- Email: [email protected]
Biomass based hydrogen production by dark fermentation — recent trends and opportunities for greener processes
Available online at www.sciencedirect.com
ScienceDirect Biomass based hydrogen production by dark fermentation — recent trends and opportunities for greener processes Gopalakrishnan Kumar1, Sutha Shobana2, Dillirani Nagarajan3,4, Duu-Jong Lee4,5, Kuo-Shing Lee6, Chiu-Yue Lin7, Chun-Yen Chen8 and Jo-Shu Chang3,9 The generation of biohydrogen as source of biofuel/bioenergy from the wide variety of biomass has gathered a substantial quantum of research efforts in several aspects. One of the major thrusts in this field has been the pursuit of technically sound and effective methods and/or approaches towards significant improvement in the bioconversion efficiency and enhanced biohydrogen yields. In this perspective, the present contribution showcases the views formulated based on the latest advances reported in dark fermentative biohydrogen production (DHFP), which is considered as the most feasible route for commercialization of biohydrogen. The potential prospects and future research avenues are also presented. Addresses 1 Green Processing, Bioremediation and Alternative Energies Research Group, Faculty of Environment and Labour Safety, Ton Duc Thang University, Ho Chi Minh City, Viet Nam 2 Department of Chemistry and Research Centre, Aditanar College of Arts and Science, Virapandianpatnam, Tiruchendur, Tamil Nadu, India 3 Department of Chemical Engineering, National Cheng-Kung University, Tainan, Taiwan 4 Department of Chemical Engineering, National Taiwan University, Taipei 10617, Taiwan 5 Department of Chemical Engineering, National Taiwan University of Science and Technology, Taipei 10607, Taiwan 6 Department of Safety Health and Environmental Engineering, Central Taiwan University of Science and Technology, Taichung, Taiwan 7 Department of Environmental Engineering and Science, Feng Chia University, Taichung, Taiwan 8 University Center for Bioscience and Biotechnology, National Cheng Kung University, Tainan 701, Taiwan 9 Research Center for Energy Technology and Strategy, National ChengKung University, Tainan, Taiwan Corresponding authors: Kumar, Gopalakrishnan ([email protected]), Lin, Chiu-Yue ([email protected]), Chang, Jo-Shu ([email protected])
Current Opinion in Biotechnology 2018, 50:136–145 This review comes from a themed issue on Energy biotechnology Edited by Akihiko Kondo
Introduction The impending lack of energy has instigated the search for eco-friendly, biodegradable, sustainable and costeffective biofuels from renewable carbon sources of various organic streams [1]. Among the biofuels, hydrogen from both renewable and non-renewable sources is highly promising because of its clean burning properties and its use in transportation and power generation sectors [2,3]. Dark fermentation (DF) or anaerobic fermentation for hydrogen production is the decomposition of organic carbon substrates using facultative or obligate anaerobic bacteria including but not exclusively Clostridium, Enterobacter, Bacillus and Escherichia coli. The pathway is described by the equations below. Glycolysis
Glucose ! Pyruvate Pyruvate þ Co A Reduction
þ 2FdðoxÞ ! Acetyl Co A þ 2FdðredÞ þ CO2
2FdðredÞ
Oxidation
!
Hydrogenase
2FdðoxÞ þ H2 "
The main soluble products are certain organic acids like acetate, propionate and butyrate along with ethanol [4,5]. Lignocellulosic biomass (LCB) is currently the most available biomass resource for biohydrogen production, but it is challenged by the recalcitrant nature of the biomass and the generation of potential fermentative inhibitors, based on the nature of the biomass and the pretreatment process used [6]. Microalgae and macroalgae are the third generation feedstock for hydrogen production [7], and wastewater treatment by DF is an alternate route to explore [8]. In this review, we explore the recent advances in biohydrogen production by DF, including feedstock, reactor design and other possible green processes.
https://doi.org/10.1016/j.copbio.2017.12.024 0958-1669/ã 2018 Elsevier Ltd. All rights reserved.
Green biomass processing for hydrogen production Natural and green biological pathways for hydrogen production are water-splitting photosynthesis, photo fermentation, DF and electro fermentation. The energy efficient
Current Opinion in Biotechnology 2018, 50:136–145
www.sciencedirect.com
Greener processes for dark fermentative bioH2 production Kumar et al. 137
hydrogen production mainly depends on the choice of a biocatalyst/inoculum involved in the bioprocess [9]. Production of hydrogen from industrial wastewater is considerably subjected to the type of inoculum, composition and nature of biodegradability and among them, the inoculum source plays a vital role [10,11]. Pretreatments and enhanced reactor designs for DF
Pretreatment of the substrates makes DF hydrogen selective by enrichment of acidogenic bacteria and inhibition of hydrogenotrophic methanogens [11,12]. Pretreatment techniques are categorized into physico-mechanical (extrusion and pyrolysis), physico-chemical (steam, ammonia fibre and CO2 explosion, hot water, wet-oxidation, sonification, microwave imposed), chemical (ozone, acid or alkaline, oxidative delignification, organo-solvation, and ionic liquid) and enzymatic pretreatments, among them the physico-chemical and chemical treatments are considered to be the most proficient pretreatment techniques [5]. Thermoanaerobacterium thermosaccharolyticum W16 produced 2.24 mol H2/mol sugar by using sulfuric acid-pretreated corn stover [13], while the NaOH-pretreated corn stover yielded 108.5 mmol/ L H2 when using the same inoculum incorporated with cellulose enzymolysis [14]. The thermophilic H2 production from mild acid and microwave pretreated corn stover was 1.53 mol H2/mol glucose, while the mesophilic fermentation of acid and steam explosion pretreated corn stover yielded 3.0 mol H2/mol glucose [15,16]. The hydrogen production rate and yield from pretreated algal biomass were about 62 mL/L d and 9.5 mL/g VSadded, respectively [11]. Optimal pretreatment methods must achieve high sugar recovery, chronological fractionation of biomass, formation of co-products, negligible formation of inhibitors, applicability to wide range of feedstock and cost-effectivity [17,18]. Table 1 shows biomass pretreatment methods for fermentative hydrogen production. Suspended bioreactors have been designed for large-scale biological hydrogen production using microorganisms viz. continuously stirred tank reactor (CSTR), anaerobic sequencing batch reactor (ASBR) and anaerobic membrane bioreactor (AnMBR) [19]. The immobilized bioreactors developed are the up-flow anaerobic sludge blanket reactor (UASB), expanded granular sludge bed reactor (EGSB), and anaerobic fluidized bed reactor (AFBR), with CSTR and UASB being the most consistently used bioreactors and anaerobic granular sludge bed (AnGSB) provides better performance towards hydrogen production. In the case of wastewater treatment, CSTR, ASBR, CSABR, CIGSBR and AGSBR were developed for the production of dark fermentative hydrogen. It was predicted that UASB and anaerobic filter (AF) reactors show some additional stable performances at a low HRT (i.e. 0.5 day), while in CSTR, operating at low HRTs might lead to biomass washout. In addition, UASB has widely been applied in laboratory/pilot-scale research and is www.sciencedirect.com
effective for converting organic wastes to biohydrogen [19,20]. Further, some fixed-bed reactors were also used to proficiently produce biohydrogen with easy operations, while poor mass transfer efficiency has been an intrinsic drawback of such system. Moreover, high-rate anaerobic sequencing batch reactor (AnSBR) is operated in chemostat using a continuously stirred reactor. Since the period for ‘Fill and React’ stages can be accustomed to instruct the AnSBR system a CSTR-like or a perfect PFR-like management characteristics [21]. Moreover, biofilm/granule based type reactor designs are suggested with the intention to retain more active and effective microbes [22]. Among the available reactor design opportunities for dark fermentative biological hydrogen production, the ASBR seems to have the best performance, in particular when using wastewater as the feed, due to its high efficiency in biological pollutants removal in the various phases during the operational process [23,24].
Process improvement strategies and cell immobilization systems for DF
The yield of hydrogen from DF is metabolically restricted to 4 mol H2/mol glucose, presenting the most important technical obstacle for its field uses [9]. Additional treatments are essential to discard the significant amounts of residual fermentative organic effluents of carbon-rich substrates into the environment [25]. Several two-stage processes have been adapted to augment biohydrogen production and to enhance hydrogen production [26]. Immobilized cell systems have been developed for largescale biohydrogen production by DF, including physical adsorption, covalent bonding, cross-linking, entrapment, and encapsulation methods. The most common immobilization method is physical adsorption which aids in effective mass transfer and carbon source consumption at short HRT with improved hydrogen productivity [27]. Immobilization of Thermotoga neapolitana cells on a cationic hydrogel resulted in a hydrogen yield of 3.3 mol H2/ mol glucose and a hydrogen production rate of about 50.6 mL/L/h. Immobilization of anaerobic sludge on activated carbon granules and thermophilic DF attained a hydrogen yield of 2.8 mol H2/mol hexose [28]. It was found that immobilization of H2-producing bacteria on some novel carriers, such as calcium-alginate amalgamactivated carbon, could promote biohydrogen production [29]. It was also observed that the encapsulated cells were more effective than the free cells for the production of biohydrogen [30]. Polyvinyl alcohol (PVA) encapsulation of Enterobacter sp. resulted in pronounced stability of the inoculum in a fed-batch reactor for biohydrogen production [31]. Immobilization of Clostridium beijerinckii NCIMB8052 in chitosan with magnetite nanoparticles and alginic acid polyelectrolytes enhanced the production of biohydrogen [32]. So far, the selection of an appropriate Current Opinion in Biotechnology 2018, 50:136–145
138 Energy biotechnology
Table 1 Biohydrogen productivity from various renewable feedstocks in dark fermentative hydrogen production Biomass type Lignocellulosic Beer lees Cornstalk
Pretreatment conditions 4% HCl (30 min, boiling) 0.6% HCl (90 C/2 hours), Trichoderma viridecellulase (50 C, 72 hours, pH 4.8) 0.2% HCl (30 min, boiling) Microbe additives (25 C, 15 days)
RCG Lawn grass Miscanthus
Poplar leaves Rice straw Soybean straw Sugarcane bagasse Sweet sorghum bagasse
P. chrysosporium (29 C, 15 days) 3% HCl (90 min, 121 C, autoclave) 4% HCl (30 min, boiling) 12% NaOH (70 C, 4 hours), commercial enzymes (45 C, 72 hours, pH 4.8) 2% Viscozyme L (50 C, 3 hours, pH 4) 10% NH4OH (60 min, 121 C) and 1% H2SO4 (50 min, 121 C) 4% HCl (30 min, boiling) 0.5% H2SO4 (60 min, 121 C, 1.47 bar) 10% NaOH (70 C, 4 hours), commercial cellulose (50 C, 24 hours, pH 5)
Inoculum
Highest H2 yield
Reference
1
Anaerobic mixed consortia Heat-pretreated anaerobic sludge
53.03 mL H2 g DB 126.22–141.29 mL H2 g1 DB
Enriched consortia from cow dung compost Aerated microbial consortium
149.69 mL H2 g1 DB 176.00 mL H2 g1 DB
Enriched mixed culture dominated by T. thermosaccharolyticum W16 89.30 mL H2 g1 DB
C. pasteurianum T. elfii DSM 9442
31.60 mL H2 g1 DB 35 C, 1 atm 72.21 mL H2 g1 DB 2280 mL H2 at 65 C, 1 atm
C. pasteurianum
44.92 mL H2 g1 DB
T. neapolitana
77.1 mL H2 g1 DB at 75 C, 1 atm 60.2 mL H2 g1 DB 44.0 mL H2 g1 DB
Enriched microbial culture
C. butiricum C. butiricum C. saccharolyticus
[14]
73.6 H2 mmol1: C6 sugars at 72 C, 1 atm
Fermentation characteristics Codiumfragil
Macroalgae
Ulva lactuca Green Gelidiumamansii
Porphyratenera
Red
Gracilariaverrucosa
Washed with fresh water, dried at 105 C, milled at 0.5 mm; batch bottles, pH 5, 35 C Washed with fresh water, dried at room temperature, milled; batch bottles, 35 C Washed with fresh water, dried at 105 C, milled at 0.5 mm; batch bottles, pH 5.5, 35 C Washed with fresh water, dried at room temperature, milled; batch bottles, 35 C Washed with fresh water, dried at 105 C, milled at 0.5 mm; batch bottles, pH 5.5, 35 C Washed with fresh water, dried at 105 C, milled at 0.5 mm; batch bottles, pH 5.5, 35 C
WWTP anaerobic digester sludge, heat pretreated: 90 C, 20 min
24.4 mL g1 TS
WWTP anaerobic digester sludge
10.0 mL g1 TS/ mL H2 g1 algae
WWTP anaerobic digester sludge, pretreated at 90 C, 20 min
43.1 mL g1 TS
WWTP anaerobic digester sludge
9.0 mL g1 TS/ mL H2 g1 algae
WWTP anaerobic digester sludge, pretreated at 90 C, 20 min
15.4 mL g1 TS
WWTP anaerobic digester sludge, pretreated at 90 C, 20 min
Brown
Washed with fresh water, dry at 105 C, milled at 0.5 mm
Current Opinion in Biotechnology 2018, 50:136–145
26.7 mL g
TS
67.0 mL g1 TS 71.4 mL g1 TS
Laminaria japonica Dried at room temperature, milled at 0.5 mm; batch bottles, pH 5.5, 35 C Dried at room temperature, milled at 0.5 mm
[10] 1
Anaerobic sequencing batch reactor (ASBR), HRT = 6 days, OLR = 3.4 g COD L1 d1, pH = 5.5, T = 35 C
61.3 mL g1 TS
58.5–34.1 mL g1 TS
www.sciencedirect.com
Greener processes for dark fermentative bioH2 production Kumar et al. 139
Table 1 (Continued ) Fermentation characteristics Microalgae
Chlamydomonas reinhardtii
D. tertiolecta sp.
Nannochloropsis sp.
