et al. [29] carried out enzymatic pretreatment of corn stalk with Trichoderma viride prior to SSF and obtained hydrogen yield of 89 mL/g corn straw. These studies were focused on only on investigating the possibilities of using SSF for hydrogen production from agriculture waste. Further, researchers also compared the outcomes of SHF and SSF for biohydrogen production to find the type of method providing desirable results in shorter time and in a more economically viable way. Ibrahim et al. [31] compared the SHF and SSF processes for hydrogen production from oil palm empty fruit bunch using Clostridium acetobutylicum. The observed results revealed 21% higher hydrogen yield for SSF as compared to SHF process. This type of comparative studies revealed that the SSF not only reduce the time and cost of hydrogen production but also enhance the hydrogen yield through less chances of contamination and continuous removal of end-products generated after hydrolysis which can serve as inhibitors [32].
Disadvantages
References
Requirement of two separate reactors which increase the cost as well as time of process, accumulation of hydrolysed soluble sugars Not possible to provide optimum conditions for individual processes and need to employ microbes that can work in similar conditions High energy consumption
[7,28,29]
[29e31]
[33e36]
Consolidated bioprocessing Consolidated bioprocessing (CBP) is the process in which specific microbial consortia is employed to produce enzyme cocktail for simultaneous hydrolysis and conversion of hexoses and pentoses to hydrogen. The presence of chosen and acclimatized microorganisms with ability to degrade cellulose, hemicellulose and produce hydrogen is crucial for success of CBP. Previous studies reported CBP using both mesophiles viz. Clostridium sp., Thermotoga sp. and thermophiles such as Clostridium thermocellum, Caldicellulosiruptor sp. and Thermoanaerobacterium sp. [33e36]. However, thermophiles are better choice owing to their ability to function at higher range of temperatures and thereby avoiding contamination of wide range of mesophiles. Higher mass transfer rates and biomass conversion at elevated temperatures are the added advantages of employing thermophiles for CBP. However lower cell density of microbes is the major drawback by which thermophillic CBP suffers. To counter this disadvantage, membrane reactors may be utilized to maintain higher concentration of microbes for continuous conversion of biomass to hydrogen [7]. Moreover, energy consumption pertaining to maintain high temperature is also need to be taken into account during energy and cost benefits analysis.
Types of fermentation process: photo and dark Bio hydrogen production from lignocellulosic biomass can be achieved via biological route encompassing the methods of DF and PF [37]. PF is the process in which organic acids are used as substrate by purple non-sulphur (PNS) photo heterotrophic microorganisms to produce hydrogen and carbon dioxide in the presence of light [38]. On the other hand, the DF is performed under anaerobic conditions and is independent of light. The DF mediated by anaerobic microorganisms results in production of volatile fatty acids (VFAs) viz. acetic acid, propionic acid, butyric acid etc. along with hydrogen [39]. The hydrogen yield attained after fermentation depends upon the adopted metabolic route, the type of microbial strain, substrate and the fermentation conditions. The microorganisms working in the DF and PF are reported to work with different enzyme systems and follow entirely different metabolic pathways for bio-hydrogen production.
Please cite this article as: Yadav M et al., Lignocellulose to bio-hydrogen: An overview on recent developments, International Journal of Hydrogen Energy, https://doi.org/10.1016/j.ijhydene.2019.10.027
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The DF requires a wide range of hydrolytic and hydrogenease enzymes to convert the organic matter into VFAs and hydrogen [40]. On the other hand, the activity of nitrogenase enzyme present in the cell membrane of PNS bacteria is crucial to perform the PF process [40].
Recent developments in technologies to improve hydrogen production from biomass Reactor configuration Reactor is the primary requirement for carrying out the fermentation of lignocellulosic biomass and its configurational aspects have direct influence on the process run [41]. Appropriate design of reactor is crucial for smooth operation of fermentation process. Khan and Kana [42] designed an innovative baffled bioreactor having a support matrix for improved cell immobilization. Appropriate mixing of substrate in reactor was ensured for enhancing the interaction between microbial cells and substrate. The outcomes of fermentation revealed 31% higher hydrogen yield in novel baffled reactor in comparison to standard fermentation flask. The study established the importance of appropriate mixing and cell immobilization to enhance the substrate and microbe’s interaction. Apart from mixing, the separation of liquid, solid and gas is also critical for stable hydrogen production through continuously removing and collecting the produced hydrogen gas from the reactor [43,44]. For achieving better biomass loading, various types of carrier material may also be used to provide a structured bed for biomass attachment [46,47]. Anzola - Rojas and Zaiat [46] explored three different types of carrier material (polyurethane foam, low density polyethylene and ceramic) for biomass attachment in anaerobic down-flow structured-bed reactor. Though ceramic provided better biomass loading, however, the hydrogen production was higher in polyethylene and polyurethane. The hydrogen production rate was hampered due to inefficient mixing and inadequate flow in reactor with ceramic material as carrier. Moreover, the computational simulation may also be adopted for better controlling and monitoring of process parameters during the scale up process [43]. Zhang et al. [45] attempted to integrate the DF and PF using corn stover as substrate for bio-hydrogen production in a pilot scale reactor. Fu et al. [48] incorporated a light guiding plate serving as light guider for microbial biofilm inside a biofilm photo bioreactor. The SiO2/chitosan modified light guide plate was observed to be most efficient for generation of microbial biofilms which resulted in significantly higher bio-hydrogen production.
Supports for augmenting microbial immobilization Adequate microbial cell immobilization is crucial to ensure maximum utilization of lignocellulosic biomass for its conversion in bio-hydrogen along with longer run of the process [49]. The major cell immobilization techniques explored in past decade are attachment-based, adsorption-based, encapsulation based, polymer based and immobilization through nanoparticles. These techniques have been explored
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extensively for successful bio-hydrogen production and optimization of the parameters including cell loading, pH, temperature, mass transfer coefficient, immobilized biomass ratio, supplements, support materials type etc. [49]. The support material type has a significant role in influencing the behavior of cell immobilization and the properties of attached biomass [50]. Support materials can be made up of polyurethane, polyethylene, expanded clay and activated carbon etc. which may have different impact on microbial metabolism as well as the qualitative and quantitative aspects of microbial community immobilized. Li et al. [51] designed a novel photothermal support material consisting of GeO2, SiO2, Chitosan Medium, LaB6 which was investigated for immobilizing photosynthetic bacterial cells. The outcomes of the study revealed the higher efficiency of the novel designed materials resulting in 4-fold increase in bio hydrogen production along with enhanced growth rate of biofilm as compared to experiment having no support material. Apart from polymers, nanoparticles/nanorods can also be used for the purpose of microbial cell immobilization [52,53]. Due to increased surface area, nanoparticles addition enhances the cell immobilization during fermentation which results in significant increase in bio-hydrogen production as reported by studies regarding addition of hematite, maghemite nanoparticles, ferrihydrite nanorods [52e54]. Pansook et al. [55] employed alginate beads for immobilization of Aphanothece halophytica cells for bio-hydrogen production. The result revealed higher bio-hydrogen production by immobilized cells as compared to the reactor having free cells. However, successful usage of nanoparticles for cell immobilization needs to be optimized for determining the appropriate size of nanoparticles. Moreover, addition of nanoparticles beyond a certain concentration can cause toxicity which would adversely affect the viability of microbes as well as the fermentation process. Therefore, the concentration for nanoparticle addition into fermentation media also needs to be investigated for manipulating the cell immobilization to achieve desirable outcomes.
Novel microbial strains Over the years, a wide range of microbes have been explored to examine their efficiency for biomass to hydrogen conversion. The possibility of discovering new microbial strain with increased cellulolytic and hemi cellulolytic ability was always existed as a major topic of research in field of bio-hydrogen production through lignocellulosic biomass. The hydrogen producing microorganisms can be classified in different categories of photosynthetic bacteria, obligate and facultative anaerobes, aerobes and photoautotrophic bacteria [56]. The hunt for novel microbial strains with increased biomass to hydrogen conversion capabilities also gained immense interest in the recent years. A number of studies reported in past two years focused on exploring novel microbial strains for bio-hydrogen production such as Escherichia coli [57], Clostridium beijerinskii [58], Rhodopseudomonas palustris [59,60], Thermoanaerobacterium sp. strain PSU-2 [61], Rhodobacter sphaeroides [62], Streptomyces rubiginosus (SM16) [63], Clostridium pasteurianum [64], Enterobacter aerogenes [65]. Trchounian et al. [40] demonstrated the
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choice of microbial strains for bio-hydrogen production as a sine qua non requirement for sustaining the biochemical conversion. The study emphasized on the role of nitrogenases and hydrogenases enzymes for viable kinetic of biomass to hydrogen production through photo and dark fermentative bacteria. An interesting report on biohythane (mixture of methane and hydrogen) production was published by Abreu et al. [66] employing garden waste as substrate. The study combined the processes of DF and anaerobic digestion in which Caldicellulosiruptor saccharolyticus and Thermotoga maritima were used for biohydrogen production. Furthermore, the co-culture of C. saccharolyticus and Caldicellulosiruptor bescii resulted in higher production of bio-hydrogen as compared to co-culture T. maritima and C. saccharolyticus. A new bio-hydrogen producing strain of Enterococcus faecium was isolated from gamma irradiated sludge [67]. Immobilizing the strain on polyvinyl alcohol-Na alginate resulted in further improvement in biohydrogen yield. Srivastava et al. [68] employed Clostridium pasteurianum for DF of enzymatically pretreated rice straw resulting in maximum hydrogen production rate after (23.96 mL/L.h) 96 h. For improvement of bio-hydrogen yield, the optimization of the process is also required to provide nest suitable conditions to microbe. The statistical tools and mathematical models may be employed for this purpose. The hydrogen production process using a novel strain Enterococcus faecium INET2 was optimized recently via response surface methodology which studied the multiple combinations of temperature, pH, substrate concentration and inoculum size at different levels [69]. These types of studies are required to study both the individual and interactive impact of parameters on fermentation process and hydrogen yield.