Scenedesmus sp.
Harvested by centrifugation (6000 g, 15 min); batch bottles, 37 C Harvested by flocculation followed by centrifugation, pH adjusted to 7 and stored at 20 C; batch bottles, 30 C Harvested by flocculation followed by centrifugation, pH adjusted to 7 and stored at 20 C; batch bottles, 37 C Harvested by centrifugation (5000 g), oven dried and powdered to 0.02 mm mesh size; batch bottles, 30 C Harvested by centrifugation at 10 000 rpm for 10 min, dried in an oven at 70 C, grounding, extraction of lipids by supercritical fluid extraction; batch bottles, 30 C Harvested by centrifugation at 10 000 rpm for 10 min, dried in an oven at 70 C, grounding, extraction of lipids by Soxhlet extraction Harvested by centrifugation at 10 000 rpm for 10 min, dried in an oven at 70 C; batch bottles, 37 C, pH 6.5
Category Wastewater
Rice mill WW BWW Distillery effluent Cassava WW Cassava starch processing WW Organic WW Textile WW Sugar beet juice
Pure culture C. butyricum NCIB 9576
40 mL g1 TS
Enrichment of compost pile
58.0 mL g1 TS/ mL H2 g1 algae
Produced by bacteria naturally present in microalgal biomass slurry, methanogenesis suppressed by 20 m MBESA Enterobacter aerogenes ATCC 13048
13 mL g1 TS
48.0 mL g1 TS
49.5–60.6 mL g1 TS
[10,34]
50.5 mL g1 TS
WWTP anaerobic digester sludge, pretreated at 95 C, 30 min
Inoculum Enterobacter aerogens EMC+ E. coli XL1 blue + Enterobacter cloacae Enterobacter cloacae C. acetobuytlicum ATCC824 EMC Romani hot spring Soil Anaerobic sludge Anaerobic digested sludge
21 mL g1 TS
Hydrogen yield (mol/mol hexose added; batch hydrogen production) 1.74 mol/mol sugar 260 mL (0.01 mol) 165.3 mL/g COD 2.41 mol/mol glucose [4,5] 128.4 mL/g starch 2.32 mol/mol 1.37 mol/mol 3.2 mol/mol
DB = dry biomass; RCG = reed canary grass; BWW = beverage wastewater; EMC = enriched mixed culture.
immobilization method is extremely specific to the dark fermentative bioreactors and hydrogen producers [27]. Consolidated bioprocessing (CBP) for DF
CBP is the integration of hydrolysis and fermentation of biomass to the desired product, which lowers the energy inputs and equipment requirements of the conventional multi-step fermentation process [33]. In case of hydrogen production, CBP can be applied for the direct conversion of LCB to hydrogen. CBP microbes that can be of great potential in hydrogen production are of the genera Clostridium, Thermoanaerobacter [34], E. coli and Caldicellulosiruptor. A rumen derived E. coli loaded with www.sciencedirect.com
a variety of extracellular glucanase activity was isolated and it produced 4.75 mL H2/g of untreated corn straw [35]. This opens new possibilities in native cellulolytic strategy for CBP, as E. coli is the most studied bacteria with a well-defined molecular toolkit and it has been modified previously for hydrogen production [36]. Clostridium species, Clostridium thermocellum in particular, has an extracellular cellulosome with 24 distinct glucanases that aid in the degradation of hemicellulose, cellulose and lignin [37]. C. thermocellum is believed to be highly efficient in plant cell wall destabilization compared to fungal cellulases [34]. C. thermocellum has been successfully used for the CBP of untreated and pretreated sugarcane Current Opinion in Biotechnology 2018, 50:136–145
140 Energy biotechnology
bagasse [38–40], corn stalk [41] and untreated biomass of Populustrichocarpa [42]. T. thermosaccharolyticum is a moderately thermophilic H2 producing anaerobic bacterium capable of utilizing pretreated and untreated LCB. The bacterium is resistant to the common fermentative inhibitors like furfural and 5-hydroxymethyl furfural [43]. It could generate around 3.5 mmol H2 per g substrate for untreated corn stalk [44], and with simple fungal pretreatment, the hydrogen yield from corn stalk increased to 7 mmol H2 per g substrate [45]. Some strains could achieve higher yields from untreated LCB, as high as 6.8 mmol H2 per g substrate from corn stalk [46]. Caldicellulosiruptor bescii is another potential CBP candidate for biohydrogen production. C. bescii is a hyperthermophilic, anaerobic, Gram positive bacterium, with the potential for utilizing diverse substrates via a mixed acid fermentation pathway producing hydrogen with yields as high as 4 mol H2 per mol glucose as indicated by the Thauer limit [47]. Hydrogen production is mediated by a [Fe–Fe] bifurcating hydrogenase [48] which allows higher yields compared to the facultative anaerobes like E. coli. C. bescii is capable of growth and hydrogen production from crystalline cellulose and raw LCB like switch grass [49], wastewater biosolids [50], as C. saccharolyticus could produce 14 mmol H2/L from untreated switch grass [51]. Deletion of the lactate dehydrogenase gene in C. bescii enhanced hydrogen production from switch grass [52–54], completely funnelling the carbon to hydrogen.
Opportunities and future trends Algae-based H2 production via DF and water-splitting photosynthesis
Microalgae and macroalgae are an attractive feedstock for biohydrogen production, as they are devoid of lignin, thus reducing the complexities of pretreatment. The carbohydrates present in microalgae including green algae and cyanobacteria are simple polyglucans like starch and glycogen, while macroalgae are composed of different sugar acids and sugar alcohols like glucuronic acid and mannitol [55]. Nutrient deprivation strategies like nitrogen or sulfur depletion has been applied successfully for the accumulation of carbohydrates in microalgae. Carbohydrate content in the range of 60–70% has been attained by various cultivation strategies from Chlamydomonas sp. and Chlorella sp. [54–56]. Microalgal cell walls are composed of cellulose and hemicellulose, which upon hydrolysis releases fermentable sugars. Mild acid/alkali hydrolysis, in combination with thermal pretreatment can effectively release the component sugars for fermentation [57]. Micro and macroalgae can be co-fermented to increase the carbon/nitrogen ratio in case of protein rich microalgae [58]. The feedstock price can be greatly reduced by using algae obtained from wastewater treatment [59] or lipid extracted microalgal biomass from the biodiesel industry [60]. The microalgal consortium obtained from wastewater with a sugar content of 28% yielded 47 mL H2/g VS [61], while the leftover biomass Current Opinion in Biotechnology 2018, 50:136–145
of Nannochloropsis sp. yielded 60.6 mL H2/g dry biomass [60]. The quality of these algae might not be adequate for food or feed industry, and the residual energy can be recovered by DF. The use of saccharolytic species like T. neapolitana as the fermentative bacterium in a thermophilic process can lower the pretreatment costs and increase hydrogen yields from thermodynamic aspects and simple cell disruption to release the stored starch would suffice the fermentation needs in simultaneous saccharification and fermentation (SSF) [61]. In addition, microalgae and cyanobacteria are capable of evolving hydrogen under specific physiological conditions. The green algal [Fe–Fe] hydrogenases are very efficient with high turnover rates of 6000–9000 s1 making microalgae an attractive source for biological hydrogen production, but they are highly sensitive to oxygen and are induced under specific anoxic conditions [62]. Hydrogen evolution in microalgae is transient and hence attaining sustained production and the oxygen sensitivity of the hydrogenases are the major bottlenecks in this green method for hydrogen production [63]. Anaerobiosis for sustained hydrogen production in microalgae has been achieved by certain culture strategies. Under sulfur deprivation which prevents the reconstruction of damaged PSII blocking oxygen evolution, sustained hydrogen production can be attained in Chlamydomonas reinhardtii via a two-stage indirect biophotolysis strategy with a hydrogen accumulation of up to 2 mL h1 for 160 hours [64]. Hydrogen production under aerobic conditions has been reported for the cyanobacteria Cyanothece sp. (465 mmol H2 (mg chlorophyll)1 h1) [65] and the green alga Chlorella vulgaris (1.2–2 mL L1) [66], alleviating the necessity of maintaining anaerobic conditions in an aerobic organism like microalgae. Integrated configurations combining photofermentation and electro-fermentation
The COD rich DF effluent can be further processed by various methods for the complete recovery of energy like photo-fermentation [67], microbial fuel cells (MFCs) [68], microbial electrolysis cells [69] and as an organic carbon source for microalgal cultivation [70]. A MFC has exoelectrogens to oxidize organic matter at anode surface and to reduce the yielded protons at cathode surface to produce water and electricity generated [71]. Thus, integrated DF and MFC can remove COD from spent liquor of DF unit with energy recovery [72]. Varanasi et al. used an integrated approach of combining thermophilic hydrogen fermentation from cellulosic substrate with MFC [73,74]. The integration of DF + MFC produced 0.55 mol H2/mol glycerol from crude glycerol with 20% COD removal [75]. In MEC, an external voltage is applied to drive electrons so hydrogen can be formed by proton reduction at the cathode. The integrated DF and MEC can achieve high hydrogen production yield and rate [76,77]. MECs require relatively low voltage (0.2–0.8 V) compared to traditional water electrolysis www.sciencedirect.com
Greener processes for dark fermentative bioH2 production Kumar et al. 141
(1.23–3.5 V) and can be supplied by a solar panel or by MFC [69,78]. Higher external voltage leads to higher hydrogen production rate with more external energy consumption. It was suggested that a voltage of 0.6– 0.8 V can optimally balance the hydrogen production and energy efficiency [76]. The pH control plays a key role in hydrogen production in MECs [79]. MEC reactor design is one of the critical factors which directly influence hydrogen production rate [78]. Guo et al. developed a tubular double chamber MEC reactor that achieved a high hydrogen production rate of 7.10 L/L/d at 1.0 V [80]. Recently, the membrane-free MEC was used to obtain high hydrogen recovery and production rates at low internal resistance [78]. The overall hydrogen production for the integrated DF–MFC–MEC was increased by 41% compared with DF [71]. Biohythane generation
A mixture of fermentative hydrogen (5–20%) and anaerobic digestive methane (80–95%) called biohythane can be produced by the two-stage biological process to be commercially consumed as vehicle fuels in India and as energy storage material in Germany [81]. A two-stage hydrogen coupled methane production paths produce biohythane (>10% methane), developed by Sapporo Breweries Ltd. together with Shimadzu Corp. and Hiroshima University using bread waste as substrate. A semipilot scale two-stage hydrogen-methane plant utilized the kitchen, paper and food waste and was adopted by The Energy Technology Research Institute of the National Institute of Advanced Industrial Science and Technology in Japan. In hydrogen producing bioreactors, both the growth of hydrogenotrophic methanogenic archaea and increase in broth pH (to >7.5) should be avoidable. Using the food waste as a carbon source, the observed yields of biohydrogen and methane were found to be 147 300 and 383 000 L/kg VS/d respectively [36,38]. The two-stage hydrogen coupled methane production paths can be efficiently applied to the waste treatment [82,83], and it could accomplish higher hydrogen and methane production by favouring the hydrolysis step [81]. Circular biorefinery
Circular biorefinery of various biomass feedstocks is an industrial regenerative system that represents the production of wide spectrum of value added chemical products, food and feed ingredients, renewable energy via fermentation and chemical paths namely aqueous phase dehydration/hydrogenation (APD/H). Figure 1 depicts a possible design of circular biorefinery of residual biomasses to value added chemicals, food and feed ingredients [84]. Catalytic gasification of the biomass towards enhancement of hydrogen production is an attractive option [40]. The pretreatment techniques disrupt the recalcitrant cellulose–hemicellulose–lignin networks and release fermentable sugars. The effluents of organic matters from fermentation process can also be consumed www.sciencedirect.com
to generate biohydrogen by either dark or photo fermentation coupled with anaerobic digestion. The residues from the pretreatment consequently undergo enzymatic/ biochemical hydrolysis to form monomeric sugars and the hexose sugar moieties are simply fermented to alcohols. In addition, pentose moieties undergo co-fermentation to alcohols along with hexose sugars in a single reactor by SSF processes, which can improve the economics of biorefinery and there is a possibility of producing a good quantity of lignin as the by-product. Lignin can be changed to aromatic-ols with phenolic skeleton through lignin depolymerization and hydrodeoxygenation in the presence of protic solvents. In the biorefinery, the formedlevulinic acid can be transformed into a range of platform chemicals and value added products like resins, plasticizers and textiles. Figure 1 shows a series of elimination and carbon–carbon bond (–C–C–) forming reactions, involving these platform chemicals formations are aldol-condensation, ketonization, oligomerization, dehydration, decarbonylation, and decarboxylation respectively to fabricate hydrocarbon fuels and fuel additives. The formed products mainly consist of long-chain alkanes and alkenes, namely ethylene, propylene, butylenes, butadienes, long-chain terminal alkenes of carbons C6–C20, isoprenoids units of isoprene, farnesene, bisabolene and pinene by employing genetically engineered microorganisms, such as E. coli, S. cerevisiae, or cyanobacteria in the reaction pathway. Very few circular biorefinery analyses have been described for LCB like agricultural biomass, switch grass and wood, since various technologies used are still in the early stages of development [84,85]. Combined efforts from the State, academia, and industries are required for the development of LCB based biorefinery as a blooming industry.
Conclusions The development of large-scale biohydrogen production by DF is challenged by the high price associated with the feedstock, the development and operation of functional bioreactors and the thermodynamic limitations on the hydrogen yield by microbial fermentation. As a sustainable biofuel, biohydrogen also faces competition from other biofuels used in the transportation sector like biodiesel and other bio-based hydrocarbon fuels. With the current advances in feedstock pretreatment of LCB biomass and the increased recognition of hydrogen as a clean burning fuel via fuel cells, DF is an excellent avenue for biohydrogen production compared to other biological systems. Integration of other energy generating systems with DF enhances the energy recovery from the substrate. Having said this, the choice of the fermentative microorganism is of pivotal importance. Robust microbes with reasonable cellulolytic properties are of great demand to make biohydrogen production economically viable. Current Opinion in Biotechnology 2018, 50:136–145
142 Energy biotechnology
Figure 1 Organic biomass
H2+CH4 C2H5OH+Biodiesel
Biofuels
Biochemical path
Dark fermentation H2+CH4+CH3OH+C2H5OH +C3H7OH
Biochemicals Pharmaceuticals
Biochemicals (C3-C6)
VFAs (C2-C6) From effluents Separation of cell components CO2 Water & Nutrients Disruption of cells Light
Biopolymers
Propagation
Textiles
Crude stabilized stuffs
Algae species & Photobioreactors Waste water CO2 Liquid fuels Ash Nanomaterials NOX Combustion & Pyrolysis
Conversion, purification & formation of products
Pharmaceuticals Nutrients & Cosmetics Char & Energy Platform chemicals Feed materials
feedstock for lignocellulosic biorefinery
Current Opinion in Biotechnology
Depiction of a possible circular biorefinery design of residual biomasses to value-added chemicals, food and feed ingredients.
Conflict of interest
2.
Ren N-Q, Zhao L, Chen C, Guo W-Q, Cao G-L: A review on bioconversion of lignocellulosic biomass to H2: key challenges and new insights. Bioresour Technol 2016, 215:92-99.
3.
Kumar G, Sivagurunathan P, Sen B, Mudhoo A, Davila-Vazquez G, Wang G, Kim S-H: Research and development perspectives of lignocellulose-based biohydrogen production. Int Biodeterior Biodegrad 2017, 119:225-238.
None declared.
Acknowledgements This work was supported by Taiwan’s Ministry of Science and Technology (MOST) under grant numbers of MOST 106-3113-E-006-011, 106-3113-E006-004-CC2, 104-2221-E-006-227-MY3, and 103-2221-E-006-190-MY3.
Author GK acknowledge the financial assistance from Ton Duc Thang University, Ho chi Minh City, Vietnam.
References and recommended reading Papers of particular interest, published within the period of review, have been highlighted as:
4.
Sivagurunathan P, Kumar G, Bakonyi P, Kim S-H, Kobayashi T, Xu KQ, Lakner G, To´th G, Nemesto´thy N, Be´lafi-Bako´ K: A critical review on issues and overcoming strategies for the enhancement of dark fermentative hydrogen production in continuous systems. Int J Hydrogen Energy 2016, 41:3820-3836. Authors describe the major issues related with the continuous operation of hydrogen production and the relevant enhancement strategies such as immobilization, bio-augmentation and effluent recycling and others were highlighted for better production performances.
5.
Sivagurunathan P, Kumar G, Mudhoo A, Rene ER, Saratale GD, Kobayashi T, Xu K, Kim S-H, Kim D-H: Fermentative hydrogen production using lignocellulose biomass: an overview of pretreatment methods, inhibitor effects and detoxification experiences. Renew Sustain Energy Rev 2017, 77:28-42.
6.
Rajendran K, Drielak E, Sudarshan Varma V, Muthusamy S, Kumar G: Updates on the pretreatment of lignocellulosic feedstocks for bioenergy production — a review. Biomass Convers Biorefinery 2017 http://dx.doi.org/10.1007/s13399017-0269-3.
of special interest of outstanding interest 1.
Boodhun BSF, Mudhoo A, Kumar G, Kim S-H, Lin C-Y: Research perspectives on constraints, prospects and opportunities in biohydrogen production. Int J Hydrogen Energy 2017, 42: 27471-27481.
Current Opinion in Biotechnology 2018, 50:136–145
www.sciencedirect.com
Greener processes for dark fermentative bioH2 production Kumar et al. 143
7.
Sambusiti C, Bellucci M, Zabaniotou A, Beneduce L, Monlau F: Algae as promising feedstocks for fermentative biohydrogen production according to a biorefinery approach: a comprehensive review. Renew Sustain Energy Rev 2015, 44: 20-36.
8.
Sivagurunathan P, Kumar G, Kim S-H, Kobayashi T, Xu K-Q, Guo W, Hao Ngo H: Enhancement strategies for hydrogen production from wastewater: a review. Curr Org Chem 2016, 20:2744-2752.
9.
Chandrasekhar K, Lee YJ, Lee DW: Biohydrogen production: strategies to improve process efficiency through microbial routes. Int J Mol Sci 2015, 16:8266-8293.
10. Kumar G, Bakonyi P, Sivagurunathan P, Kim SH, Nemestothy N, Belafi-Bako K, Lin CY: Enhanced biohydrogen production from beverage industrial wastewater using external nitrogen sources and bioaugmentation with facultative anaerobic strains. J Biosci Bioeng 2015, 120:155-160. 11. Kumar G, Zhen G, Kobayashi T, Sivagurunathan P, Kim SH, Xu KQ: Impact of pH control and heat pre-treatment of seed inoculum in dark H2 fermentation: a feasibility report using mixed microalgae biomass as feedstock. Int J Hydrogen Energy 2016, 41:4382-4392. An interesting article that revels the major impact of controlling the pH at 5.5 and the combination effect of heat pretreatment of various inocula and proved that incoulum source play important role in the enrichment of hydrogen producers. 12. Kumar G, Sivagurunathan P, Pugazhendhi A, Thi NBD, Zhen G, Chandrasekhar K, Kadier A: A comprehensive overview on light independent fermentative hydrogen production from wastewater feedstock and possible integrative options. Energy Convers Manag 2017, 141:390-402. 13. Cao G, Ren N, Wang A, Lee D-J, Guo W, Liu B, Feng Y, Zhao Q: Acid hydrolysis of corn stover for biohydrogen production using Thermoanaerobacterium thermosaccharolyticum W16. Int J Hydrogen Energy 2009, 34:7182-7188. 14. Ren N-Q, Cao G-L, Guo W-Q, Wang A-J, Zhu Y-H, Liu B-f, Xu J-F: Biological hydrogen production from corn stover by moderately thermophile Thermoanaerobacterium thermosaccharolyticum W16. Int J Hydrogen Energy 2010, 35:2708-2712. 15. Liu C-z, Cheng X-y: Improved hydrogen production via thermophilic fermentation of corn stover by microwaveassisted acid pretreatment. Int J Hydrogen Energy 2010, 35:8945-8952. 16. Zhang K, Ren N-Q, Wang A-J: Fermentative hydrogen production from corn stover hydrolyzate by two typical seed sludges: effect of temperature. Int J Hydrogen Energy 2015, 40:3838-3848. 17. Kumar G, Bakonyi P, Periyasamy S, Kim SH, Nemesto´thy N, Be´lafi-Bako´ K: Lignocellulose biohydrogen: practical challenges and recent progress. Renew Sustain Energy Rev 2015, 44:728-737. This paper describes the technical barriers associated with the lignocellulose biohydrogen production by means of pretreatment and inhibitor formation along with the possible integration schemes to over come these barriers to improve the hydrogen production rates and yield are described and well documented. 18. Moreno AD, Olsson L: Pretreatment of lignocellulosic feedstocks. In Extremophilic Enzymatic Processing of Lignocellulosic Feedstocks to Bioenergy. Edited by Sani RK, Krishnaraj RN. Springer International Publishing; 2017:31-52. 19. Bakonyi P, Nemesto´thy N, Simon V, Be´lafi-Bako´ K: Review on the start-up experiences of continuous fermentative hydrogen producing bioreactors. Renew Sustain Energy Rev 2014, 40: 806-813. 20. Ren N, Guo W, Liu B, Cao G, Ding J: Biological hydrogen production by dark fermentation: challenges and prospects towards scaled-up production. Curr Opin Biotechnol 2011, 22:365-370. 21. Aparna D, Sudipta S: Sequencing batch reactor for wastewater treatment: recent advances. Curr Pollut Rep 2015, 1:177-190. www.sciencedirect.com
22. Show KY, Zhang ZP, Lee DJ: Design of bioreactors for biohydrogen production. J Sci Ind Res 2008, 67:941-949. 23. Ravi Kumar P, Pushpendra K, Ravi Dhar D, Delan Singh D: Production of biohydrogen gas from sewage wastewater by anaerobic fermentation process. Int J Chem Stud 2017, 5:35-38. 24. Pirsaheb M, Hossini H, Sebastia Secula M, Parvaneh M, Md Ashraf G: Application of high rate integrated anaerobicaerobic/biogranular activated carbon sequencing batch reactor (IAnA-BioGACSBR) for treating strong municipal landfill leachate. Sci Rep 2017 http://dx.doi.org/10.1038/s41598017-02936-1. 25. Saratale GD, Kshirsagar SD, Saratale RG, Govindwar SP, Oh M-K: Fermentative hydrogen production using sorghum husk as a biomass feedstock and process optimization. Biotechnol Bioprocess Eng 2015, 20:733-743. 26. Azman NF, Abdeshahian P, Kadier A, Nasser Al-Shorgani NK, Salih NKM, Lananan I, Hamid AA, Kalil MS: Biohydrogen production from de-oiled rice bran as sustainable feedstock in fermentative process. Int J Hydrogen Energy 2016, 41:145-156. 27. Kumar G, Mudhoo A, Sivagurunathan P, Nagarajan D, Ghimire A, Lay C-H, Lin C-Y, Lee D-J, Chang J-S: Recent insights into the cell immobilization technology applied for dark fermentative hydrogen production. Bioresour Technol 2016, 219:725-737. 28. Lutpi NA, Md Jahim J, Mumtaz T, Harun S, Abdul PM: Batch and continuous thermophilic hydrogen fermentation of sucrose using anaerobic sludge from palm oil mill effluent via immobilisation technique. Process Biochem 2016, 51:297-307. 29. Sivagurunathan P, Kumar G, Sen B, Lin C-Y: Development of a novel hybrid immobilization material (HY-IM) for fermentative biohydrogen production from beverage wastewater. J Chin Chem Soc 2014, 61:827-830. 30. Akinbomi J, Wikandari R, Taherzadeh MJ: Enhanced fermentative hydrogen and methane production from an inhibitory fruit-flavored medium with membraneencapsulated cells. Membranes 2015, 5:616-631. 31. Yun J, Kim TG, Cho K-S: Effect of PVA-Encapsulation on Hydrogen Production and Bacterial Community Structure. 2014. 32. Seelert T, Ghosh D, Yargeau V: Improving biohydrogen production using Clostridium beijerinckii immobilized with magnetite nanoparticles. Appl Microbiol Biotechnol 2015, 99:4107-4116. 33. Olson DG, McBride JE, Joe Shaw A, Lynd LR: Recent progress in consolidated bioprocessing. Curr Opin Biotechnol 2012, 23:396-405. 34. Lynd LR, Guss AM, Himmel ME, Beri D, Herring C, Holwerda EK, Murphy SJ, Olson DG, Paye J, Rydzak T et al.: Advances in consolidated bioprocessing using Clostridium thermocellum and Thermoanaerobacter saccharolyticum. Industrial Biotechnology. Wiley-VCH Verlag GmbH & Co. KGaA; 2017: 365-394. 35. Pang J, Liu ZY, Hao M, Zhang YF, Qi QS: An isolated cellulolytic Escherichia coli from bovine rumen produces ethanol and hydrogen from corn straw. Biotechnol Biofuels 2017, 10:165. 36. Ghosh D, Hallenbeck PC: Response surface methodology for process parameter optimization of hydrogen yield by the metabolically engineered strain Escherichia coli DJT135. Bioresour Technol 2010, 101:1820-1825. 37. Zverlov VV, Schantz N, Schwarz WH: A major new component in the cellulosome of Clostridium thermocellum is a processive endo-b-1,4-glucanase producing cellotetraose. FEMS Microbiol Lett 2005, 249:353-358. 38. Cheng J-R, Zhu M-J: Biohydrogen production from pretreated lignocellulose by Clostridium thermocellum. Biotechnol Bioprocess Eng 2016, 21:87-94. 39. Cheng J, Yu Y, Zhu M: Enhanced biodegradation of sugarcane bagasse by Clostridium thermocellum with surfactant addition. Green Chem 2014, 16:2689-2695. 40. Tian QQ, Liang L, Zhu MJ: Enhanced biohydrogen production from sugarcane bagasse by Clostridium thermocellum Current Opinion in Biotechnology 2018, 50:136–145