Mitigation of inhibitory effects Though the pretreatment methods are adopted to enhance the degradability of lignocellulosic biomass leading to improved conversion to hydrogen. However, a number of pretreatment methods including chemical and thermal methods result in generation of certain compounds that impose inhibitory effects on the fermentation process. Furans and phenolic compounds are acknowledged to have the most detrimental impact over the bio-hydrogen production process [23]. Furfural and 5-hydroxymethylfurfural produced from pretreatment of cellulose and hemicellulose are reported to adversely impact the kinetics of microbial metabolism during the fermentation processes. The inhibitory mechanism of these compounds includes reduction in growth rate and permeability of microbial cells as well as increased formation of reactive oxygen species [23]. The quantity and action level of inhibitory compounds majorly depend upon the type and severity of pretreatment, chemical composition of biomass and the microbes employed to mediate the bio-hydrogen production process [70,71]. The primary inhibitory mechanism involves the permeation of unionized weak acids through the cell wall of microbes and reduce the pH within cell environment leading to hostile conditions for biohydrogen synthesizing microbes. Examining the impact of
furfural concentration on the bio-hydrogen yield revealed that the bio-hydrogen yield declines as the furfural concentration increases. A decline of 21, 29 and 62% was reported for 1, 2 and 4 g/L concentrations of furfural respectively [72]. Interestingly, Akobi et al. [71] achieved increase in bio-hydrogen yield upto 1 g/L concentration of furfural. Increasing the furfural concentration beyond 1 g/L resulted in the decline of biohydrogen production. To mitigate these inhibitory effects, a number of detoxification methods are employed including biological and physiochemical approaches viz. evaporation, flocculation, adsorption on activated carbon, use of enzymes and ion exchange resins.
Integrated fermentations In the recent years, an increasing trend of studies combining fermentation schemes with other processes has been observed to attain higher biomass to hydrogen conversion. For instance, biohythane production involved the combination of fermentation with anaerobic digestion [66]. Further, many recent studies combined PF and DF schemes to improve the efficacy of the bio-hydrogen production process [73,74]. Marone et al. [75] combined the DF process with bio catalyzed electrolytic processes. The most intensively explored integrated fermentation scheme includes coupling of DF and PFs. As shown in Fig. 2, VFAs such as acetic acid, propionic acid and butyric acid present in the effluent of DF, may be employed as a substrate for PF to attain extra hydrogen [76]. Therefore, integrating these two fermentation process results in more efficient biohydrogen production with higher substrate utilization and hydrogen yield. While single step integration allows utilization of DF effluent utilization, the two-stage coupling of DF and PF processes enables the effective optimization and regulation of growth conditions for both processes separately [74,76]. However, the two-stage fermentation integration scheme requires two separate bio-reactors to carry out both type of fermentations and thereby, increases the implementation cost (Fig. 3). The necessity of pretreating DF effluents in some cases further complicates the integrated scheme and its economic aspects [76]. Therefore, the potential to utilize the organic matter to utmost extent and attain complete conversion makes the integrated single stage fermentation scheme ideal and most desirable strategy. Lu and Lee [77] carried out single stage integrated fermentation by employing Clostridium cellulovorans for cellulose degradation during DF and photosynthetic Rhodopseudomonas palustris for PF. The study reported balance of pH by Rhodopseudomonas palustris through consumption of generated VFAs which in turn boosted the cellulose conversion by Clostridium cellulovorans. The overall mutual interaction between both microbes resulted in more competent bio-hydrogen generation process. Similar mutual interaction was observed with coculture of Clostridium butyricum and Rhodobacter sphaeroides and a 3-fold higher bio-hydrogen yield was attained as compared to the monoculture of Clostridium butyricum [78]. Zagrodnik and Łaniecki [79] employed Clostridium acetobutylicum and Rhodobacter sphaeroides for single step DF and PF of
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Fig. 2 e Dark and photo fermentation processes linked through organic acids. corn starch and observed 23% increase in bio-hydrogen yield as compared to the yield of DF alone. The integrated fermentation process carried out at optimum pH 7 with the same co-culture resulted in stable microbial interaction leading to 2.5-fold increase in hydrogen yield [80]. Biohydrogen production from palm oil mill effluent through two stage successive DF and PF resulted in approximately 3.9fold rise in hydrogen production due to the activity of Clostridium butyricum LS2 and Rhodopseudomonas palustris during first and second stage respectively [81]. Zhang et al. [82] carried out two stage sequential fermentation of mediated by Rhodopseudomonas palustris and Clostridium butyricum for fermentation of Platanus orientalis leaves. The fermentation effluent was further used for methane production and resulted in higher biomass conversion efficiency of anaerobic treatment plants. Though, the integration of fermentation processes has potential to achieve higher bio-hydrogen yields; however, the integration method requires to be optimized to attain the best as well as balanced conditions suitable for the individual processes combined during integration. The optimization
needs to be done in terms of culture conditions, pH, temperature, substrate concentration etc. Hitit et al. [74] attempted to optimize the culture conditions to meet the different growth requirements of dark and photo fermenting bacteria in single stage. Buffer and substrate concentrations as well as the ratio of Clostridium butyricum and Rhodopseudomonas palustris was optimized using response surface methodology to achieve the maximum hydrogen production. Highest hydrogen yield was obtained at 50 mM buffer concentration and 15 g/L substrate concentration with microbial ratio of 3 growing at 30 C under illumination of 40 W m2 light intensity. Table 3 summarizes the prominent studies regarding the integration of PF and DF in single stage and two stages.
Metal additives for improving catalytic activity Catalysts play an important role in transforming reaction kinetics leading to more efficient conversion process with high turnover. Improving the properties of catalysts itself result in further boost in end product yield owing to the better
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Fig. 3 e Single stage and two stage integrated fermentation schemes. Here, DFM: dark fermentation microbes; PFM: photo fermentation microbes; VFA: volatile fatty acids.
performance of catalytic conversion. A wide range of metals nanoparticles, zeolites, ionic liquids etc. can be used as catalysts or can be incorporated in fermentation process as additives to improve the activity of targeted bio-catalysts viz. hydrogenase or nitrogenase. Nanoparticles proved to be the most favored choice of research for catalyzing and improving the bio-hydrogen production process in the recent studies (Table 4) [52,64,88]. The presence of nanoparticles enhances the conductivity effects leading to efficient movement and exchange of electrons within the periplasm. Ferrous ions are specifically favored as additives since it is present in the active sites of hydrogenases as well as ferredoxins [89]. This resulted in enhanced electron transfer process mediated by ferredoxins to facilitate the mechanism of ferredoxin oxidoreductase and hydrogenase enzymes involved in carbohydrate degradation during fermentation
[64]. The stability of these metal-based nanoparticles further increases their desirability as catalysts for improving biohydrogen as well as biomethane and ethanol production processes. Taherdanak et al. [88] investigated the influence of Fe and Ni nanoparticles on the bio-hydrogen production from glucose through DF process. The observations revealed highest hydrogen yield for the process employing Niþ2 as catalyst as compared to Feþ2 nanocatalysts. Hsieh et al. [64] compared the effects of adding Fe and TiO2 nanoparticles as catalysts. The study reported significant improvement in biohydrogen yield using Fe nanocatalyst, while no substantial improvement was observed after adding TiO2 as catalyst. Lin et al. [90] observed improved bio-hydrogen yield after addition of Fe2O3 nanoparticles as catalyst. The outcomes were in line with previously published study reporting increased hydrogen yield owing to the action of Fe2O3 nanocatalyst [91]. Engliman
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Table 3 e Integrative fermentation schemes for bio-hydrogen production. S.No. Single 1. 2. 3. 4. 5. 6.
Substrate
stage integration Cellulose Starch Glucose Corn starch Corn starch Potato juice and glucose Two stage integration 7. Potato stem peel 8. Beet molasses 9. Cassava starch 10. Cheese whey 11. Palm oil mill effluent 12. Platanus Orientalis leaves
Microorganisms Clostridium Clostridium Clostridium Clostridium Clostridium Clostridium
cellulovorans, Rhodopseudomonas palustris butyricum and Rhodobacter sphaeroides acetobutylicum and Rhodobacter sphaeroides acetobutylicum and Rhodobacter sphaeroides acetobutylicum and Rhodobacter sphaeroides butyricum Rhodopseudomonas palustris
Caldicelluluiruptor saccharolyticus, Rhodobacter capsulatus Caldicelluluiruptor saccharolyticus, Rhodobacter capsulatus Mixed culture for DF, Rhodopseudomonas palustris for PF E. aerogenes and Rhodopseudomonas BHU 01 Clostridium butyricum LS2 and Rhodopseudomonas palustris Rhodopseudomonas palustris, Clostridium butyricum
Hydrogen yield
References
3-fold increase in hydrogen yield 3-fold increase in hydrogen yield 23% increase in bio-hydrogen yield 2.5-fold increase in bio-hydrogen yield 6.4 ± 1.3 mol/mol glucose hydrogen yield
[77] [78] [83] [79] [80] [74]
5.81 mol/mol hexose hydrogen yield 13.7 mol/mol hexose hydrogen yield 0.035 mol/g starch hydrogen yield 2.04 mol/mol lactose hydrogen yield 3.9-fold increase in hydrogen yield e
[84] [85] [86] [87] [81] [82]
et al. [92] achieved 53% increase in hydrogen yield after addition of Iron (II) oxide nanoparticles as biocatalyst for thermophillic fermentation process carried out by mixed culture of microbes. Liu et al. [93] investigated and compared the effect of three types of nanoparticles (ZnO, TiO2 and SiC) on the PF of beef extract and other substrates including sodium glutamate and sodium acetate by Rhodopseudomonas sp. The outcomes revealed maximum hydrogen yield for the fermentation involving SiC nanoparticles (200 mg/L) as catalyst. The above-mentioned studies indicates the potential of metal nanoparticles for improving bio-hydrogen yield through fermentation process. Nanoparticle addition not only improves the metabolic action of microbes but also aids in enhancing the electron transfer during the fermentation reactions pertaining to the high surface area and quantum impact of nanoparticles [98]. However, the contradictory patterns of influence for the same type of nanoparticles in different study raise the concern over the consistency of research outcomes. This challenge needs to be addressed through the determination of ideal size and concentrations of nano catalysts to be added in the fermentation reactor to achieve positive influence on the bio-hydrogen yield.
metal centers. The three types of hydrogenases are e Fe, FeFe and NiFe hydrogenase. Though, FeFe hydrogenase can both mediate the reduction of Hþ and oxidation of H2, it is mainly involved in the hydrogen production process [102]. On the other hand, NiFe hydrogenase is primarily involved in hydrogen consumption process. The hydrogen production reaction catalyzed by hydrogenase may be represented as follows:
Hydrogen production pathways in microorganisms and the enzyme system
Genetic engineering
The pathway of bio-hydrogen production differs for photo and DF processes. During PF, the purple non-sulphur photosynthetic bacteria generate ATP and reduce ferredoxins (Fd) through reverse electron flow in presence of light and anaerobic conditions [99]. The organic compounds provided as substrate act as electron donor. The hydrogen ions are catalyzed by either hydrogenase or nitrogenase in the presence of light to produce hydrogen gas [100]. On the other hand, DF harvest energy from microbial oxidation process of organic substrates such as glycolysis. DF results into varying metabolic products depending upon the microbes involved in the process as well as the substrate, nutrients, pH, temperature etc. [99,101]. The hydrogenase enzyme involved in the fermentation process can be grouped in three categories on the basis of the
2Fdþ þ 2Hþ ————— 2Fd2þ þ H2 [ The nitrogenase enzyme which is well known for nitrogen fixation, catalyzes the conversion of nitrogen to ammonia. The hydrogen is produced in this reaction as a by-product. The reaction of nitrogen is as follows: N2 þ 2Hþ þ2e ————— 2NH3 þ H2 [ The nitrogenase enzyme consists of three metal clusters including P cluster, FeS cluster and FeMo cluster. The FeS cluster aids in transferring electron to FeMo and P cluster which actively participates in the reduction of nitrogen to ammonia [99].
Possessing the ability to manipulate the metabolic pathways of hydrogen producing microbial strains, genetic engineering has great potential to augment the competence of biomass to hydrogen conversion process and thereby the hydrogen yield. The theoretical potential of hydrogen yield by using lignocellulosic biomass may be attained by improved modifications in the existing metabolism of dark and photo fermenting organisms or by discovering the new pathways. The positive impact on hydrogen yield through genetic manipulation may be achieved by developing more efficient enzyme machinery, maximizing substrate utilization by enzymes, downregulation of genes and transcription factors involved in the processes competing or interfering with hydrogen production. Despite the bright prospects, this area of research remained largely unexplored with only a few published reports in past decade. Wu et al. [103] employed genetically
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Table 4 e Nanocatalyst addition during fermentation for hydrogen production. S.No
Substrate
Microorganisms
Nanoparticles type
Concentration (mg/L)
Hydrogen Yield
2.54 mol/mol of glucose 2.33 mol/mol of glucose
1.
Glucose
Mixed culture
Nickel
5.67
2.
Glucose
Iron oxide nanoparticles
175
3.
Starch
Clostridium acetobutylicum NCIM 2337 Mixed culture
Fe0 and Ni0
37.5
4.
Mixed culture
Hematite
200
5.
Distillery waste water Glucose
Fe and TiO2
50
6.
Glucose
Clostridium pasteurianum Mixed culture
Iron (II) oxide
…
7.
Beef extract, sodium acetate, l-cysteine, sodium glutamate and other components
Rhodopseudomonas sp. A7
TiO2, SiC and ZnO
ZnO (100), SiC (200), TiO2 (300)
modified Klebsiella oxytoca HP1 by inactivating adhE gene and achieved improved hydrogen production after two step DF and PF of sugarcane bagasse. Deletion of lactate dehydrogenase (ldh) gene in Caldicellulosiruptor bescii led to divert the electron transfer from lactate production pathway to hydrogen production [104]. The mutant strain with deleted ldh gene showcased higher hydrogen production. The formate hydrogen lyase (FHL) gene system is also targeted for genetic manipulation as it is involved in maturation of hydrogenases. FHLA gene is the most important gene in this system which activates the FHL system by promoting the synthesis of other component of system such as FDH-H [105]. On the other hand, hycA gene encode for the HYCA suppressor protein which stop the FHL transcription through binding with FHLA and promotes the expression of uptake hydrogenases. Interstingly, Kim et al. [106] discovered an upswing in FHL activity by deleting the hycA gene resulting in increased hydrogen yield. Further deletion of hya and hyb genes (uptake hydrogenase genes) led to 1.2-fold increase in hydrogen yield. In facultative anaerobes, both FHL and pyruvate formate lyase (PFL) assist in hydrogen production process. Madeda et al. [107] reported 41 fold increase in hydrogen yield after cloning the hoxEFUYH gene found in Cyanobacterium synechocystis encoding for the expression of bidirectional hydrogenase and transferring it into E. coli. The other method for improving bio-hydrogen yield is to knock out or suppress the genes coding for uptake hydrogenases. The genetic manipulations can be achieved through chemical mutagenesis as well as exposing the strains to ultraviolet rays [108]. Undesirable phenotypes may be expressed sometimes due to genetic modifications. However, it is noteworthy that the outcomes of employing these methods of genetic manipulations may not always be positive. Though the few reported studies clearly achieved a significant upsurge in hydrogen yield owing to the genetic manipulation of fermenting microbes. However, the stability of newly found phenotypes, genetic expression as well as the alternate
Impact on hydrogen production
Reference
23% increase
[94]
33% increase
[95]
0.0062 mol H2/g- 200% increase VS 8.83 mmol/g COD 62% increase
[96]
2.1 mol/mol hexose 1.92 mol/mol glucose 2.99 mol/mol acetate for SiC
25% increase
[64]
53% increase
[92]
18.6% increase by SiC addition
[93]
[97]
metabolic pathways are required to be tested through more up scaled studies beyond the laboratory trials.
Conclusion The review of the cutting-edge researches carried out in recent years reveal the possibilities of improvement in the existing fermentation technologies as well as the necessity to divulge into the untapped and poorly explored research arenas for improving the bio-hydrogen yield. The major observation of the review can be concluded as below: Appropriate pretreatment methods can be employed to reduce the recalcitrance of biomass structural components and enhance the degradability of biomass for hydrogen production. Further addition of nano catalysts, cell immobilization, use of more efficient novel strains etc. may be used to improve the biomass to hydrogen conversion reactions. The integration schemes of DF and PF processes have been emerged as the most intensively explored research area in past three years with a large number of published reports and proved to be an appealing option for enhanced hydrogen production. The genetic engineering approaches may provide many folds increase in bio-hydrogen production through the manipulation in the genetic makeup of hydrogen producing bacteria.
Future perspectives Though the research in bio-hydrogen production are in continuous drift, however, some of the necessary concerns need to be addressed before taking up the novel technology advancements from lab scale to commercial scale. Feasibility study of potential integrated fermentation schemes through
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international journal of hydrogen energy xxx (xxxx) xxx
modelling and simulation before proceeding for up scaling. Optimization of the key process parameters involved in the utilization of new strategies and techniques for bio-hydrogen yield augmentation. Novel strain with higher biomass to hydrogen conversion efficiency can be prepared by manipulating the key genes and transcriptional factors involved in the process. For this, better understanding of the enzyme mechanism and metabolism pathways is crucial. The major focus needs to be put on FHL and PFL system and developing alternative pathways by using gene knockout techniques. The proteomics approach may be helpful to study the role of different proteins involved in hydrogen production as well as identifying the key factors that need to be targeted.
Authors contribution MY and KP contributed equally in writing the manuscript as well as preparing the figures and tables. VV provided scientific insights and technical guidance during manuscript writing.
Acknowledgement MY and KP would like to acknowledge Malaviya National Institute of Technology Jaipur to provide the fellowships and infrastructure. VV acknowledges Department of Biotechnology, Ministry of Science and Technology, Government of India for providing financial support through Ramalingaswami Re-Entry fellowship (No. BT/RLF/Reentry/04/ 2013).
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Available online at www.sciencedirect.com
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Lignocellulose to bio-hydrogen: An overview on recent developments Monika Yadav, Kunwar Paritosh, Vivekanand Vivekanand* Centre for Energy and Environment, Malaviya National Institute of Technology Jaipur, JLN Marg, Jaipur, Rajasthan, 302017, India
highlights Lignocellulose to biohydrogen production has been reviewed. Pretreatment strategies to improve biohydrogen have been discussed. Recent trends in research for biomass to hydrogen conversion have been summarized.
article info
abstract
Article history:
Production of hydrogen from lignocellulosic biomass using biological methods is an
Received 25 April 2019
alluring approach to generate green and clean energy. However, the challenges levied by
Received in revised form
structural and compositional aspects of lignocellulosic biomass block the way to harness
27 September 2019
their complete energy potential. The review revisits the available methods of pretreatment
Accepted 2 October 2019
to augment the accessibility of carbon source required for microorganism to perform
Available online xxx
biomass to hydrogen conversion. The fermentation methods that have been employed for years for bio-hydrogen production are discussed in brief to provide the background of
Keywords:
biological routes of hydrogen production. The review further highlights the latest research
Lignocellulosic biomass
trends and upgrades in technologies including the identified novel microbial strains,
Pretreatment
reactor configurations, integrated schemes of fermentations, nanocatalysts addition and
Bio-hydrogen
the genetic engineering tactics to enhance the competence of hydrogen producing bacteria.
Dark fermentation
© 2019 Hydrogen Energy Publications LLC. Published by Elsevier Ltd. All rights reserved.