144 Energy biotechnology
supplemented with CaCO3. Bioresour Technol 2015, 197: 422-428. 41. Cheng X-Y, Liu C-Z: Hydrogen production via thermophilic fermentation of cornstalk by Clostridium thermocellum. Energy Fuels 2011, 25:1714-1720. 42. Dumitrache A, Akinosho H, Rodriguez M, Meng X, Yoo CG, Natzke J, Engle NL, Sykes RW, Tschaplinski TJ, Muchero W et al.: Consolidated bioprocessing of Populus using Clostridium (Ruminiclostridium) thermocellum: a case study on the impact of lignin composition and structure. Biotechnol Biofuels 2016, 9:31. 43. Hu B-B, Zhu M-J: Direct hydrogen production from dilute-acid pretreated sugarcane bagasse hydrolysate using the newly isolated Thermoanaerobacterium thermosaccharolyticum MJ1. Microb Cell Factories 2017, 16:77. 44. Cao G-L, Zhao L, Wang A-J, Wang Z-Y, Ren N-Q: Single-step bioconversion of lignocellulose to hydrogen using novel moderately thermophilic bacteria. Biotechnol Biofuels 2014, 7:82. 45. Zhao L, Cao G-L, Wang A-J, Ren H-Y, Zhang K, Ren N-Q: Consolidated bioprocessing performance of Thermoanaerobacterium thermosaccharolyticum M18 on fungal pretreated cornstalk for enhanced hydrogen production. Biotechnol Biofuels 2014, 7:178. 46. Sheng T, Gao L, Zhao L, Liu W, Wang A: Direct hydrogen production from lignocellulose by the newly isolated Thermoanaerobacterium thermosaccharolyticum strain DD32. RSC Adv 2015, 5:99781-99788. 47. Zurawski JV, Blumer-Schuette SE, Conway JM, Kelly RM: The extremely thermophilic genus Caldicellulosiruptor: physiological and genomic characteristics for complex carbohydrate conversion to molecular hydrogen. In Microbial BioEnergy: Hydrogen Production. Edited by Zannoni D, De Philippis R. Springer Netherlands; 2014:177-195. 48. Cha M, Chung D, Westpheling J: Deletion of a gene cluster for [Ni–Fe] hydrogenase maturation in the anaerobic hyperthermophilic bacterium Caldicellulosiruptor bescii identifies its role in hydrogen metabolism. Appl Microbiol Biotechnol 2016, 100:1823-1831. 49. Basen M, Rhaesa AM, Kataeva I, Prybol CJ, Scott IM, Poole FL, Adams MWW: Degradation of high loads of crystalline cellulose and of unpretreated plant biomass by the thermophilic bacterium Caldicellulosiruptor bescii. Bioresour Technol 2014, 152:384-392. 50. Yilmazel YD, Johnston D, Duran M: Hyperthermophilic hydrogen production from wastewater biosolids by Caldicellulosiruptor bescii. Int J Hydrogen Energy 2015, 40:12177-12186. 51. Talluri S, Raj SM, Christopher LP: Consolidated bioprocessing of untreated switchgrass to hydrogen by the extreme thermophile Caldicellulosiruptor saccharolyticus DSM 8903. Bioresour Technol 2013, 139:272-279. 52. Cha M, Chung D, Elkins JG, Guss AM, Westpheling J: Metabolic engineering of Caldicellulosiruptor bescii yields increased hydrogen production from lignocellulosic biomass. Biotechnol Biofuels 2013, 6:85. 53. Jung KA, Lim S-R, Kim Y, Park JM: Potentials of macroalgae as feedstocks for biorefinery. Bioresour Technol 2013, 135: 182-190. 54. Wang X, Ruan Z, Sheridan P, Boileau D, Liu Y, Liao W: Two-stage photoautotrophic cultivation to improve carbohydrate production in Chlamydomonas reinhardtii. Biomass Bioenergy 2015, 74:280-287.
57. Chen C-Y, Zhao X-Q, Yen H-W, Ho S-H, Cheng C-L, Lee D-J, Bai F-W, Chang J-S: Microalgae-based carbohydrates for biofuel production. Biochem Eng J 2013, 78:1-10. 58. Xia A, Jacob A, Tabassum MR, Herrmann C, Murphy JD: Production of hydrogen, ethanol and volatile fatty acids through co-fermentation of macro- and micro-algae. Bioresour Technol 2016, 205:118-125. 59. Batista AP, Ambrosano L, Grac¸a S, Sousa C, Marques PASS, Ribeiro B, Botrel EP, Castro Neto P, Gouveia L: Combining urban wastewater treatment with biohydrogen production — an integrated microalgae-based approach. Bioresour Technol 2015, 184:230-235. 60. Nobre BP, Villalobos F, Barraga´n BE, Oliveira AC, Batista AP, Marques PASS, Mendes RL, Sovova´ H, Palavra AF, Gouveia L: A biorefinery from Nannochloropsis sp. microalga — extraction of oils and pigments. Production of biohydrogen from the leftover biomass. Bioresour Technol 2013, 135:128-136. 61. Nguyen T.-A.D., Kim K-R, Nguyen M-T, Kim MS, Kim D, Sim SJ: Enhancement of fermentative hydrogen production from green algal biomass of Thermotoga neapolitana by various pretreatment methods. Int J Hydrogen Energy 2010, 35: 13035-13040. 62. Ghirardi ML, Dubini A, Yu J, Maness PC: Photobiological hydrogen-producing systems. Chem Soc Rev 2009, 38:52-61. 63. Nagarajan D, Lee D-J, Kondo A, Chang J-S: Recent insights into biohydrogen production by microalgae — from biophotolysis to dark fermentation. Bioresour Technol 2017, 227:373-387. 64. Melis A, Zhang L, Forestier M, Ghirardi ML, Seibert M: Sustained photobiological hydrogen gas production upon reversible inactivation of oxygen evolution in the green alga Chlamydomonas reinhardtii. Plant Physiol 2000, 122:127-136. An outstanding approach of approach of photobiological production of H (2) gas via the reversible hydrogenase pathway in the green alga Chlamydomonas reinhardtii. Two-stage H(2) production which involves at (stage 1) as circumventing the severe O(2) sensitivity of the reversible hydrogenase and in (stage 2) as temporally separating photosynthetic O (2) evolution and carbon accumulation from the consumption of cellular metabolites and concomitant H(2) production. 65. Bandyopadhyay A, Stockel J, Min H, Sherman LA, Pakrasi HB: High rates of photobiological H2 production by a cyanobacterium under aerobic conditions. Nat Commun 2010, 1:139. Authors describe about the potential of photobiological hydrogen production by oxygenic photosynthetic microbes by highlighting that nitrogenase and hydrogenase are generally oxygen sensitive, and require protective mechanisms to function in an aerobic extracellular environment. Authors took Cyanothece sp. ATCC 51142, a unicellular, diazotrophic cyanobacterium as an example with the capacity to generate high levels of hydrogen under aerobic conditions. 66. Hwang J-H, Kim H-C, Choi J-A, Abou-Shanab RAI, Dempsey BA, Regan JM, Kim JR, Song H, Nam I-H, Kim S-N et al.: Photoautotrophic hydrogen production by eukaryotic microalgae under aerobic conditions. Nat Commun 2014, 5:3234. 67. Chen C-Y, Yang M-H, Yeh K-L, Liu C-H, Chang J-S: Biohydrogen production using sequential two-stage dark and photo fermentation processes. Int J Hydrogen Energy 2008, 33: 4755-4762. 68. Pasupuleti SB, Srikanth S, Venkata Mohan S, Pant D: Continuous mode operation of microbial fuel cell (MFC) stack with dual gas diffusion cathode design for the treatment of dark fermentation effluent. Int J Hydrogen Energy 2015, 40: 12424-12435.
55. Zhu S, Wang Y, Huang W, Xu J, Wang Z, Xu J, Yuan Z: Enhanced accumulation of carbohydrate and starch in Chlorella zofingiensis induced by nitrogen starvation. Appl Biochem Biotechnol 2014, 174:2435-2445.
69. Wang A, Sun D, Cao G, Wang H, Ren N, Wu W-M, Logan BE: Integrated hydrogen production process from cellulose by combining dark fermentation, microbial fuel cells, and a microbial electrolysis cell. Bioresour Technol 2011, 102: 4137-4143.
56. Cheng D, Li D, Yuan Y, Zhou L, Li X, Wu T, Wang L, Zhao Q, Wei W, Sun Y: Improving carbohydrate and starch accumulation in Chlorella sp. AE10 by a novel two-stage process with cell dilution. Biotechnol Biofuels 2017, 10:75.
70. Liu C-H, Chang C-Y, Liao Q, Zhu X, Liao C-F, Chang J-S: Biohydrogen production by a novel integration of dark fermentation and mixotrophic microalgae cultivation. Int J Hydrogen Energy 2013, 38:15807-15814.
Current Opinion in Biotechnology 2018, 50:136–145
www.sciencedirect.com
Greener processes for dark fermentative bioH2 production Kumar et al. 145
Authors described about a unique and novel approach of cultivation of the mixotrophic culture of an isolated microalga (Chlorella vulgaris ESP6) to simultaneously consume CO2 and COD by-products from dark fermentation. 71. Santoro C, Arbizzani C, Erable B, Ieropoulos I: Microbial fuel cells: from fundamentals to applications. A review. J Power Sources 2017, 356:225-244. 72. Pandit S, Balachandar G, Das D: Improved energy recovery from dark fermented cane molasses using microbial fuel cells. Front Chem Sci Eng 2014, 8:43-54. 73. Varanasi J, Roy S, Pandit S, Das D: Improvement of energy recovery from cellobiose by thermophillic dark fermentative hydrogen production followed by microbial fuel cell. Int J Hydrogen Energy 2015, 40:8311-8321. 74. Varanasi JL, Sinha P, Das D: Maximizing power generation from dark fermentation effluents in microbial fuel cell by selective enrichment of exoelectrogens and optimization of anodic operational parameters. Biotechnol Lett 2017, 39:721-730. 75. Chookaew T, Prasertsan P, Ren ZJ: Two-stage conversion of crude glycerol to energy using dark fermentation linked with microbial fuel cell or microbial electrolysis cell. N Biotechnol 2014, 31:179-184. 76. Lu L, Ren ZJ: Microbial electrolysis cells for waste biorefinery: a state of the art review. Bioresour Technol 2016, 215:254-264. 77. Rivera I, Buitro´n G, Bakonyi P, Nemesto´thy N, Be´lafi-Bako´ K: Hydrogen production in a microbial electrolysis cell fed with a dark fermentation effluent. J Appl Electrochem 2015, 45: 1223-1229. 78. Kadier A, Simayi Y, Abdeshahian P, Azman NF, Chandrasekhar K, Kalil MS: A comprehensive review of microbial electrolysis cells (MEC) reactor designs and configurations for sustainable hydrogen gas production. Alex Eng J 2016, 55:427-443. 79. Yang Y, Qin M, Yang X, He Z: Enhancing hydrogen production in microbial electrolysis cells by in situ hydrogen oxidation for
www.sciencedirect.com
self-buffering pH through periodic polarity reversal. J Power Sources 2017, 347:21-28. 80. Guo K, Pre´voteau A, Rabaey K: A novel tubular microbial electrolysis cell for high rate hydrogen production. J Power Sources 2017, 356:484-490. 81. Tapia-Venegas E, Ramirez-Morales J, Silva-Illanes F, ToledoAlarco´n J, Paillet F, Escudie R, Lay CH, Chu CY, Leu HJ, Marone A, Lin CY, Kim DH, Trably E, Ruiz-Filippi G: Biohydrogen production by dark fermentation: scaling-up and technologies integration for a sustainable system. Rev Environ Sci Bio/Technol 2015, 14:761-785. 82. Liu L, Pang C, Wu S, Dong R: Optimization and evaluation of an air-recirculated stripping for ammonia removal from the anaerobic digestate of pig manure. Process Saf Environ Prot 2015, 94:350-357. 83. Malamis S, Katsou E, Di Fabio S, Bolzonella D, Fatone F: Biological nutrients removal from the supernatant originating from the anaerobic digestion of the organic fraction of municipal solid waste. Crit Rev Biotechnol 2014, 34:244-257. 84. Maity SK: Opportunities, recent trends and challenges of integrated biorefinery: Part I. Renew Sustain Energy Rev 2015, 43:1427-1445. In this review, author describes about the biomass classification of four general types based on their origin which are; energy crops, agricultural residues and waste, forestry waste and residues and industrial and municipal wastes. Additionally, further elucidation of the chemistry of various types of biomass used in the biorefinery is well explained. 85. Maity SK: Opportunities, recent trends and challenges of integrated biorefinery: Part II. Renew Sustain Energy Rev 2015, 43:1446-1466. This article presented an outline of opportunities and socio-technoeconomic challenges of various biomass processing technologies. Besides, overview of production of hydrocarbon fuels viz various biomass processing technologies such as hydrodeoxygenation of triglycerides, biosynthetic pathways and aqueous phase catalysis in hydrocarbon biorefinery was highlighted.