Photo fermentation
Introduction Developing countries like India, are struggling to have clean energy sources to fulfil gross energy demand [1]. Conventional sources such as coal and petroleum are exhausting day by day and search for non-conventional alternatives is stressed for uninterrupted supply of energy. Renewable sources (viz. Solar, wind, biomass, ocean and small hydro), on the other hand, may be helpful to meet the gross energy demand and may
create a sustainable cum circular economy [2]. However, in the context of transportation fuel from renewable sources, only biomass-based fuels may replace the petroleum-based transportation industry as solar and wind are intended to other energy applications. In transportation sector, hydrogen is now a days considered as a potential fuel. Automobile companies in different countries are putting effort for hydrogen driven vehicle to curb environmental pollution and degradation. Most of the world-renowned companies in vehicle are shifting towards hydrogen-based
* Corresponding author. E-mail address: [email protected] (V. Vivekanand). https://doi.org/10.1016/j.ijhydene.2019.10.027 0360-3199/© 2019 Hydrogen Energy Publications LLC. Published by Elsevier Ltd. All rights reserved. Please cite this article as: Yadav M et al., Lignocellulose to bio-hydrogen: An overview on recent developments, International Journal of Hydrogen Energy, https://doi.org/10.1016/j.ijhydene.2019.10.027
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economy in terms of transportation fuel. The burning of hydrogen as a fuel only releases water vapour as coproduct which makes it attractive option for sustainable approach. Also, 1 g of hydrogen possess around 142 kJ of energy which is further alluring for fuel application [3]. However, the world needs alternative for hydrogen production as most of the hydrogen is being produced from nonrenewable sources. The carbon rich non-biodegradable matters exploited for production of hydrogen are non-desirable option for sustainable city, society and economy. Hence, the focus needs to be shifted on degradable and renewable resources for hydrogen production. There are various ways by which bio-hydrogen may be produced. Some of notable processes are dark fermentation (DF), photo fermentation (PF), bio photolysis and indirect bio photolysis. From all the processes to produce hydrogen, DF is reported to be an efficient one as it does not require additional energy to operate [3]. However, the major obstructions associated with DF for hydrogen production are high operational cost and production efficiency. Being a carbon neutral substrate, lignocellulosic biomass is an attractive feedstock for production of bio-hydrogen. Since the food or fuel debate dominates the use of first-generation biomass for fuel production, employing non-edible second generation biomass is recommended [4]. Second generation biomass is consisting of lignin rich feedstock such as stalks, stover and residues of crops, forestry waste, wood chips and clippings, twigs and fallen leaves. The second-generation biomass is rich in various fermentable sugars (pentoses and hexoses) along with the existence of lignin. These fermentable polysaccharide sugar such as hexose and pentose could be advantageous for bio-hydrogen production [5]. However, lignin, a polymer, encircles the physical structure of lignocellulosic biomass, the holocellulose (cellulose þ hemicellulose) which makes its hydrolysis an energy intense process and tedious. To expose the fermentable sugar existing in the lignocellulose for hydrolysis, pretreatment is required. The next section of the review
summarizes the structural arrangement of biomass and the pretreatment approaches to improve its degradability for hydrogen production. The review further confers the fermentation approaches and the recent trends in research and technologies to enhance the bio-hydrogen yield in the subsequent sections.
Lignocellulosic biomass structure, pretreatment and inhibitions Structure of lignocellulosic biomass Lignocelluloses are the most abundant raw material on earth [6]. The lignocellulosic biomass comprises of wood (hardwood and softwood), grass, leaves, agricultural stubble, crop residues, forestry waste and organic fraction of municipal solid waste. The production of lignocellulosic biomass is stated to be around 0.22 trillion tonnes [7]. The lignocellulosic biomass is composed of cellulose and hemicellulose collectively known as holocellulose (Fig. 1). This combination of cellulose and hemicellulose is encircled with a recalcitrant material, lignin. For bio-hydrogen production, holocellulose is needed as it consists of C6 and C5 linear and branched polysaccharides. For example, glucose, mannose, xylose and arabinose are common example of sugar present in lignocellulosic biomass. However, lignin shows recalcitrant nature in bio-hydrogen production and decreases the conversion efficiency and effectiveness of lignocellulosic biomass into bio-hydrogen. The sturdy nature of lignin is responsible for low performance of direct conversion of lignocellulosic biomass to biohydrogen.
Cellulose Cellulose is the most ample and highly stable polymer in nature. The lignocellulosic biomass comprises of nearly 40e45% of cellulose having both crystalline and amorphous structure.
Fig. 1 e Structural arrangement of plant cell wall. Please cite this article as: Yadav M et al., Lignocellulose to bio-hydrogen: An overview on recent developments, International Journal of Hydrogen Energy, https://doi.org/10.1016/j.ijhydene.2019.10.027
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Most of the cellulose is well assembled and crystalline in nature while the rest of it is amorphous. Amorphous cellulose is preferred for degradation over crystalline cellulose as crystallinity makes the degradation difficult [4]. The bonds present in cellulose molecules are hydrogen and covalent with Vander-wall force. Hydrogen bonding present in cellulose is responsible for its straight nature whereas interchain hydrogen bonds presents in the cellulose decides the structural arrangement. Inter and intramolecular hydrogen bonds existing in the cellulose makes it rigid in nature. This rigid nature of cellulose opposes any solubilization in organic solvent and shows resistant to it.
Hemicellulose Hemicellulose which is the second most abundant polymer in nature, shares around 30% of lignocellulosic biomass. The molecular weight of hemicellulose is around 30000 g/mol. Unlike cellulose, hemicellulose is made of heterogeneous polymers which mainly consist of lateral chains of various sugars such as pentoses, hexoses and uronic acids. Composition of hemicellulose varies in lignocellulosic biomass. Grass and agricultural stubbles are mainly consisting of xylan while glucomannan is main constituent of softwoods. Extraction of xylan is responsive to mild acid or alkali treatment whereas glucomannan requires strong environment of alkali [6]. It was also reported that hemicellulose is very sensitive to thermochemical treatment as compared to cellulose and lignin [3]. In lignocellulosic biomass, hemicellulose covers cellulose from outside and to expose cellulose for enzymatic actions, 50% of hemicellulose should be displaced. However, if the disruption of hemicellulose is severe and not controlled, degradation products of hemicellulose such as furfural and hydroxymethyl furfural (5 e HMF) may hamper the biomass degradation process. Furthermore, severity condition of biomass treatment may be compromised to dodge the generation of inhibiting by-product of hemicellulose degradationand to increase the sugar availability [6].
Lignin After cellulose and hemicellulose, lignin is the third most abundant polymer in nature. Cross linkages of phenolic monomers make lignin a complex and large molecule. The phenolic monomers which make impermeable structure of lignin are coniferyl, sinapyl and coumaryl alcohols [8]. These phenolic monomers are linked together by alkyl-alkyl, arylalkyl and aryl e aryl ether bonds [6]. The complex and sturdy nature of lignin acts as a barrier to the plant cell wall degradation and oxidative stress caused by microbes. Generally, the grasses are reported to have lower percentage of lignin while softwood has higher percentage. Lignin often makes lignin-cellulose complex (LCC) with cellulose microfibrils which makes biomass deterrent to the microbial activity and hydrolysis. The percentage of lignin in lignocellulosic biomass mainly depends on the origin and type of the biomass [8].
Extractives Extractives are chemicals that are non-polymeric part of lignocellulosic biomass which can be extracted with the help of solvents [7]. Solvents such as acetone, water, toluene,
3
hexane etc. may be employed for extraction of extractives. In general, biomass consists various extractives such as proteins, pectin, waxes, essential oils, phenolics, flavonoids etc. Based on solubility, extractives may be classified as water soluble, ether soluble and toluene/ethanol soluble extractives. Bark of the hardwood consists phenolic extractives. These phenolic extractives protect the plant cell wall against microbial attack.
Pretreatment of lignocellulosic biomass Pretreatment of lignocellulosic biomass is intended for enhanced hydrolysis rate and a smoother process stability for hydrogen production. Pretreatment helps to alleviate the enzymatic activity by breaking the lignocellulosic structure and rupturing the lignin cellulose complex [9]. The plant cell wall lysis is often increased by delignification of biomass which consecutively boosts the increase the hydrolysis.
Chemical pretreatment Use of chemicals and reagents for removing the lignin barrier in lignocellulosic biomass is called as chemical pretreatment. Alkalis, acids, organic solvents, ionic liquids and chlorides of metal ions are commonly employed chemicals for pretreatment of biomass. Alkalis and acid pretreatment are most explored and economical pretreatment strategy among all the chemical pretreatment. Alkalis generally targets the ester bonding between the lignin and hemicellulose which help to solubilize the hemicellulose as well as expose the cellulose for hydrolysis. NaOH, KOH and CaOH2 are the most commonly used alkalis for pretreatment of lignocellulosic biomass to produce bio-hydrogen. However, higher concentration of alkalis may dissolve substantial hemicellulose which might be a loss of useful product for hydrolysis [10]. Lime, on the other hand, is a safe and economically competitive alternative to sodium hydroxide. Cao et al. [11] employed lime to pretreat corn stalk for bio-hydrogen production. It was reported that 38% higher bio-hydrogen yield was obtaines as compared to untreated corn stalk at the loading of 0.1 g of lime for 1 g of corn stalk. Also, the characterization of corn stalk showed that 23% of lignin was removed. It was also reported that kiln technique may help to recover the lime which could be an economical and effective approach for enhanced bio-hydrogen production. Pretreatment of sweet sorghum bagasse with sodium hydroxide for enhanced bio-hydrogen yield was performed by Panagiotopoulos et al. [12]. It was observed that at 10% of NaOH (w/w of dry matter) showed maximum delignification (46%) and maximum biohydrogen yield (10.2 mmol/(L h)). For acid pretreatment of lignocellulosic biomass, Sulphuric acid, hydrochloric acid, boric acid and nitric acid are common examples. In acid pretreatment, lignin gets solubilized which expose the holocellulose for better and improved hydrolysis. The degree of solubilization of lignin depends on the strength of acid whether the acid is dilute or strong. Cao et al. [13] employed dilute hydrochloric acid for the pretreatment of corn stover for enhance bio-hydrogen production. The H2SO4 concentration was selected as 0.25e4% v/v for the pretreatment of corn stover at 121 C for 30e180 min.
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As per results, 1.69% of acid showed maximum hydrogen yield (3305 ml H2/L medium) at the time of 117 min. Unlike separate alkali and acid pretreatment of lignocellulosic biomass, combined ammonia and dilute acid pretreatment of rice straw was attempted by Nguyen et al. [14]. The digestibility of rice straw was increased up to 85% in the case of combined pretreatment (10% ammonia and 1% dilute sulphuric acid). It was also reported that 72% of glucose and 95% of xylose was converted to bio-hydrogen. Chong et al. [15] studied the effect of acid pretreatment on palm oil fruit brunch for bio-hydrogen production. 6% of sulphuric acid yielded maximum bio-hydrogen which was 690 mL/L medium for palm oil fruit brunch. The sugar production was also increased by 78% with acid pretreatment.
Physical pretreatment Physical pretreatment refers to the use of mechanical instruments to disrupt the tough lignocellulosic structure for accessible holocellulose. Mechanical instruments such as grinder, ball milling, screw press, microwave and sonication are commonly used for physical pretreatment of biomass. These instruments reduce or change the surface area of lignocellulosic biomass making it amenable for digestion and solubilization. Silva et al. [16] reported that yield of glucose was more in case of ball milling pretreatment as compared to steam explosion. Also, the size reduction by physical pretreatment help to reduce the crystallinity of cellulose as crystalline cellulose is less accessible as compared to amorphous one. Zhao et al. [17] reported that ball milling helped to reduce the crystallinity of a e cellulose. One of the drawbacks of physical pretreatment is that the method is energy intense and may distort the equation of net energy gain. It was suggested to combine the physical pretreatment with chemical or biological pretreatment for positive net energy gain [17]. Microwave and sonication use electromagnetic wave to disrupt the ester and ether linkages in lignin cellulose complex. Leano et al. [18] employed ultrasonication for the pretreatment of palm oil mill effluent in bio-hydrogen production. Results showed that the bio-hydrogen productivity and COD removal was 38 and 20% more as compared to untreated one at ultrasonication dose of 195 J/ml. The maximum biohydrogen produced was 0.7 mmol H2/g COD. It was also reported that lower dose of ultrasonic waves (91 J/ml) showed negligible effect on biohydrogen production but increasing the frequency showed positive results. Apart from ultrasonication, microwave assisted acid pretreatment of corn stover for improved biohydrogen production was performed by Liu and Cheng [19]. A microwave with rated power 700 W was selected for acid assisted pretreatment. The time of microwave pretreatment was selected as 5, 15, 30, 45, 60 and 90 min. Results showed that maximum hydrogen production was observed at 45 min which was 1.53 mol H2/mol glucose. Coupling the microwave pretreatment with other pretreatment may have fruitful impact on biohydrogen production. Also, coupling acid assisted microwave pretreatment has been reported to have short pretreatment duration, higher sugar yield and no or less inhibitor formation [20]. Palm oil trunk was pretreated with microwave irradiation (450 W)
assisted with sulphuric acid for improved hydrolysis and it was observed that 1.56% of sulphuric acid (w/v) at 450 W and 7.5 min reaction time in microwave showed maximum hydrolysis of glucose, xylose and arabinose. The yield of glucose, xylose and arabinose was 8.95, 8.29 and 4.57 g/L respectively. Increasing the concentration of sulphuric acid from 1 to 3% w/v showed increment in sugar yield. However, increasing the concentration of sulphuric acid in above reported study did increase the inhibitors as HAc. Maximum HAc (3.97 g/L) as inhibitor was observed at 3% of sulphuric acid (w/v).
Biological and biochemical pretreatment In biological pretreatment, enzymes or microbes perform the depolymerization of lignocellulosic biomass. Enzymes or microbes act as a precursor to the hydrolysis of biomass in biological pretreatment. Fungus is commonly used biological entity to perform biological pretreatment for its exclusive lignolytic and delignification property [4,9]. Fungus such as brown rot, white rot and soft rot are common example of fungal species employed for biological pretreatment. During biological pretreatment with fungus, depolymerization of biomass generally happens outside the plant cell wall due to insolubility of biomass. In this regard, lignolytic enzymes are required in the pretreatment process for efficient lignin disruption. Peroxidase of lignin and manganese and laccase are the enzymes secreted by fungus which are responsible for oxidative stress in lignin. Zhao et al. [21] employed Phanerochaete chrysosporium for pretreatment of corn stalk for biohydrogen production. The corn stalk was pretreated at 29 C for 15 days with Phanerochaete chrysosporium and delignification was reported to be 34%. It was also observed that in pretreated corn stalk enzymatic saccharification was 20% higher as compared to the untreated corn stalk. Though depolymerization of lignin with the help of fungi is reported supportive, selectivity of fungi for lignin degradation is of utter importance to prevent loss of hemicellulose. Enzymes may reduce the time of biological pretreatment process and may provide better delignification. In enzymes, cellulase, endoxylanase, amylase and bromelain are common example for biochemical pretreatment of lignocellulosic me neur et al. [22] performed biochemical prebiomass. Que treatment by adding exogenous enzymes in fermentation of wheat straw for bio-hydrogen production. Results showed that addition of 1e5 mg of enzyme for per g of wheat straw yielded maximum bio-hydrogen. While untreated showed 10.5 ml of hydrogen per g of volatile solid, enzyme addition enhanced the bio-hydrogen production up to 19.6 ml/g VS. Although enzymatic pretreatment saves time, cost of the enzyme and its synergy with chemical mediators for oxidative stress are still an explorable concern [23].
Physiochemical pretreatment Other than chemical, physical and biological, pretreatment of lignocellulosic biomass is also performed under steam explosion, ammonia fibre explosion (AFEX) and liquid hot water. These pretreatment methods are termed as physiochemical pretreatment of biomass. In steam explosion, which is one of the oldest techniques, biomass is exposed to high pressure and temperature and left for some time before quickly
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decompressing it. Huang et al. [24] performed steam explosion pretreatment cotton stalk in 1% sulphuric acid solution for enhanced enzymatic saccharification. High conversion rate of sugar to biofuel from cotton stalk with no or less inhibition was observed as per the results. Vivekanand et al. [25] demonstrated the effect of severity on birch after steam explosion at 13 combinations of temperature (170 - 230 C) and time (5e15 min). The study reported xylan degradation and generation of pseudo-lignin caused by the increased severity of steam explosion pretreatment. All types of pretreatment and the relevant studies regarding their impact on bio-hydrogen yield and lignin removal discussed in this section are summarized in Table 1.
Inhibition in pretreatment Pretreatment may be considered as a promising route to rise the production of bio-hydrogen from lignocellulosic biomass. However, degradation products formed in different pretreatment approaches may hamper the improved bio-hydrogen production. The degradation products or the inhibitors may be classified in to two categories, furan compounds and weak acids [3]. Furfural and 5 - hydroxymethyl furfural (5 - HMF) are called furan compounds while acetic and formic acids are called weak acids. It is noteworthy that production of degradation products and inhibitors may rupture the microbial cell wall and hinder the microbial and biochemical activity for biohydrogen production. Toxic substances such as furan derivatives may change the pH level in the reactor if present by shifting carboxylic acids into intracellular space and may puncture the cell wall. Weak acids may disturb the optimum acid concentration in the process which also disturb the optimum pH level. Monlau et al. [26] studied the effect of dilute acid hydrolysate on formation of inhibitors while pretreating sunflower stalk for biohydrogen production. Sunflower stalk hydrolysate was prepared by mixing 4 g of HCL in 100 g total solid (TS) of stalks at 170 C for 1 h duration. It was observed that furan derivatives and weak acids were also released besides fermentable sugar from sunflower stalk. The concentration of acetic and formic acid were 0.6 and 0.8 g/L and concentration of furfural and 5 e HMF were 1.15 and 0.13 g/L respectively in the hydrolysate of sunflower stalks. After preparing the hydrolysates, it was mixed in the ratio of 0, 3.5, 7.5, 15 and 35% v/v with glucose as carbon source which was 5 g VS/L of
concentration. A sharp decline was noticed in biohydrogen yield at 15% concentration of hydrolysate þ glucose (0 mol of hydrogen per mole equivalent hexose consumed) compared to glucose only which was 2.04 mol of hydrogen per mole equivalent hexose consumed. Similar results were also reported by Arisht et al. [27] in acid hydrolysate of coconut husk. Pretreatment with phosphoric acid resulted in 0.19, 0.23 and 0.65 g/L of furfural at 1, 5 and 10% v/v concentration. The acetic acid at 1, 5 and 10% concentration of phosphoric acid was 0.36, 0.43 and 0.75 g/L respectively. However, the accumulation of 5 e HMF was minimal (0.0048, 0.0164 and 0.0189 g/L) at various concentration of phosphoric acid (1, 5 and 10%). Also, the bio-hydrogen production was 0.68, 0.52 and 0.45 mol hydrogen/mol sugar consumed from acid hydrolysates (1, 5 and 10% respectively). The extent of the inhibition strongly depends on the concentration of degradation products in the system as well as tolerance capacity of specific microorganisms. Detoxification process of acid hydrolysates may reduce the adverse effect on biohydrogen production. Ion exchange and oxidation processes may be adopted prior to fermentation to reduce ill effects of inhibitors.
Approaches for bio-hydrogen production Classification on the basis of process configuration The fermentation process for hydrogen production can be categorized on the basis of arrangement of pretreatment, hydrolysis and fermentation steps, which can be performed simultaneously in same reactor or sequentially in separate vessels. The three approaches for hydrogen production from lignocellulosic biomass are summarized in the following subsections and Table 2:
Separate hydrolysis and fermentation The conventional approach of producing hydrogen from lignocellulosic biomass comprises of performing hydrolysis and fermentation processes separately in two different reactors [28]. The optimum conditions for hydrolysis and fermentation can be different. Therefore, separate hydrolysis and fermentation (SHF) can enhance the hydrogen production efficiency by carrying out hydrolysis and fermentation at desired optimum conditions in two separate apparatus [7]. Since the ease of fermentation relies upon the efficient
Table 1 e Pretreatment for improved bio-hydrogen production. Feedstock Corn stalk Sweet sorghum Corn stover Rice straw Palm oil fruit brunch Palm oil mill effluent Corn stover Corn stalk Wheat straw Cotton stalk
Pretreatment
Lignin removal (%)
Bio-hydrogen yield
References
Alkali (Lime) Alkali (NaOH) Acid (HCL) Combined (alkali þ acid) Acid (H2SO4) Physical (Ultrasonication) Physical (Microwave) Biological Biochemical Physiochemical (Steam explosion þ H2SO4)
23 53 e 66 e e e 34 e 3
38% increment Maximum 3 mol H2/mol sugar Maximum yield 2.24 mol H2/mol sugar Maximum yield of 0.0027 mol H2/g straw Maximum yield 1.98 mol H2/mol xylose 20% 1.5 mol H2/mol glucose 20% 96%
[11] [12] [13] [14] [15] [18] [20] [21] [22] [24]
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Table 2 e Advantages and disadvantages of bio-hydrogen production methods on the basis of process configurations. S.No.