Current Opinion in Biotechnology 2018, 50:136–145
ScienceDirect Biomass based hydrogen production by dark fermentation — recent trends and opportunities for greener processes Gopalakrishnan Kumar1, Sutha Shobana2, Dillirani Nagarajan3,4, Duu-Jong Lee4,5, Kuo-Shing Lee6, Chiu-Yue Lin7, Chun-Yen Chen8 and Jo-Shu Chang3,9 The generation of biohydrogen as source of biofuel/bioenergy from the wide variety of biomass has gathered a substantial quantum of research efforts in several aspects. One of the major thrusts in this field has been the pursuit of technically sound and effective methods and/or approaches towards significant improvement in the bioconversion efficiency and enhanced biohydrogen yields. In this perspective, the present contribution showcases the views formulated based on the latest advances reported in dark fermentative biohydrogen production (DHFP), which is considered as the most feasible route for commercialization of biohydrogen. The potential prospects and future research avenues are also presented. Addresses 1 Green Processing, Bioremediation and Alternative Energies Research Group, Faculty of Environment and Labour Safety, Ton Duc Thang University, Ho Chi Minh City, Viet Nam 2 Department of Chemistry and Research Centre, Aditanar College of Arts and Science, Virapandianpatnam, Tiruchendur, Tamil Nadu, India 3 Department of Chemical Engineering, National Cheng-Kung University, Tainan, Taiwan 4 Department of Chemical Engineering, National Taiwan University, Taipei 10617, Taiwan 5 Department of Chemical Engineering, National Taiwan University of Science and Technology, Taipei 10607, Taiwan 6 Department of Safety Health and Environmental Engineering, Central Taiwan University of Science and Technology, Taichung, Taiwan 7 Department of Environmental Engineering and Science, Feng Chia University, Taichung, Taiwan 8 University Center for Bioscience and Biotechnology, National Cheng Kung University, Tainan 701, Taiwan 9 Research Center for Energy Technology and Strategy, National ChengKung University, Tainan, Taiwan Corresponding authors: Kumar, Gopalakrishnan ([email protected]), Lin, Chiu-Yue ([email protected]), Chang, Jo-Shu ([email protected])
Current Opinion in Biotechnology 2018, 50:136–145 This review comes from a themed issue on Energy biotechnology Edited by Akihiko Kondo
Introduction The impending lack of energy has instigated the search for eco-friendly, biodegradable, sustainable and costeffective biofuels from renewable carbon sources of various organic streams [1]. Among the biofuels, hydrogen from both renewable and non-renewable sources is highly promising because of its clean burning properties and its use in transportation and power generation sectors [2,3]. Dark fermentation (DF) or anaerobic fermentation for hydrogen production is the decomposition of organic carbon substrates using facultative or obligate anaerobic bacteria including but not exclusively Clostridium, Enterobacter, Bacillus and Escherichia coli. The pathway is described by the equations below. Glycolysis
Glucose ! Pyruvate Pyruvate þ Co A Reduction
þ 2FdðoxÞ ! Acetyl Co A þ 2FdðredÞ þ CO2
2FdðredÞ
Oxidation
!
Hydrogenase
2FdðoxÞ þ H2 "
The main soluble products are certain organic acids like acetate, propionate and butyrate along with ethanol [4,5]. Lignocellulosic biomass (LCB) is currently the most available biomass resource for biohydrogen production, but it is challenged by the recalcitrant nature of the biomass and the generation of potential fermentative inhibitors, based on the nature of the biomass and the pretreatment process used [6]. Microalgae and macroalgae are the third generation feedstock for hydrogen production [7], and wastewater treatment by DF is an alternate route to explore [8]. In this review, we explore the recent advances in biohydrogen production by DF, including feedstock, reactor design and other possible green processes.
https://doi.org/10.1016/j.copbio.2017.12.024 0958-1669/ã 2018 Elsevier Ltd. All rights reserved.
Green biomass processing for hydrogen production Natural and green biological pathways for hydrogen production are water-splitting photosynthesis, photo fermentation, DF and electro fermentation. The energy efficient
Current Opinion in Biotechnology 2018, 50:136–145
www.sciencedirect.com
Greener processes for dark fermentative bioH2 production Kumar et al. 137
hydrogen production mainly depends on the choice of a biocatalyst/inoculum involved in the bioprocess [9]. Production of hydrogen from industrial wastewater is considerably subjected to the type of inoculum, composition and nature of biodegradability and among them, the inoculum source plays a vital role [10,11]. Pretreatments and enhanced reactor designs for DF
Pretreatment of the substrates makes DF hydrogen selective by enrichment of acidogenic bacteria and inhibition of hydrogenotrophic methanogens [11,12]. Pretreatment techniques are categorized into physico-mechanical (extrusion and pyrolysis), physico-chemical (steam, ammonia fibre and CO2 explosion, hot water, wet-oxidation, sonification, microwave imposed), chemical (ozone, acid or alkaline, oxidative delignification, organo-solvation, and ionic liquid) and enzymatic pretreatments, among them the physico-chemical and chemical treatments are considered to be the most proficient pretreatment techniques [5]. Thermoanaerobacterium thermosaccharolyticum W16 produced 2.24 mol H2/mol sugar by using sulfuric acid-pretreated corn stover [13], while the NaOH-pretreated corn stover yielded 108.5 mmol/ L H2 when using the same inoculum incorporated with cellulose enzymolysis [14]. The thermophilic H2 production from mild acid and microwave pretreated corn stover was 1.53 mol H2/mol glucose, while the mesophilic fermentation of acid and steam explosion pretreated corn stover yielded 3.0 mol H2/mol glucose [15,16]. The hydrogen production rate and yield from pretreated algal biomass were about 62 mL/L d and 9.5 mL/g VSadded, respectively [11]. Optimal pretreatment methods must achieve high sugar recovery, chronological fractionation of biomass, formation of co-products, negligible formation of inhibitors, applicability to wide range of feedstock and cost-effectivity [17,18]. Table 1 shows biomass pretreatment methods for fermentative hydrogen production. Suspended bioreactors have been designed for large-scale biological hydrogen production using microorganisms viz. continuously stirred tank reactor (CSTR), anaerobic sequencing batch reactor (ASBR) and anaerobic membrane bioreactor (AnMBR) [19]. The immobilized bioreactors developed are the up-flow anaerobic sludge blanket reactor (UASB), expanded granular sludge bed reactor (EGSB), and anaerobic fluidized bed reactor (AFBR), with CSTR and UASB being the most consistently used bioreactors and anaerobic granular sludge bed (AnGSB) provides better performance towards hydrogen production. In the case of wastewater treatment, CSTR, ASBR, CSABR, CIGSBR and AGSBR were developed for the production of dark fermentative hydrogen. It was predicted that UASB and anaerobic filter (AF) reactors show some additional stable performances at a low HRT (i.e. 0.5 day), while in CSTR, operating at low HRTs might lead to biomass washout. In addition, UASB has widely been applied in laboratory/pilot-scale research and is www.sciencedirect.com
effective for converting organic wastes to biohydrogen [19,20]. Further, some fixed-bed reactors were also used to proficiently produce biohydrogen with easy operations, while poor mass transfer efficiency has been an intrinsic drawback of such system. Moreover, high-rate anaerobic sequencing batch reactor (AnSBR) is operated in chemostat using a continuously stirred reactor. Since the period for ‘Fill and React’ stages can be accustomed to instruct the AnSBR system a CSTR-like or a perfect PFR-like management characteristics [21]. Moreover, biofilm/granule based type reactor designs are suggested with the intention to retain more active and effective microbes [22]. Among the available reactor design opportunities for dark fermentative biological hydrogen production, the ASBR seems to have the best performance, in particular when using wastewater as the feed, due to its high efficiency in biological pollutants removal in the various phases during the operational process [23,24].
Process improvement strategies and cell immobilization systems for DF
The yield of hydrogen from DF is metabolically restricted to 4 mol H2/mol glucose, presenting the most important technical obstacle for its field uses [9]. Additional treatments are essential to discard the significant amounts of residual fermentative organic effluents of carbon-rich substrates into the environment [25]. Several two-stage processes have been adapted to augment biohydrogen production and to enhance hydrogen production [26]. Immobilized cell systems have been developed for largescale biohydrogen production by DF, including physical adsorption, covalent bonding, cross-linking, entrapment, and encapsulation methods. The most common immobilization method is physical adsorption which aids in effective mass transfer and carbon source consumption at short HRT with improved hydrogen productivity [27]. Immobilization of Thermotoga neapolitana cells on a cationic hydrogel resulted in a hydrogen yield of 3.3 mol H2/ mol glucose and a hydrogen production rate of about 50.6 mL/L/h. Immobilization of anaerobic sludge on activated carbon granules and thermophilic DF attained a hydrogen yield of 2.8 mol H2/mol hexose [28]. It was found that immobilization of H2-producing bacteria on some novel carriers, such as calcium-alginate amalgamactivated carbon, could promote biohydrogen production [29]. It was also observed that the encapsulated cells were more effective than the free cells for the production of biohydrogen [30]. Polyvinyl alcohol (PVA) encapsulation of Enterobacter sp. resulted in pronounced stability of the inoculum in a fed-batch reactor for biohydrogen production [31]. Immobilization of Clostridium beijerinckii NCIMB8052 in chitosan with magnetite nanoparticles and alginic acid polyelectrolytes enhanced the production of biohydrogen [32]. So far, the selection of an appropriate Current Opinion in Biotechnology 2018, 50:136–145
138 Energy biotechnology
Table 1 Biohydrogen productivity from various renewable feedstocks in dark fermentative hydrogen production Biomass type Lignocellulosic Beer lees Cornstalk
Pretreatment conditions 4% HCl (30 min, boiling) 0.6% HCl (90 C/2 hours), Trichoderma viridecellulase (50 C, 72 hours, pH 4.8) 0.2% HCl (30 min, boiling) Microbe additives (25 C, 15 days)
RCG Lawn grass Miscanthus
Poplar leaves Rice straw Soybean straw Sugarcane bagasse Sweet sorghum bagasse
P. chrysosporium (29 C, 15 days) 3% HCl (90 min, 121 C, autoclave) 4% HCl (30 min, boiling) 12% NaOH (70 C, 4 hours), commercial enzymes (45 C, 72 hours, pH 4.8) 2% Viscozyme L (50 C, 3 hours, pH 4) 10% NH4OH (60 min, 121 C) and 1% H2SO4 (50 min, 121 C) 4% HCl (30 min, boiling) 0.5% H2SO4 (60 min, 121 C, 1.47 bar) 10% NaOH (70 C, 4 hours), commercial cellulose (50 C, 24 hours, pH 5)
Inoculum
Highest H2 yield
Reference
1
Anaerobic mixed consortia Heat-pretreated anaerobic sludge
53.03 mL H2 g DB 126.22–141.29 mL H2 g1 DB
Enriched consortia from cow dung compost Aerated microbial consortium
149.69 mL H2 g1 DB 176.00 mL H2 g1 DB
Enriched mixed culture dominated by T. thermosaccharolyticum W16 89.30 mL H2 g1 DB
C. pasteurianum T. elfii DSM 9442
31.60 mL H2 g1 DB 35 C, 1 atm 72.21 mL H2 g1 DB 2280 mL H2 at 65 C, 1 atm
C. pasteurianum
44.92 mL H2 g1 DB
T. neapolitana
77.1 mL H2 g1 DB at 75 C, 1 atm 60.2 mL H2 g1 DB 44.0 mL H2 g1 DB
Enriched microbial culture
C. butiricum C. butiricum C. saccharolyticus
[14]
73.6 H2 mmol1: C6 sugars at 72 C, 1 atm
Fermentation characteristics Codiumfragil
Macroalgae
Ulva lactuca Green Gelidiumamansii
Porphyratenera
Red
Gracilariaverrucosa
Washed with fresh water, dried at 105 C, milled at 0.5 mm; batch bottles, pH 5, 35 C Washed with fresh water, dried at room temperature, milled; batch bottles, 35 C Washed with fresh water, dried at 105 C, milled at 0.5 mm; batch bottles, pH 5.5, 35 C Washed with fresh water, dried at room temperature, milled; batch bottles, 35 C Washed with fresh water, dried at 105 C, milled at 0.5 mm; batch bottles, pH 5.5, 35 C Washed with fresh water, dried at 105 C, milled at 0.5 mm; batch bottles, pH 5.5, 35 C
WWTP anaerobic digester sludge, heat pretreated: 90 C, 20 min
24.4 mL g1 TS
WWTP anaerobic digester sludge
10.0 mL g1 TS/ mL H2 g1 algae
WWTP anaerobic digester sludge, pretreated at 90 C, 20 min
43.1 mL g1 TS
WWTP anaerobic digester sludge
9.0 mL g1 TS/ mL H2 g1 algae
WWTP anaerobic digester sludge, pretreated at 90 C, 20 min
15.4 mL g1 TS
WWTP anaerobic digester sludge, pretreated at 90 C, 20 min
Brown
Washed with fresh water, dry at 105 C, milled at 0.5 mm
Current Opinion in Biotechnology 2018, 50:136–145
26.7 mL g
TS
67.0 mL g1 TS 71.4 mL g1 TS
Laminaria japonica Dried at room temperature, milled at 0.5 mm; batch bottles, pH 5.5, 35 C Dried at room temperature, milled at 0.5 mm
[10] 1
Anaerobic sequencing batch reactor (ASBR), HRT = 6 days, OLR = 3.4 g COD L1 d1, pH = 5.5, T = 35 C
61.3 mL g1 TS
58.5–34.1 mL g1 TS
www.sciencedirect.com
Greener processes for dark fermentative bioH2 production Kumar et al. 139
Table 1 (Continued ) Fermentation characteristics Microalgae
Chlamydomonas reinhardtii
D. tertiolecta sp.
Nannochloropsis sp.