Type of process
Advantages
1.
Separate hydrolysis and fermentation
Possible to maintain optimize conditions for both processes separately
2.
Simultaneous saccharification and fermentation
Save the reactor cost, shorten the time duration
3.
Consolidated bioprocessing
High mass transfer rates and conversion efficiency due to chosen cultures
conversion of lignocellulosic biomass to soluble sugars, adopting pretreatment prior to hydrolysis may enhance the hydrogen yield by many folds. However, accumulation of monomeric sugars after hydrolysis is the major bottleneck associated of this approach [28]. To remove this hurdle, the accumulated sugars need to be processed further by employing microorganisms capable of fermenting both hexose and pentose sugars [7]. In this regard, performing hydrolysis and fermentation simultaneously in a single apparatus would be an appropriate solution where the converted soluble sugars can be utilized for fermentation [29].
Simultaneous saccharification and fermentation As discussed above, simultaneous saccharification and fermentation (SSF) is an integrated concept in which saccharification of biomass and fermentation of the soluble sugars is performed simultaneously in a single apparatus. SSF improves the hydrogen production efficiency by mitigating the inhibition imposed accumulating sugars during hydrolysis. Apart from rectifying the operational drawback of SHF, SSF also reduce the operational cost by lowering the operation time and apparatus requirements. However, it requires the adjustment of optimum conditions to work for both processes rather than being specific for the individual processes. Li and Chen [30] carried out SSF of corn straw pretreated with steam explosion. After 72 h of SSF, the process achieved the highest cumulative hydrogen yield of 68 mL/g corn straw. Zhao et al. [29] carried out enzymatic pretreatment of corn stalk with Trichoderma viride prior to SSF and obtained hydrogen yield of 89 mL/g corn straw. These studies were focused on only on investigating the possibilities of using SSF for hydrogen production from agriculture waste. Further, researchers also compared the outcomes of SHF and SSF for biohydrogen production to find the type of method providing desirable results in shorter time and in a more economically viable way. Ibrahim et al. [31] compared the SHF and SSF processes for hydrogen production from oil palm empty fruit bunch using Clostridium acetobutylicum. The observed results revealed 21% higher hydrogen yield for SSF as compared to SHF process. This type of comparative studies revealed that the SSF not only reduce the time and cost of hydrogen production but also enhance the hydrogen yield through less chances of contamination and continuous removal of end-products generated after hydrolysis which can serve as inhibitors [32].
Disadvantages
References
Requirement of two separate reactors which increase the cost as well as time of process, accumulation of hydrolysed soluble sugars Not possible to provide optimum conditions for individual processes and need to employ microbes that can work in similar conditions High energy consumption
[7,28,29]
[29e31]
[33e36]
Consolidated bioprocessing Consolidated bioprocessing (CBP) is the process in which specific microbial consortia is employed to produce enzyme cocktail for simultaneous hydrolysis and conversion of hexoses and pentoses to hydrogen. The presence of chosen and acclimatized microorganisms with ability to degrade cellulose, hemicellulose and produce hydrogen is crucial for success of CBP. Previous studies reported CBP using both mesophiles viz. Clostridium sp., Thermotoga sp. and thermophiles such as Clostridium thermocellum, Caldicellulosiruptor sp. and Thermoanaerobacterium sp. [33e36]. However, thermophiles are better choice owing to their ability to function at higher range of temperatures and thereby avoiding contamination of wide range of mesophiles. Higher mass transfer rates and biomass conversion at elevated temperatures are the added advantages of employing thermophiles for CBP. However lower cell density of microbes is the major drawback by which thermophillic CBP suffers. To counter this disadvantage, membrane reactors may be utilized to maintain higher concentration of microbes for continuous conversion of biomass to hydrogen [7]. Moreover, energy consumption pertaining to maintain high temperature is also need to be taken into account during energy and cost benefits analysis.
Types of fermentation process: photo and dark Bio hydrogen production from lignocellulosic biomass can be achieved via biological route encompassing the methods of DF and PF [37]. PF is the process in which organic acids are used as substrate by purple non-sulphur (PNS) photo heterotrophic microorganisms to produce hydrogen and carbon dioxide in the presence of light [38]. On the other hand, the DF is performed under anaerobic conditions and is independent of light. The DF mediated by anaerobic microorganisms results in production of volatile fatty acids (VFAs) viz. acetic acid, propionic acid, butyric acid etc. along with hydrogen [39]. The hydrogen yield attained after fermentation depends upon the adopted metabolic route, the type of microbial strain, substrate and the fermentation conditions. The microorganisms working in the DF and PF are reported to work with different enzyme systems and follow entirely different metabolic pathways for bio-hydrogen production.
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The DF requires a wide range of hydrolytic and hydrogenease enzymes to convert the organic matter into VFAs and hydrogen [40]. On the other hand, the activity of nitrogenase enzyme present in the cell membrane of PNS bacteria is crucial to perform the PF process [40].
Recent developments in technologies to improve hydrogen production from biomass Reactor configuration Reactor is the primary requirement for carrying out the fermentation of lignocellulosic biomass and its configurational aspects have direct influence on the process run [41]. Appropriate design of reactor is crucial for smooth operation of fermentation process. Khan and Kana [42] designed an innovative baffled bioreactor having a support matrix for improved cell immobilization. Appropriate mixing of substrate in reactor was ensured for enhancing the interaction between microbial cells and substrate. The outcomes of fermentation revealed 31% higher hydrogen yield in novel baffled reactor in comparison to standard fermentation flask. The study established the importance of appropriate mixing and cell immobilization to enhance the substrate and microbe’s interaction. Apart from mixing, the separation of liquid, solid and gas is also critical for stable hydrogen production through continuously removing and collecting the produced hydrogen gas from the reactor [43,44]. For achieving better biomass loading, various types of carrier material may also be used to provide a structured bed for biomass attachment [46,47]. Anzola - Rojas and Zaiat [46] explored three different types of carrier material (polyurethane foam, low density polyethylene and ceramic) for biomass attachment in anaerobic down-flow structured-bed reactor. Though ceramic provided better biomass loading, however, the hydrogen production was higher in polyethylene and polyurethane. The hydrogen production rate was hampered due to inefficient mixing and inadequate flow in reactor with ceramic material as carrier. Moreover, the computational simulation may also be adopted for better controlling and monitoring of process parameters during the scale up process [43]. Zhang et al. [45] attempted to integrate the DF and PF using corn stover as substrate for bio-hydrogen production in a pilot scale reactor. Fu et al. [48] incorporated a light guiding plate serving as light guider for microbial biofilm inside a biofilm photo bioreactor. The SiO2/chitosan modified light guide plate was observed to be most efficient for generation of microbial biofilms which resulted in significantly higher bio-hydrogen production.
Supports for augmenting microbial immobilization Adequate microbial cell immobilization is crucial to ensure maximum utilization of lignocellulosic biomass for its conversion in bio-hydrogen along with longer run of the process [49]. The major cell immobilization techniques explored in past decade are attachment-based, adsorption-based, encapsulation based, polymer based and immobilization through nanoparticles. These techniques have been explored
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extensively for successful bio-hydrogen production and optimization of the parameters including cell loading, pH, temperature, mass transfer coefficient, immobilized biomass ratio, supplements, support materials type etc. [49]. The support material type has a significant role in influencing the behavior of cell immobilization and the properties of attached biomass [50]. Support materials can be made up of polyurethane, polyethylene, expanded clay and activated carbon etc. which may have different impact on microbial metabolism as well as the qualitative and quantitative aspects of microbial community immobilized. Li et al. [51] designed a novel photothermal support material consisting of GeO2, SiO2, Chitosan Medium, LaB6 which was investigated for immobilizing photosynthetic bacterial cells. The outcomes of the study revealed the higher efficiency of the novel designed materials resulting in 4-fold increase in bio hydrogen production along with enhanced growth rate of biofilm as compared to experiment having no support material. Apart from polymers, nanoparticles/nanorods can also be used for the purpose of microbial cell immobilization [52,53]. Due to increased surface area, nanoparticles addition enhances the cell immobilization during fermentation which results in significant increase in bio-hydrogen production as reported by studies regarding addition of hematite, maghemite nanoparticles, ferrihydrite nanorods [52e54]. Pansook et al. [55] employed alginate beads for immobilization of Aphanothece halophytica cells for bio-hydrogen production. The result revealed higher bio-hydrogen production by immobilized cells as compared to the reactor having free cells. However, successful usage of nanoparticles for cell immobilization needs to be optimized for determining the appropriate size of nanoparticles. Moreover, addition of nanoparticles beyond a certain concentration can cause toxicity which would adversely affect the viability of microbes as well as the fermentation process. Therefore, the concentration for nanoparticle addition into fermentation media also needs to be investigated for manipulating the cell immobilization to achieve desirable outcomes.
Novel microbial strains Over the years, a wide range of microbes have been explored to examine their efficiency for biomass to hydrogen conversion. The possibility of discovering new microbial strain with increased cellulolytic and hemi cellulolytic ability was always existed as a major topic of research in field of bio-hydrogen production through lignocellulosic biomass. The hydrogen producing microorganisms can be classified in different categories of photosynthetic bacteria, obligate and facultative anaerobes, aerobes and photoautotrophic bacteria [56]. The hunt for novel microbial strains with increased biomass to hydrogen conversion capabilities also gained immense interest in the recent years. A number of studies reported in past two years focused on exploring novel microbial strains for bio-hydrogen production such as Escherichia coli [57], Clostridium beijerinskii [58], Rhodopseudomonas palustris [59,60], Thermoanaerobacterium sp. strain PSU-2 [61], Rhodobacter sphaeroides [62], Streptomyces rubiginosus (SM16) [63], Clostridium pasteurianum [64], Enterobacter aerogenes [65]. Trchounian et al. [40] demonstrated the
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choice of microbial strains for bio-hydrogen production as a sine qua non requirement for sustaining the biochemical conversion. The study emphasized on the role of nitrogenases and hydrogenases enzymes for viable kinetic of biomass to hydrogen production through photo and dark fermentative bacteria. An interesting report on biohythane (mixture of methane and hydrogen) production was published by Abreu et al. [66] employing garden waste as substrate. The study combined the processes of DF and anaerobic digestion in which Caldicellulosiruptor saccharolyticus and Thermotoga maritima were used for biohydrogen production. Furthermore, the co-culture of C. saccharolyticus and Caldicellulosiruptor bescii resulted in higher production of bio-hydrogen as compared to co-culture T. maritima and C. saccharolyticus. A new bio-hydrogen producing strain of Enterococcus faecium was isolated from gamma irradiated sludge [67]. Immobilizing the strain on polyvinyl alcohol-Na alginate resulted in further improvement in biohydrogen yield. Srivastava et al. [68] employed Clostridium pasteurianum for DF of enzymatically pretreated rice straw resulting in maximum hydrogen production rate after (23.96 mL/L.h) 96 h. For improvement of bio-hydrogen yield, the optimization of the process is also required to provide nest suitable conditions to microbe. The statistical tools and mathematical models may be employed for this purpose. The hydrogen production process using a novel strain Enterococcus faecium INET2 was optimized recently via response surface methodology which studied the multiple combinations of temperature, pH, substrate concentration and inoculum size at different levels [69]. These types of studies are required to study both the individual and interactive impact of parameters on fermentation process and hydrogen yield.
Mitigation of inhibitory effects Though the pretreatment methods are adopted to enhance the degradability of lignocellulosic biomass leading to improved conversion to hydrogen. However, a number of pretreatment methods including chemical and thermal methods result in generation of certain compounds that impose inhibitory effects on the fermentation process. Furans and phenolic compounds are acknowledged to have the most detrimental impact over the bio-hydrogen production process [23]. Furfural and 5-hydroxymethylfurfural produced from pretreatment of cellulose and hemicellulose are reported to adversely impact the kinetics of microbial metabolism during the fermentation processes. The inhibitory mechanism of these compounds includes reduction in growth rate and permeability of microbial cells as well as increased formation of reactive oxygen species [23]. The quantity and action level of inhibitory compounds majorly depend upon the type and severity of pretreatment, chemical composition of biomass and the microbes employed to mediate the bio-hydrogen production process [70,71]. The primary inhibitory mechanism involves the permeation of unionized weak acids through the cell wall of microbes and reduce the pH within cell environment leading to hostile conditions for biohydrogen synthesizing microbes. Examining the impact of
furfural concentration on the bio-hydrogen yield revealed that the bio-hydrogen yield declines as the furfural concentration increases. A decline of 21, 29 and 62% was reported for 1, 2 and 4 g/L concentrations of furfural respectively [72]. Interestingly, Akobi et al. [71] achieved increase in bio-hydrogen yield upto 1 g/L concentration of furfural. Increasing the furfural concentration beyond 1 g/L resulted in the decline of biohydrogen production. To mitigate these inhibitory effects, a number of detoxification methods are employed including biological and physiochemical approaches viz. evaporation, flocculation, adsorption on activated carbon, use of enzymes and ion exchange resins.
Integrated fermentations In the recent years, an increasing trend of studies combining fermentation schemes with other processes has been observed to attain higher biomass to hydrogen conversion. For instance, biohythane production involved the combination of fermentation with anaerobic digestion [66]. Further, many recent studies combined PF and DF schemes to improve the efficacy of the bio-hydrogen production process [73,74]. Marone et al. [75] combined the DF process with bio catalyzed electrolytic processes. The most intensively explored integrated fermentation scheme includes coupling of DF and PFs. As shown in Fig. 2, VFAs such as acetic acid, propionic acid and butyric acid present in the effluent of DF, may be employed as a substrate for PF to attain extra hydrogen [76]. Therefore, integrating these two fermentation process results in more efficient biohydrogen production with higher substrate utilization and hydrogen yield. While single step integration allows utilization of DF effluent utilization, the two-stage coupling of DF and PF processes enables the effective optimization and regulation of growth conditions for both processes separately [74,76]. However, the two-stage fermentation integration scheme requires two separate bio-reactors to carry out both type of fermentations and thereby, increases the implementation cost (Fig. 3). The necessity of pretreating DF effluents in some cases further complicates the integrated scheme and its economic aspects [76]. Therefore, the potential to utilize the organic matter to utmost extent and attain complete conversion makes the integrated single stage fermentation scheme ideal and most desirable strategy. Lu and Lee [77] carried out single stage integrated fermentation by employing Clostridium cellulovorans for cellulose degradation during DF and photosynthetic Rhodopseudomonas palustris for PF. The study reported balance of pH by Rhodopseudomonas palustris through consumption of generated VFAs which in turn boosted the cellulose conversion by Clostridium cellulovorans. The overall mutual interaction between both microbes resulted in more competent bio-hydrogen generation process. Similar mutual interaction was observed with coculture of Clostridium butyricum and Rhodobacter sphaeroides and a 3-fold higher bio-hydrogen yield was attained as compared to the monoculture of Clostridium butyricum [78]. Zagrodnik and Łaniecki [79] employed Clostridium acetobutylicum and Rhodobacter sphaeroides for single step DF and PF of
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Fig. 2 e Dark and photo fermentation processes linked through organic acids. corn starch and observed 23% increase in bio-hydrogen yield as compared to the yield of DF alone. The integrated fermentation process carried out at optimum pH 7 with the same co-culture resulted in stable microbial interaction leading to 2.5-fold increase in hydrogen yield [80]. Biohydrogen production from palm oil mill effluent through two stage successive DF and PF resulted in approximately 3.9fold rise in hydrogen production due to the activity of Clostridium butyricum LS2 and Rhodopseudomonas palustris during first and second stage respectively [81]. Zhang et al. [82] carried out two stage sequential fermentation of mediated by Rhodopseudomonas palustris and Clostridium butyricum for fermentation of Platanus orientalis leaves. The fermentation effluent was further used for methane production and resulted in higher biomass conversion efficiency of anaerobic treatment plants. Though, the integration of fermentation processes has potential to achieve higher bio-hydrogen yields; however, the integration method requires to be optimized to attain the best as well as balanced conditions suitable for the individual processes combined during integration. The optimization
needs to be done in terms of culture conditions, pH, temperature, substrate concentration etc. Hitit et al. [74] attempted to optimize the culture conditions to meet the different growth requirements of dark and photo fermenting bacteria in single stage. Buffer and substrate concentrations as well as the ratio of Clostridium butyricum and Rhodopseudomonas palustris was optimized using response surface methodology to achieve the maximum hydrogen production. Highest hydrogen yield was obtained at 50 mM buffer concentration and 15 g/L substrate concentration with microbial ratio of 3 growing at 30 C under illumination of 40 W m2 light intensity. Table 3 summarizes the prominent studies regarding the integration of PF and DF in single stage and two stages.
Metal additives for improving catalytic activity Catalysts play an important role in transforming reaction kinetics leading to more efficient conversion process with high turnover. Improving the properties of catalysts itself result in further boost in end product yield owing to the better
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Fig. 3 e Single stage and two stage integrated fermentation schemes. Here, DFM: dark fermentation microbes; PFM: photo fermentation microbes; VFA: volatile fatty acids.
performance of catalytic conversion. A wide range of metals nanoparticles, zeolites, ionic liquids etc. can be used as catalysts or can be incorporated in fermentation process as additives to improve the activity of targeted bio-catalysts viz. hydrogenase or nitrogenase. Nanoparticles proved to be the most favored choice of research for catalyzing and improving the bio-hydrogen production process in the recent studies (Table 4) [52,64,88]. The presence of nanoparticles enhances the conductivity effects leading to efficient movement and exchange of electrons within the periplasm. Ferrous ions are specifically favored as additives since it is present in the active sites of hydrogenases as well as ferredoxins [89]. This resulted in enhanced electron transfer process mediated by ferredoxins to facilitate the mechanism of ferredoxin oxidoreductase and hydrogenase enzymes involved in carbohydrate degradation during fermentation
[64]. The stability of these metal-based nanoparticles further increases their desirability as catalysts for improving biohydrogen as well as biomethane and ethanol production processes. Taherdanak et al. [88] investigated the influence of Fe and Ni nanoparticles on the bio-hydrogen production from glucose through DF process. The observations revealed highest hydrogen yield for the process employing Niþ2 as catalyst as compared to Feþ2 nanocatalysts. Hsieh et al. [64] compared the effects of adding Fe and TiO2 nanoparticles as catalysts. The study reported significant improvement in biohydrogen yield using Fe nanocatalyst, while no substantial improvement was observed after adding TiO2 as catalyst. Lin et al. [90] observed improved bio-hydrogen yield after addition of Fe2O3 nanoparticles as catalyst. The outcomes were in line with previously published study reporting increased hydrogen yield owing to the action of Fe2O3 nanocatalyst [91]. Engliman
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Table 3 e Integrative fermentation schemes for bio-hydrogen production. S.No. Single 1. 2. 3. 4. 5. 6.