Scenedesmus sp.
Harvested by centrifugation (6000 g, 15 min); batch bottles, 37 C Harvested by flocculation followed by centrifugation, pH adjusted to 7 and stored at 20 C; batch bottles, 30 C Harvested by flocculation followed by centrifugation, pH adjusted to 7 and stored at 20 C; batch bottles, 37 C Harvested by centrifugation (5000 g), oven dried and powdered to 0.02 mm mesh size; batch bottles, 30 C Harvested by centrifugation at 10 000 rpm for 10 min, dried in an oven at 70 C, grounding, extraction of lipids by supercritical fluid extraction; batch bottles, 30 C Harvested by centrifugation at 10 000 rpm for 10 min, dried in an oven at 70 C, grounding, extraction of lipids by Soxhlet extraction Harvested by centrifugation at 10 000 rpm for 10 min, dried in an oven at 70 C; batch bottles, 37 C, pH 6.5
Category Wastewater
Rice mill WW BWW Distillery effluent Cassava WW Cassava starch processing WW Organic WW Textile WW Sugar beet juice
Pure culture C. butyricum NCIB 9576
40 mL g1 TS
Enrichment of compost pile
58.0 mL g1 TS/ mL H2 g1 algae
Produced by bacteria naturally present in microalgal biomass slurry, methanogenesis suppressed by 20 m MBESA Enterobacter aerogenes ATCC 13048
13 mL g1 TS
48.0 mL g1 TS
49.5–60.6 mL g1 TS
[10,34]
50.5 mL g1 TS
WWTP anaerobic digester sludge, pretreated at 95 C, 30 min
Inoculum Enterobacter aerogens EMC+ E. coli XL1 blue + Enterobacter cloacae Enterobacter cloacae C. acetobuytlicum ATCC824 EMC Romani hot spring Soil Anaerobic sludge Anaerobic digested sludge
21 mL g1 TS
Hydrogen yield (mol/mol hexose added; batch hydrogen production) 1.74 mol/mol sugar 260 mL (0.01 mol) 165.3 mL/g COD 2.41 mol/mol glucose [4,5] 128.4 mL/g starch 2.32 mol/mol 1.37 mol/mol 3.2 mol/mol
DB = dry biomass; RCG = reed canary grass; BWW = beverage wastewater; EMC = enriched mixed culture.
immobilization method is extremely specific to the dark fermentative bioreactors and hydrogen producers [27]. Consolidated bioprocessing (CBP) for DF
CBP is the integration of hydrolysis and fermentation of biomass to the desired product, which lowers the energy inputs and equipment requirements of the conventional multi-step fermentation process [33]. In case of hydrogen production, CBP can be applied for the direct conversion of LCB to hydrogen. CBP microbes that can be of great potential in hydrogen production are of the genera Clostridium, Thermoanaerobacter [34], E. coli and Caldicellulosiruptor. A rumen derived E. coli loaded with www.sciencedirect.com
a variety of extracellular glucanase activity was isolated and it produced 4.75 mL H2/g of untreated corn straw [35]. This opens new possibilities in native cellulolytic strategy for CBP, as E. coli is the most studied bacteria with a well-defined molecular toolkit and it has been modified previously for hydrogen production [36]. Clostridium species, Clostridium thermocellum in particular, has an extracellular cellulosome with 24 distinct glucanases that aid in the degradation of hemicellulose, cellulose and lignin [37]. C. thermocellum is believed to be highly efficient in plant cell wall destabilization compared to fungal cellulases [34]. C. thermocellum has been successfully used for the CBP of untreated and pretreated sugarcane Current Opinion in Biotechnology 2018, 50:136–145
140 Energy biotechnology
bagasse [38–40], corn stalk [41] and untreated biomass of Populustrichocarpa [42]. T. thermosaccharolyticum is a moderately thermophilic H2 producing anaerobic bacterium capable of utilizing pretreated and untreated LCB. The bacterium is resistant to the common fermentative inhibitors like furfural and 5-hydroxymethyl furfural [43]. It could generate around 3.5 mmol H2 per g substrate for untreated corn stalk [44], and with simple fungal pretreatment, the hydrogen yield from corn stalk increased to 7 mmol H2 per g substrate [45]. Some strains could achieve higher yields from untreated LCB, as high as 6.8 mmol H2 per g substrate from corn stalk [46]. Caldicellulosiruptor bescii is another potential CBP candidate for biohydrogen production. C. bescii is a hyperthermophilic, anaerobic, Gram positive bacterium, with the potential for utilizing diverse substrates via a mixed acid fermentation pathway producing hydrogen with yields as high as 4 mol H2 per mol glucose as indicated by the Thauer limit [47]. Hydrogen production is mediated by a [Fe–Fe] bifurcating hydrogenase [48] which allows higher yields compared to the facultative anaerobes like E. coli. C. bescii is capable of growth and hydrogen production from crystalline cellulose and raw LCB like switch grass [49], wastewater biosolids [50], as C. saccharolyticus could produce 14 mmol H2/L from untreated switch grass [51]. Deletion of the lactate dehydrogenase gene in C. bescii enhanced hydrogen production from switch grass [52–54], completely funnelling the carbon to hydrogen.
Opportunities and future trends Algae-based H2 production via DF and water-splitting photosynthesis
Microalgae and macroalgae are an attractive feedstock for biohydrogen production, as they are devoid of lignin, thus reducing the complexities of pretreatment. The carbohydrates present in microalgae including green algae and cyanobacteria are simple polyglucans like starch and glycogen, while macroalgae are composed of different sugar acids and sugar alcohols like glucuronic acid and mannitol [55]. Nutrient deprivation strategies like nitrogen or sulfur depletion has been applied successfully for the accumulation of carbohydrates in microalgae. Carbohydrate content in the range of 60–70% has been attained by various cultivation strategies from Chlamydomonas sp. and Chlorella sp. [54–56]. Microalgal cell walls are composed of cellulose and hemicellulose, which upon hydrolysis releases fermentable sugars. Mild acid/alkali hydrolysis, in combination with thermal pretreatment can effectively release the component sugars for fermentation [57]. Micro and macroalgae can be co-fermented to increase the carbon/nitrogen ratio in case of protein rich microalgae [58]. The feedstock price can be greatly reduced by using algae obtained from wastewater treatment [59] or lipid extracted microalgal biomass from the biodiesel industry [60]. The microalgal consortium obtained from wastewater with a sugar content of 28% yielded 47 mL H2/g VS [61], while the leftover biomass Current Opinion in Biotechnology 2018, 50:136–145
of Nannochloropsis sp. yielded 60.6 mL H2/g dry biomass [60]. The quality of these algae might not be adequate for food or feed industry, and the residual energy can be recovered by DF. The use of saccharolytic species like T. neapolitana as the fermentative bacterium in a thermophilic process can lower the pretreatment costs and increase hydrogen yields from thermodynamic aspects and simple cell disruption to release the stored starch would suffice the fermentation needs in simultaneous saccharification and fermentation (SSF) [61]. In addition, microalgae and cyanobacteria are capable of evolving hydrogen under specific physiological conditions. The green algal [Fe–Fe] hydrogenases are very efficient with high turnover rates of 6000–9000 s1 making microalgae an attractive source for biological hydrogen production, but they are highly sensitive to oxygen and are induced under specific anoxic conditions [62]. Hydrogen evolution in microalgae is transient and hence attaining sustained production and the oxygen sensitivity of the hydrogenases are the major bottlenecks in this green method for hydrogen production [63]. Anaerobiosis for sustained hydrogen production in microalgae has been achieved by certain culture strategies. Under sulfur deprivation which prevents the reconstruction of damaged PSII blocking oxygen evolution, sustained hydrogen production can be attained in Chlamydomonas reinhardtii via a two-stage indirect biophotolysis strategy with a hydrogen accumulation of up to 2 mL h1 for 160 hours [64]. Hydrogen production under aerobic conditions has been reported for the cyanobacteria Cyanothece sp. (465 mmol H2 (mg chlorophyll)1 h1) [65] and the green alga Chlorella vulgaris (1.2–2 mL L1) [66], alleviating the necessity of maintaining anaerobic conditions in an aerobic organism like microalgae. Integrated configurations combining photofermentation and electro-fermentation
The COD rich DF effluent can be further processed by various methods for the complete recovery of energy like photo-fermentation [67], microbial fuel cells (MFCs) [68], microbial electrolysis cells [69] and as an organic carbon source for microalgal cultivation [70]. A MFC has exoelectrogens to oxidize organic matter at anode surface and to reduce the yielded protons at cathode surface to produce water and electricity generated [71]. Thus, integrated DF and MFC can remove COD from spent liquor of DF unit with energy recovery [72]. Varanasi et al. used an integrated approach of combining thermophilic hydrogen fermentation from cellulosic substrate with MFC [73,74]. The integration of DF + MFC produced 0.55 mol H2/mol glycerol from crude glycerol with 20% COD removal [75]. In MEC, an external voltage is applied to drive electrons so hydrogen can be formed by proton reduction at the cathode. The integrated DF and MEC can achieve high hydrogen production yield and rate [76,77]. MECs require relatively low voltage (0.2–0.8 V) compared to traditional water electrolysis www.sciencedirect.com
Greener processes for dark fermentative bioH2 production Kumar et al. 141
(1.23–3.5 V) and can be supplied by a solar panel or by MFC [69,78]. Higher external voltage leads to higher hydrogen production rate with more external energy consumption. It was suggested that a voltage of 0.6– 0.8 V can optimally balance the hydrogen production and energy efficiency [76]. The pH control plays a key role in hydrogen production in MECs [79]. MEC reactor design is one of the critical factors which directly influence hydrogen production rate [78]. Guo et al. developed a tubular double chamber MEC reactor that achieved a high hydrogen production rate of 7.10 L/L/d at 1.0 V [80]. Recently, the membrane-free MEC was used to obtain high hydrogen recovery and production rates at low internal resistance [78]. The overall hydrogen production for the integrated DF–MFC–MEC was increased by 41% compared with DF [71]. Biohythane generation
A mixture of fermentative hydrogen (5–20%) and anaerobic digestive methane (80–95%) called biohythane can be produced by the two-stage biological process to be commercially consumed as vehicle fuels in India and as energy storage material in Germany [81]. A two-stage hydrogen coupled methane production paths produce biohythane (>10% methane), developed by Sapporo Breweries Ltd. together with Shimadzu Corp. and Hiroshima University using bread waste as substrate. A semipilot scale two-stage hydrogen-methane plant utilized the kitchen, paper and food waste and was adopted by The Energy Technology Research Institute of the National Institute of Advanced Industrial Science and Technology in Japan. In hydrogen producing bioreactors, both the growth of hydrogenotrophic methanogenic archaea and increase in broth pH (to >7.5) should be avoidable. Using the food waste as a carbon source, the observed yields of biohydrogen and methane were found to be 147 300 and 383 000 L/kg VS/d respectively [36,38]. The two-stage hydrogen coupled methane production paths can be efficiently applied to the waste treatment [82,83], and it could accomplish higher hydrogen and methane production by favouring the hydrolysis step [81]. Circular biorefinery
Circular biorefinery of various biomass feedstocks is an industrial regenerative system that represents the production of wide spectrum of value added chemical products, food and feed ingredients, renewable energy via fermentation and chemical paths namely aqueous phase dehydration/hydrogenation (APD/H). Figure 1 depicts a possible design of circular biorefinery of residual biomasses to value added chemicals, food and feed ingredients [84]. Catalytic gasification of the biomass towards enhancement of hydrogen production is an attractive option [40]. The pretreatment techniques disrupt the recalcitrant cellulose–hemicellulose–lignin networks and release fermentable sugars. The effluents of organic matters from fermentation process can also be consumed www.sciencedirect.com
to generate biohydrogen by either dark or photo fermentation coupled with anaerobic digestion. The residues from the pretreatment consequently undergo enzymatic/ biochemical hydrolysis to form monomeric sugars and the hexose sugar moieties are simply fermented to alcohols. In addition, pentose moieties undergo co-fermentation to alcohols along with hexose sugars in a single reactor by SSF processes, which can improve the economics of biorefinery and there is a possibility of producing a good quantity of lignin as the by-product. Lignin can be changed to aromatic-ols with phenolic skeleton through lignin depolymerization and hydrodeoxygenation in the presence of protic solvents. In the biorefinery, the formedlevulinic acid can be transformed into a range of platform chemicals and value added products like resins, plasticizers and textiles. Figure 1 shows a series of elimination and carbon–carbon bond (–C–C–) forming reactions, involving these platform chemicals formations are aldol-condensation, ketonization, oligomerization, dehydration, decarbonylation, and decarboxylation respectively to fabricate hydrocarbon fuels and fuel additives. The formed products mainly consist of long-chain alkanes and alkenes, namely ethylene, propylene, butylenes, butadienes, long-chain terminal alkenes of carbons C6–C20, isoprenoids units of isoprene, farnesene, bisabolene and pinene by employing genetically engineered microorganisms, such as E. coli, S. cerevisiae, or cyanobacteria in the reaction pathway. Very few circular biorefinery analyses have been described for LCB like agricultural biomass, switch grass and wood, since various technologies used are still in the early stages of development [84,85]. Combined efforts from the State, academia, and industries are required for the development of LCB based biorefinery as a blooming industry.