Substrate
stage integration Cellulose Starch Glucose Corn starch Corn starch Potato juice and glucose Two stage integration 7. Potato stem peel 8. Beet molasses 9. Cassava starch 10. Cheese whey 11. Palm oil mill effluent 12. Platanus Orientalis leaves
Microorganisms Clostridium Clostridium Clostridium Clostridium Clostridium Clostridium
cellulovorans, Rhodopseudomonas palustris butyricum and Rhodobacter sphaeroides acetobutylicum and Rhodobacter sphaeroides acetobutylicum and Rhodobacter sphaeroides acetobutylicum and Rhodobacter sphaeroides butyricum Rhodopseudomonas palustris
Caldicelluluiruptor saccharolyticus, Rhodobacter capsulatus Caldicelluluiruptor saccharolyticus, Rhodobacter capsulatus Mixed culture for DF, Rhodopseudomonas palustris for PF E. aerogenes and Rhodopseudomonas BHU 01 Clostridium butyricum LS2 and Rhodopseudomonas palustris Rhodopseudomonas palustris, Clostridium butyricum
Hydrogen yield
References
3-fold increase in hydrogen yield 3-fold increase in hydrogen yield 23% increase in bio-hydrogen yield 2.5-fold increase in bio-hydrogen yield 6.4 ± 1.3 mol/mol glucose hydrogen yield
[77] [78] [83] [79] [80] [74]
5.81 mol/mol hexose hydrogen yield 13.7 mol/mol hexose hydrogen yield 0.035 mol/g starch hydrogen yield 2.04 mol/mol lactose hydrogen yield 3.9-fold increase in hydrogen yield e
[84] [85] [86] [87] [81] [82]
et al. [92] achieved 53% increase in hydrogen yield after addition of Iron (II) oxide nanoparticles as biocatalyst for thermophillic fermentation process carried out by mixed culture of microbes. Liu et al. [93] investigated and compared the effect of three types of nanoparticles (ZnO, TiO2 and SiC) on the PF of beef extract and other substrates including sodium glutamate and sodium acetate by Rhodopseudomonas sp. The outcomes revealed maximum hydrogen yield for the fermentation involving SiC nanoparticles (200 mg/L) as catalyst. The above-mentioned studies indicates the potential of metal nanoparticles for improving bio-hydrogen yield through fermentation process. Nanoparticle addition not only improves the metabolic action of microbes but also aids in enhancing the electron transfer during the fermentation reactions pertaining to the high surface area and quantum impact of nanoparticles [98]. However, the contradictory patterns of influence for the same type of nanoparticles in different study raise the concern over the consistency of research outcomes. This challenge needs to be addressed through the determination of ideal size and concentrations of nano catalysts to be added in the fermentation reactor to achieve positive influence on the bio-hydrogen yield.
metal centers. The three types of hydrogenases are e Fe, FeFe and NiFe hydrogenase. Though, FeFe hydrogenase can both mediate the reduction of Hþ and oxidation of H2, it is mainly involved in the hydrogen production process [102]. On the other hand, NiFe hydrogenase is primarily involved in hydrogen consumption process. The hydrogen production reaction catalyzed by hydrogenase may be represented as follows:
Hydrogen production pathways in microorganisms and the enzyme system
Genetic engineering
The pathway of bio-hydrogen production differs for photo and DF processes. During PF, the purple non-sulphur photosynthetic bacteria generate ATP and reduce ferredoxins (Fd) through reverse electron flow in presence of light and anaerobic conditions [99]. The organic compounds provided as substrate act as electron donor. The hydrogen ions are catalyzed by either hydrogenase or nitrogenase in the presence of light to produce hydrogen gas [100]. On the other hand, DF harvest energy from microbial oxidation process of organic substrates such as glycolysis. DF results into varying metabolic products depending upon the microbes involved in the process as well as the substrate, nutrients, pH, temperature etc. [99,101]. The hydrogenase enzyme involved in the fermentation process can be grouped in three categories on the basis of the
2Fdþ þ 2Hþ ————— 2Fd2þ þ H2 [ The nitrogenase enzyme which is well known for nitrogen fixation, catalyzes the conversion of nitrogen to ammonia. The hydrogen is produced in this reaction as a by-product. The reaction of nitrogen is as follows: N2 þ 2Hþ þ2e ————— 2NH3 þ H2 [ The nitrogenase enzyme consists of three metal clusters including P cluster, FeS cluster and FeMo cluster. The FeS cluster aids in transferring electron to FeMo and P cluster which actively participates in the reduction of nitrogen to ammonia [99].
Possessing the ability to manipulate the metabolic pathways of hydrogen producing microbial strains, genetic engineering has great potential to augment the competence of biomass to hydrogen conversion process and thereby the hydrogen yield. The theoretical potential of hydrogen yield by using lignocellulosic biomass may be attained by improved modifications in the existing metabolism of dark and photo fermenting organisms or by discovering the new pathways. The positive impact on hydrogen yield through genetic manipulation may be achieved by developing more efficient enzyme machinery, maximizing substrate utilization by enzymes, downregulation of genes and transcription factors involved in the processes competing or interfering with hydrogen production. Despite the bright prospects, this area of research remained largely unexplored with only a few published reports in past decade. Wu et al. [103] employed genetically
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Table 4 e Nanocatalyst addition during fermentation for hydrogen production. S.No
Substrate
Microorganisms
Nanoparticles type
Concentration (mg/L)
Hydrogen Yield
2.54 mol/mol of glucose 2.33 mol/mol of glucose
1.
Glucose
Mixed culture
Nickel
5.67
2.
Glucose
Iron oxide nanoparticles
175
3.
Starch
Clostridium acetobutylicum NCIM 2337 Mixed culture
Fe0 and Ni0
37.5
4.
Mixed culture
Hematite
200
5.
Distillery waste water Glucose
Fe and TiO2
50
6.
Glucose
Clostridium pasteurianum Mixed culture
Iron (II) oxide
…
7.
Beef extract, sodium acetate, l-cysteine, sodium glutamate and other components
Rhodopseudomonas sp. A7
TiO2, SiC and ZnO
ZnO (100), SiC (200), TiO2 (300)
modified Klebsiella oxytoca HP1 by inactivating adhE gene and achieved improved hydrogen production after two step DF and PF of sugarcane bagasse. Deletion of lactate dehydrogenase (ldh) gene in Caldicellulosiruptor bescii led to divert the electron transfer from lactate production pathway to hydrogen production [104]. The mutant strain with deleted ldh gene showcased higher hydrogen production. The formate hydrogen lyase (FHL) gene system is also targeted for genetic manipulation as it is involved in maturation of hydrogenases. FHLA gene is the most important gene in this system which activates the FHL system by promoting the synthesis of other component of system such as FDH-H [105]. On the other hand, hycA gene encode for the HYCA suppressor protein which stop the FHL transcription through binding with FHLA and promotes the expression of uptake hydrogenases. Interstingly, Kim et al. [106] discovered an upswing in FHL activity by deleting the hycA gene resulting in increased hydrogen yield. Further deletion of hya and hyb genes (uptake hydrogenase genes) led to 1.2-fold increase in hydrogen yield. In facultative anaerobes, both FHL and pyruvate formate lyase (PFL) assist in hydrogen production process. Madeda et al. [107] reported 41 fold increase in hydrogen yield after cloning the hoxEFUYH gene found in Cyanobacterium synechocystis encoding for the expression of bidirectional hydrogenase and transferring it into E. coli. The other method for improving bio-hydrogen yield is to knock out or suppress the genes coding for uptake hydrogenases. The genetic manipulations can be achieved through chemical mutagenesis as well as exposing the strains to ultraviolet rays [108]. Undesirable phenotypes may be expressed sometimes due to genetic modifications. However, it is noteworthy that the outcomes of employing these methods of genetic manipulations may not always be positive. Though the few reported studies clearly achieved a significant upsurge in hydrogen yield owing to the genetic manipulation of fermenting microbes. However, the stability of newly found phenotypes, genetic expression as well as the alternate
Impact on hydrogen production
Reference
23% increase
[94]
33% increase
[95]
0.0062 mol H2/g- 200% increase VS 8.83 mmol/g COD 62% increase
[96]
2.1 mol/mol hexose 1.92 mol/mol glucose 2.99 mol/mol acetate for SiC
25% increase
[64]
53% increase
[92]
18.6% increase by SiC addition
[93]
[97]
metabolic pathways are required to be tested through more up scaled studies beyond the laboratory trials.
Conclusion The review of the cutting-edge researches carried out in recent years reveal the possibilities of improvement in the existing fermentation technologies as well as the necessity to divulge into the untapped and poorly explored research arenas for improving the bio-hydrogen yield. The major observation of the review can be concluded as below: Appropriate pretreatment methods can be employed to reduce the recalcitrance of biomass structural components and enhance the degradability of biomass for hydrogen production. Further addition of nano catalysts, cell immobilization, use of more efficient novel strains etc. may be used to improve the biomass to hydrogen conversion reactions. The integration schemes of DF and PF processes have been emerged as the most intensively explored research area in past three years with a large number of published reports and proved to be an appealing option for enhanced hydrogen production. The genetic engineering approaches may provide many folds increase in bio-hydrogen production through the manipulation in the genetic makeup of hydrogen producing bacteria.
Future perspectives Though the research in bio-hydrogen production are in continuous drift, however, some of the necessary concerns need to be addressed before taking up the novel technology advancements from lab scale to commercial scale. Feasibility study of potential integrated fermentation schemes through
Please cite this article as: Yadav M et al., Lignocellulose to bio-hydrogen: An overview on recent developments, International Journal of Hydrogen Energy, https://doi.org/10.1016/j.ijhydene.2019.10.027
international journal of hydrogen energy xxx (xxxx) xxx
modelling and simulation before proceeding for up scaling. Optimization of the key process parameters involved in the utilization of new strategies and techniques for bio-hydrogen yield augmentation. Novel strain with higher biomass to hydrogen conversion efficiency can be prepared by manipulating the key genes and transcriptional factors involved in the process. For this, better understanding of the enzyme mechanism and metabolism pathways is crucial. The major focus needs to be put on FHL and PFL system and developing alternative pathways by using gene knockout techniques. The proteomics approach may be helpful to study the role of different proteins involved in hydrogen production as well as identifying the key factors that need to be targeted.
Authors contribution MY and KP contributed equally in writing the manuscript as well as preparing the figures and tables. VV provided scientific insights and technical guidance during manuscript writing.
Acknowledgement MY and KP would like to acknowledge Malaviya National Institute of Technology Jaipur to provide the fellowships and infrastructure. VV acknowledges Department of Biotechnology, Ministry of Science and Technology, Government of India for providing financial support through Ramalingaswami Re-Entry fellowship (No. BT/RLF/Reentry/04/ 2013).
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