Conclusions The development of large-scale biohydrogen production by DF is challenged by the high price associated with the feedstock, the development and operation of functional bioreactors and the thermodynamic limitations on the hydrogen yield by microbial fermentation. As a sustainable biofuel, biohydrogen also faces competition from other biofuels used in the transportation sector like biodiesel and other bio-based hydrocarbon fuels. With the current advances in feedstock pretreatment of LCB biomass and the increased recognition of hydrogen as a clean burning fuel via fuel cells, DF is an excellent avenue for biohydrogen production compared to other biological systems. Integration of other energy generating systems with DF enhances the energy recovery from the substrate. Having said this, the choice of the fermentative microorganism is of pivotal importance. Robust microbes with reasonable cellulolytic properties are of great demand to make biohydrogen production economically viable. Current Opinion in Biotechnology 2018, 50:136–145
142 Energy biotechnology
Figure 1 Organic biomass
H2+CH4 C2H5OH+Biodiesel
Biofuels
Biochemical path
Dark fermentation H2+CH4+CH3OH+C2H5OH +C3H7OH
Biochemicals Pharmaceuticals
Biochemicals (C3-C6)
VFAs (C2-C6) From effluents Separation of cell components CO2 Water & Nutrients Disruption of cells Light
Biopolymers
Propagation
Textiles
Crude stabilized stuffs
Algae species & Photobioreactors Waste water CO2 Liquid fuels Ash Nanomaterials NOX Combustion & Pyrolysis
Conversion, purification & formation of products
Pharmaceuticals Nutrients & Cosmetics Char & Energy Platform chemicals Feed materials
feedstock for lignocellulosic biorefinery
Current Opinion in Biotechnology
Depiction of a possible circular biorefinery design of residual biomasses to value-added chemicals, food and feed ingredients.
Conflict of interest
2.
Ren N-Q, Zhao L, Chen C, Guo W-Q, Cao G-L: A review on bioconversion of lignocellulosic biomass to H2: key challenges and new insights. Bioresour Technol 2016, 215:92-99.
3.
Kumar G, Sivagurunathan P, Sen B, Mudhoo A, Davila-Vazquez G, Wang G, Kim S-H: Research and development perspectives of lignocellulose-based biohydrogen production. Int Biodeterior Biodegrad 2017, 119:225-238.
None declared.
Acknowledgements This work was supported by Taiwan’s Ministry of Science and Technology (MOST) under grant numbers of MOST 106-3113-E-006-011, 106-3113-E006-004-CC2, 104-2221-E-006-227-MY3, and 103-2221-E-006-190-MY3.
Author GK acknowledge the financial assistance from Ton Duc Thang University, Ho chi Minh City, Vietnam.
References and recommended reading Papers of particular interest, published within the period of review, have been highlighted as:
4.
Sivagurunathan P, Kumar G, Bakonyi P, Kim S-H, Kobayashi T, Xu KQ, Lakner G, To´th G, Nemesto´thy N, Be´lafi-Bako´ K: A critical review on issues and overcoming strategies for the enhancement of dark fermentative hydrogen production in continuous systems. Int J Hydrogen Energy 2016, 41:3820-3836. Authors describe the major issues related with the continuous operation of hydrogen production and the relevant enhancement strategies such as immobilization, bio-augmentation and effluent recycling and others were highlighted for better production performances.
5.
Sivagurunathan P, Kumar G, Mudhoo A, Rene ER, Saratale GD, Kobayashi T, Xu K, Kim S-H, Kim D-H: Fermentative hydrogen production using lignocellulose biomass: an overview of pretreatment methods, inhibitor effects and detoxification experiences. Renew Sustain Energy Rev 2017, 77:28-42.
6.
Rajendran K, Drielak E, Sudarshan Varma V, Muthusamy S, Kumar G: Updates on the pretreatment of lignocellulosic feedstocks for bioenergy production — a review. Biomass Convers Biorefinery 2017 http://dx.doi.org/10.1007/s13399017-0269-3.
of special interest of outstanding interest 1.
Boodhun BSF, Mudhoo A, Kumar G, Kim S-H, Lin C-Y: Research perspectives on constraints, prospects and opportunities in biohydrogen production. Int J Hydrogen Energy 2017, 42: 27471-27481.
Current Opinion in Biotechnology 2018, 50:136–145
www.sciencedirect.com
Greener processes for dark fermentative bioH2 production Kumar et al. 143
7.
Sambusiti C, Bellucci M, Zabaniotou A, Beneduce L, Monlau F: Algae as promising feedstocks for fermentative biohydrogen production according to a biorefinery approach: a comprehensive review. Renew Sustain Energy Rev 2015, 44: 20-36.
8.
Sivagurunathan P, Kumar G, Kim S-H, Kobayashi T, Xu K-Q, Guo W, Hao Ngo H: Enhancement strategies for hydrogen production from wastewater: a review. Curr Org Chem 2016, 20:2744-2752.
9.
Chandrasekhar K, Lee YJ, Lee DW: Biohydrogen production: strategies to improve process efficiency through microbial routes. Int J Mol Sci 2015, 16:8266-8293.
10. Kumar G, Bakonyi P, Sivagurunathan P, Kim SH, Nemestothy N, Belafi-Bako K, Lin CY: Enhanced biohydrogen production from beverage industrial wastewater using external nitrogen sources and bioaugmentation with facultative anaerobic strains. J Biosci Bioeng 2015, 120:155-160. 11. Kumar G, Zhen G, Kobayashi T, Sivagurunathan P, Kim SH, Xu KQ: Impact of pH control and heat pre-treatment of seed inoculum in dark H2 fermentation: a feasibility report using mixed microalgae biomass as feedstock. Int J Hydrogen Energy 2016, 41:4382-4392. An interesting article that revels the major impact of controlling the pH at 5.5 and the combination effect of heat pretreatment of various inocula and proved that incoulum source play important role in the enrichment of hydrogen producers. 12. Kumar G, Sivagurunathan P, Pugazhendhi A, Thi NBD, Zhen G, Chandrasekhar K, Kadier A: A comprehensive overview on light independent fermentative hydrogen production from wastewater feedstock and possible integrative options. Energy Convers Manag 2017, 141:390-402. 13. Cao G, Ren N, Wang A, Lee D-J, Guo W, Liu B, Feng Y, Zhao Q: Acid hydrolysis of corn stover for biohydrogen production using Thermoanaerobacterium thermosaccharolyticum W16. Int J Hydrogen Energy 2009, 34:7182-7188. 14. Ren N-Q, Cao G-L, Guo W-Q, Wang A-J, Zhu Y-H, Liu B-f, Xu J-F: Biological hydrogen production from corn stover by moderately thermophile Thermoanaerobacterium thermosaccharolyticum W16. Int J Hydrogen Energy 2010, 35:2708-2712. 15. Liu C-z, Cheng X-y: Improved hydrogen production via thermophilic fermentation of corn stover by microwaveassisted acid pretreatment. Int J Hydrogen Energy 2010, 35:8945-8952. 16. Zhang K, Ren N-Q, Wang A-J: Fermentative hydrogen production from corn stover hydrolyzate by two typical seed sludges: effect of temperature. Int J Hydrogen Energy 2015, 40:3838-3848. 17. Kumar G, Bakonyi P, Periyasamy S, Kim SH, Nemesto´thy N, Be´lafi-Bako´ K: Lignocellulose biohydrogen: practical challenges and recent progress. Renew Sustain Energy Rev 2015, 44:728-737. This paper describes the technical barriers associated with the lignocellulose biohydrogen production by means of pretreatment and inhibitor formation along with the possible integration schemes to over come these barriers to improve the hydrogen production rates and yield are described and well documented. 18. Moreno AD, Olsson L: Pretreatment of lignocellulosic feedstocks. In Extremophilic Enzymatic Processing of Lignocellulosic Feedstocks to Bioenergy. Edited by Sani RK, Krishnaraj RN. Springer International Publishing; 2017:31-52. 19. Bakonyi P, Nemesto´thy N, Simon V, Be´lafi-Bako´ K: Review on the start-up experiences of continuous fermentative hydrogen producing bioreactors. Renew Sustain Energy Rev 2014, 40: 806-813. 20. Ren N, Guo W, Liu B, Cao G, Ding J: Biological hydrogen production by dark fermentation: challenges and prospects towards scaled-up production. Curr Opin Biotechnol 2011, 22:365-370. 21. Aparna D, Sudipta S: Sequencing batch reactor for wastewater treatment: recent advances. Curr Pollut Rep 2015, 1:177-190. www.sciencedirect.com
22. Show KY, Zhang ZP, Lee DJ: Design of bioreactors for biohydrogen production. J Sci Ind Res 2008, 67:941-949. 23. Ravi Kumar P, Pushpendra K, Ravi Dhar D, Delan Singh D: Production of biohydrogen gas from sewage wastewater by anaerobic fermentation process. Int J Chem Stud 2017, 5:35-38. 24. Pirsaheb M, Hossini H, Sebastia Secula M, Parvaneh M, Md Ashraf G: Application of high rate integrated anaerobicaerobic/biogranular activated carbon sequencing batch reactor (IAnA-BioGACSBR) for treating strong municipal landfill leachate. Sci Rep 2017 http://dx.doi.org/10.1038/s41598017-02936-1. 25. Saratale GD, Kshirsagar SD, Saratale RG, Govindwar SP, Oh M-K: Fermentative hydrogen production using sorghum husk as a biomass feedstock and process optimization. Biotechnol Bioprocess Eng 2015, 20:733-743. 26. Azman NF, Abdeshahian P, Kadier A, Nasser Al-Shorgani NK, Salih NKM, Lananan I, Hamid AA, Kalil MS: Biohydrogen production from de-oiled rice bran as sustainable feedstock in fermentative process. Int J Hydrogen Energy 2016, 41:145-156. 27. Kumar G, Mudhoo A, Sivagurunathan P, Nagarajan D, Ghimire A, Lay C-H, Lin C-Y, Lee D-J, Chang J-S: Recent insights into the cell immobilization technology applied for dark fermentative hydrogen production. Bioresour Technol 2016, 219:725-737. 28. Lutpi NA, Md Jahim J, Mumtaz T, Harun S, Abdul PM: Batch and continuous thermophilic hydrogen fermentation of sucrose using anaerobic sludge from palm oil mill effluent via immobilisation technique. Process Biochem 2016, 51:297-307. 29. Sivagurunathan P, Kumar G, Sen B, Lin C-Y: Development of a novel hybrid immobilization material (HY-IM) for fermentative biohydrogen production from beverage wastewater. J Chin Chem Soc 2014, 61:827-830. 30. Akinbomi J, Wikandari R, Taherzadeh MJ: Enhanced fermentative hydrogen and methane production from an inhibitory fruit-flavored medium with membraneencapsulated cells. Membranes 2015, 5:616-631. 31. Yun J, Kim TG, Cho K-S: Effect of PVA-Encapsulation on Hydrogen Production and Bacterial Community Structure. 2014. 32. Seelert T, Ghosh D, Yargeau V: Improving biohydrogen production using Clostridium beijerinckii immobilized with magnetite nanoparticles. Appl Microbiol Biotechnol 2015, 99:4107-4116. 33. Olson DG, McBride JE, Joe Shaw A, Lynd LR: Recent progress in consolidated bioprocessing. Curr Opin Biotechnol 2012, 23:396-405. 34. Lynd LR, Guss AM, Himmel ME, Beri D, Herring C, Holwerda EK, Murphy SJ, Olson DG, Paye J, Rydzak T et al.: Advances in consolidated bioprocessing using Clostridium thermocellum and Thermoanaerobacter saccharolyticum. Industrial Biotechnology. Wiley-VCH Verlag GmbH & Co. KGaA; 2017: 365-394. 35. Pang J, Liu ZY, Hao M, Zhang YF, Qi QS: An isolated cellulolytic Escherichia coli from bovine rumen produces ethanol and hydrogen from corn straw. Biotechnol Biofuels 2017, 10:165. 36. Ghosh D, Hallenbeck PC: Response surface methodology for process parameter optimization of hydrogen yield by the metabolically engineered strain Escherichia coli DJT135. Bioresour Technol 2010, 101:1820-1825. 37. Zverlov VV, Schantz N, Schwarz WH: A major new component in the cellulosome of Clostridium thermocellum is a processive endo-b-1,4-glucanase producing cellotetraose. FEMS Microbiol Lett 2005, 249:353-358. 38. Cheng J-R, Zhu M-J: Biohydrogen production from pretreated lignocellulose by Clostridium thermocellum. Biotechnol Bioprocess Eng 2016, 21:87-94. 39. Cheng J, Yu Y, Zhu M: Enhanced biodegradation of sugarcane bagasse by Clostridium thermocellum with surfactant addition. Green Chem 2014, 16:2689-2695. 40. Tian QQ, Liang L, Zhu MJ: Enhanced biohydrogen production from sugarcane bagasse by Clostridium thermocellum Current Opinion in Biotechnology 2018, 50:136–145
144 Energy biotechnology
supplemented with CaCO3. Bioresour Technol 2015, 197: 422-428. 41. Cheng X-Y, Liu C-Z: Hydrogen production via thermophilic fermentation of cornstalk by Clostridium thermocellum. Energy Fuels 2011, 25:1714-1720. 42. Dumitrache A, Akinosho H, Rodriguez M, Meng X, Yoo CG, Natzke J, Engle NL, Sykes RW, Tschaplinski TJ, Muchero W et al.: Consolidated bioprocessing of Populus using Clostridium (Ruminiclostridium) thermocellum: a case study on the impact of lignin composition and structure. Biotechnol Biofuels 2016, 9:31. 43. Hu B-B, Zhu M-J: Direct hydrogen production from dilute-acid pretreated sugarcane bagasse hydrolysate using the newly isolated Thermoanaerobacterium thermosaccharolyticum MJ1. Microb Cell Factories 2017, 16:77. 44. Cao G-L, Zhao L, Wang A-J, Wang Z-Y, Ren N-Q: Single-step bioconversion of lignocellulose to hydrogen using novel moderately thermophilic bacteria. Biotechnol Biofuels 2014, 7:82. 45. Zhao L, Cao G-L, Wang A-J, Ren H-Y, Zhang K, Ren N-Q: Consolidated bioprocessing performance of Thermoanaerobacterium thermosaccharolyticum M18 on fungal pretreated cornstalk for enhanced hydrogen production. Biotechnol Biofuels 2014, 7:178. 46. Sheng T, Gao L, Zhao L, Liu W, Wang A: Direct hydrogen production from lignocellulose by the newly isolated Thermoanaerobacterium thermosaccharolyticum strain DD32. RSC Adv 2015, 5:99781-99788. 47. Zurawski JV, Blumer-Schuette SE, Conway JM, Kelly RM: The extremely thermophilic genus Caldicellulosiruptor: physiological and genomic characteristics for complex carbohydrate conversion to molecular hydrogen. In Microbial BioEnergy: Hydrogen Production. Edited by Zannoni D, De Philippis R. Springer Netherlands; 2014:177-195. 48. Cha M, Chung D, Westpheling J: Deletion of a gene cluster for [Ni–Fe] hydrogenase maturation in the anaerobic hyperthermophilic bacterium Caldicellulosiruptor bescii identifies its role in hydrogen metabolism. Appl Microbiol Biotechnol 2016, 100:1823-1831. 49. Basen M, Rhaesa AM, Kataeva I, Prybol CJ, Scott IM, Poole FL, Adams MWW: Degradation of high loads of crystalline cellulose and of unpretreated plant biomass by the thermophilic bacterium Caldicellulosiruptor bescii. Bioresour Technol 2014, 152:384-392. 50. Yilmazel YD, Johnston D, Duran M: Hyperthermophilic hydrogen production from wastewater biosolids by Caldicellulosiruptor bescii. Int J Hydrogen Energy 2015, 40:12177-12186. 51. Talluri S, Raj SM, Christopher LP: Consolidated bioprocessing of untreated switchgrass to hydrogen by the extreme thermophile Caldicellulosiruptor saccharolyticus DSM 8903. Bioresour Technol 2013, 139:272-279. 52. Cha M, Chung D, Elkins JG, Guss AM, Westpheling J: Metabolic engineering of Caldicellulosiruptor bescii yields increased hydrogen production from lignocellulosic biomass. Biotechnol Biofuels 2013, 6:85. 53. Jung KA, Lim S-R, Kim Y, Park JM: Potentials of macroalgae as feedstocks for biorefinery. Bioresour Technol 2013, 135: 182-190. 54. Wang X, Ruan Z, Sheridan P, Boileau D, Liu Y, Liao W: Two-stage photoautotrophic cultivation to improve carbohydrate production in Chlamydomonas reinhardtii. Biomass Bioenergy 2015, 74:280-287.
57. Chen C-Y, Zhao X-Q, Yen H-W, Ho S-H, Cheng C-L, Lee D-J, Bai F-W, Chang J-S: Microalgae-based carbohydrates for biofuel production. Biochem Eng J 2013, 78:1-10. 58. Xia A, Jacob A, Tabassum MR, Herrmann C, Murphy JD: Production of hydrogen, ethanol and volatile fatty acids through co-fermentation of macro- and micro-algae. Bioresour Technol 2016, 205:118-125. 59. Batista AP, Ambrosano L, Grac¸a S, Sousa C, Marques PASS, Ribeiro B, Botrel EP, Castro Neto P, Gouveia L: Combining urban wastewater treatment with biohydrogen production — an integrated microalgae-based approach. Bioresour Technol 2015, 184:230-235. 60. Nobre BP, Villalobos F, Barraga´n BE, Oliveira AC, Batista AP, Marques PASS, Mendes RL, Sovova´ H, Palavra AF, Gouveia L: A biorefinery from Nannochloropsis sp. microalga — extraction of oils and pigments. Production of biohydrogen from the leftover biomass. Bioresour Technol 2013, 135:128-136. 61. Nguyen T.-A.D., Kim K-R, Nguyen M-T, Kim MS, Kim D, Sim SJ: Enhancement of fermentative hydrogen production from green algal biomass of Thermotoga neapolitana by various pretreatment methods. Int J Hydrogen Energy 2010, 35: 13035-13040. 62. Ghirardi ML, Dubini A, Yu J, Maness PC: Photobiological hydrogen-producing systems. Chem Soc Rev 2009, 38:52-61. 63. Nagarajan D, Lee D-J, Kondo A, Chang J-S: Recent insights into biohydrogen production by microalgae — from biophotolysis to dark fermentation. Bioresour Technol 2017, 227:373-387. 64. Melis A, Zhang L, Forestier M, Ghirardi ML, Seibert M: Sustained photobiological hydrogen gas production upon reversible inactivation of oxygen evolution in the green alga Chlamydomonas reinhardtii. Plant Physiol 2000, 122:127-136. An outstanding approach of approach of photobiological production of H (2) gas via the reversible hydrogenase pathway in the green alga Chlamydomonas reinhardtii. Two-stage H(2) production which involves at (stage 1) as circumventing the severe O(2) sensitivity of the reversible hydrogenase and in (stage 2) as temporally separating photosynthetic O (2) evolution and carbon accumulation from the consumption of cellular metabolites and concomitant H(2) production. 65. Bandyopadhyay A, Stockel J, Min H, Sherman LA, Pakrasi HB: High rates of photobiological H2 production by a cyanobacterium under aerobic conditions. Nat Commun 2010, 1:139. Authors describe about the potential of photobiological hydrogen production by oxygenic photosynthetic microbes by highlighting that nitrogenase and hydrogenase are generally oxygen sensitive, and require protective mechanisms to function in an aerobic extracellular environment. Authors took Cyanothece sp. ATCC 51142, a unicellular, diazotrophic cyanobacterium as an example with the capacity to generate high levels of hydrogen under aerobic conditions. 66. Hwang J-H, Kim H-C, Choi J-A, Abou-Shanab RAI, Dempsey BA, Regan JM, Kim JR, Song H, Nam I-H, Kim S-N et al.: Photoautotrophic hydrogen production by eukaryotic microalgae under aerobic conditions. Nat Commun 2014, 5:3234. 67. Chen C-Y, Yang M-H, Yeh K-L, Liu C-H, Chang J-S: Biohydrogen production using sequential two-stage dark and photo fermentation processes. Int J Hydrogen Energy 2008, 33: 4755-4762. 68. Pasupuleti SB, Srikanth S, Venkata Mohan S, Pant D: Continuous mode operation of microbial fuel cell (MFC) stack with dual gas diffusion cathode design for the treatment of dark fermentation effluent. Int J Hydrogen Energy 2015, 40: 12424-12435.
55. Zhu S, Wang Y, Huang W, Xu J, Wang Z, Xu J, Yuan Z: Enhanced accumulation of carbohydrate and starch in Chlorella zofingiensis induced by nitrogen starvation. Appl Biochem Biotechnol 2014, 174:2435-2445.
69. Wang A, Sun D, Cao G, Wang H, Ren N, Wu W-M, Logan BE: Integrated hydrogen production process from cellulose by combining dark fermentation, microbial fuel cells, and a microbial electrolysis cell. Bioresour Technol 2011, 102: 4137-4143.
56. Cheng D, Li D, Yuan Y, Zhou L, Li X, Wu T, Wang L, Zhao Q, Wei W, Sun Y: Improving carbohydrate and starch accumulation in Chlorella sp. AE10 by a novel two-stage process with cell dilution. Biotechnol Biofuels 2017, 10:75.
70. Liu C-H, Chang C-Y, Liao Q, Zhu X, Liao C-F, Chang J-S: Biohydrogen production by a novel integration of dark fermentation and mixotrophic microalgae cultivation. Int J Hydrogen Energy 2013, 38:15807-15814.
Current Opinion in Biotechnology 2018, 50:136–145
www.sciencedirect.com
Greener processes for dark fermentative bioH2 production Kumar et al. 145
Authors described about a unique and novel approach of cultivation of the mixotrophic culture of an isolated microalga (Chlorella vulgaris ESP6) to simultaneously consume CO2 and COD by-products from dark fermentation. 71. Santoro C, Arbizzani C, Erable B, Ieropoulos I: Microbial fuel cells: from fundamentals to applications. A review. J Power Sources 2017, 356:225-244. 72. Pandit S, Balachandar G, Das D: Improved energy recovery from dark fermented cane molasses using microbial fuel cells. Front Chem Sci Eng 2014, 8:43-54. 73. Varanasi J, Roy S, Pandit S, Das D: Improvement of energy recovery from cellobiose by thermophillic dark fermentative hydrogen production followed by microbial fuel cell. Int J Hydrogen Energy 2015, 40:8311-8321. 74. Varanasi JL, Sinha P, Das D: Maximizing power generation from dark fermentation effluents in microbial fuel cell by selective enrichment of exoelectrogens and optimization of anodic operational parameters. Biotechnol Lett 2017, 39:721-730. 75. Chookaew T, Prasertsan P, Ren ZJ: Two-stage conversion of crude glycerol to energy using dark fermentation linked with microbial fuel cell or microbial electrolysis cell. N Biotechnol 2014, 31:179-184. 76. Lu L, Ren ZJ: Microbial electrolysis cells for waste biorefinery: a state of the art review. Bioresour Technol 2016, 215:254-264. 77. Rivera I, Buitro´n G, Bakonyi P, Nemesto´thy N, Be´lafi-Bako´ K: Hydrogen production in a microbial electrolysis cell fed with a dark fermentation effluent. J Appl Electrochem 2015, 45: 1223-1229. 78. Kadier A, Simayi Y, Abdeshahian P, Azman NF, Chandrasekhar K, Kalil MS: A comprehensive review of microbial electrolysis cells (MEC) reactor designs and configurations for sustainable hydrogen gas production. Alex Eng J 2016, 55:427-443. 79. Yang Y, Qin M, Yang X, He Z: Enhancing hydrogen production in microbial electrolysis cells by in situ hydrogen oxidation for
www.sciencedirect.com
self-buffering pH through periodic polarity reversal. J Power Sources 2017, 347:21-28. 80. Guo K, Pre´voteau A, Rabaey K: A novel tubular microbial electrolysis cell for high rate hydrogen production. J Power Sources 2017, 356:484-490. 81. Tapia-Venegas E, Ramirez-Morales J, Silva-Illanes F, ToledoAlarco´n J, Paillet F, Escudie R, Lay CH, Chu CY, Leu HJ, Marone A, Lin CY, Kim DH, Trably E, Ruiz-Filippi G: Biohydrogen production by dark fermentation: scaling-up and technologies integration for a sustainable system. Rev Environ Sci Bio/Technol 2015, 14:761-785. 82. Liu L, Pang C, Wu S, Dong R: Optimization and evaluation of an air-recirculated stripping for ammonia removal from the anaerobic digestate of pig manure. Process Saf Environ Prot 2015, 94:350-357. 83. Malamis S, Katsou E, Di Fabio S, Bolzonella D, Fatone F: Biological nutrients removal from the supernatant originating from the anaerobic digestion of the organic fraction of municipal solid waste. Crit Rev Biotechnol 2014, 34:244-257. 84. Maity SK: Opportunities, recent trends and challenges of integrated biorefinery: Part I. Renew Sustain Energy Rev 2015, 43:1427-1445. In this review, author describes about the biomass classification of four general types based on their origin which are; energy crops, agricultural residues and waste, forestry waste and residues and industrial and municipal wastes. Additionally, further elucidation of the chemistry of various types of biomass used in the biorefinery is well explained. 85. Maity SK: Opportunities, recent trends and challenges of integrated biorefinery: Part II. Renew Sustain Energy Rev 2015, 43:1446-1466. This article presented an outline of opportunities and socio-technoeconomic challenges of various biomass processing technologies. Besides, overview of production of hydrocarbon fuels viz various biomass processing technologies such as hydrodeoxygenation of triglycerides, biosynthetic pathways and aqueous phase catalysis in hydrocarbon biorefinery was highlighted.
Current Opinion in Biotechnology 2018, 50:136–145