Outlook of fermentative hydrogen production techniques: An overview of dark, photo and integrated dark-photo fermentative approach to biomass

Energy Strategy Reviews 24 (2019) 27–37

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Review

Outlook of fermentative hydrogen production techniques: An overview of dark, photo and integrated dark-photo fermentative approach to biomass

T

Puranjan Mishraa, Santhana Krishnana, Supriyanka Ranaa, Lakhveer Singha,b, Mimi Sakinaha, Zularisam Ab Wahida,∗ a b

Faculty of Engineering Technology, Universiti Malaysia Pahang, Lebuhraya Tun Razak, 26300, Gambang, Kuantan, Pahang, Malaysia Department of Biological and Ecological Engineering, Oregon State University, Corvallis, OR, 97333, USA

A R T I C LE I N FO

A B S T R A C T

Keywords: Hydrogen Biomass Fermentation Dark and photo fermentation

Biomass can be a sustainable choice for bioenergy production worldwide. Biohydrogen production using fermentative conversion of biomass has gained great interest during the last decade. Besides being an efficient transportation fuel, biohydrogen can also be also be a low-carbon source of heat and electricity. Microbes assisted conversion (bioconversion) can be take place either in presence or absence of light. This is called photofermentation or dark-fermentation respectively. This review provides an overview of approaches of fermentative hydrogen production. This includes: dark, photo and integrated fermentative modes of hydrogen production; the molecular basis behind its production and diverse range of its applicability industrially. Mechanistic understanding of the metabolic pathways involved in biomass-based fermentative hydrogen production are also reviewed.

1. Introduction In the beginning of 1800s, biomass was a major source of energy and fuels. Onset of the fossil fuel era has almost phased out its existence from the industrialized nations until the “First oil Shock” shook the world in mid-1970s, only then biomass revival started to begin. Importance of the biomass was acknowledged by the governments and policy makers in order to use it to regain the balance of depleting natural non renewable resources. As per statistics of REN 2016 report, overall primary energy usage of biomass has reached 57 exa-joules (approx.) in 2013, out of which 60% was shared by traditional biomass resources and the remainder includes modern bioenergy fuels like solid, gaseous or liquid biofuels. However, despite the prior known hazards associated with fossil fuels, its usage has been continued over the years, which are a major source of greenhouse gases (i.e. CO2, CH4 and CO) emission thereby polluting the environment. Such sole dependence on fossil fuels (especially in developing countries) may lead to drastic environmental effects like climate change and global warming, and would create global energy security crisis worldwide [1]. So, the exploration of carbon free, high energy density and alternative renewable energy sources would be the only long term solution to these problems. A a reasonable solution to this situation, European Renewable Energy Council (EREC) 2010, has proposed an initiative to enhance their

∗

renewable energy consumption rate from 11% to 20% by 2020 [2]. Biomass energy contributes a major portion in global renewable energy along with its ever-growing share in electricity production worldwide [3]. Biofuels represent an ecofriendly, sustainable, cost effective, biodegradable, and promising alternative for fossil fuels. Among which, H2 is considered as a clean energy fuel having high energy density (122 kj/ g) [4], which is three times higher than hydrocarbon fuels. Combustion of H2 fuels produces water hence it does not contribute to GHG gas effect. Heating value of (61,100 Btu/Ib) of H2 is also nearly three times higher than methane (23,879 Btu/Ib) [5]. Biohydrogen combustion produces generates only water thereby presenting itself as a prominent substitute of GHG emitting fossil fuels. So, the versatility of its application is broadening from biofuel to bio-fertilizer and fuel cells as well, which can be understood by witnessing the commercialization of automobile prototypes running on biohydrogen by several renowned automobile companies. Notably, the global statics revealed that natural sources contribute to only 8% of hydrogen production, while majority of its proportion is produced hydrogen is produced from petroleum, coal and water i.e. 30%, 18% and 4% respectively [6]. Virtually hydrogen produced by the reformation of fossils fuels (petroleum or coal) is neither renewable nor carbon neutral as such production involves large greenhouse-gas footprints. So, the actual benefits of hydrogen can only be attained, only if

Corresponding author. E-mail address: [email protected] (Z. Ab Wahid).

https://doi.org/10.1016/j.esr.2019.01.001 Received 9 July 2017; Received in revised form 3 June 2018; Accepted 16 January 2019 2211-467X/ © 2019 Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/BY-NC-ND/4.0/).

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the substrate is widely available and renewable without inducing any GHG gas after-effects [7]. We present a review of the promising approaches applied to achieve biomass based hydrogen production by using microbes, called biohydrogen fermentation using crops straws, agri-wastes, industrial waste or naturally occurring organic rich biomasses (like molasses). This approach will not only turn low-value feedstock into a valuable product, but also minimize the environmental issues derived from these reduces (like burning straws, wastewater led water pollution, clogged water bodies by molasses choking the aquatic life to death so on and so forth. The aim of this review is to provide an overview of the importance of biomass as a prominent alternative feedstock for biohydrogen production and to discuss various mechanisms associated with its production including dark-fermentation, photo fermentation and combined (hybrid) dark-photo fermentation.

Fig. 1. Potential biomass as renewable energy.

hand, major biological processes involves direct and indirect bio-photolysis, dark-, photo-and hybrid (combination of both dark- and photofermentation) fermentation [12]. Thermochemical process generally have an expensive design setup and requires high temperature, high pressure, electricity for thermochemical process, prompted researchers to find out a sustainable and flexible H2 production methods which utilize the biomass as a substrate [13]. As the solution to these issues, microbial H2 production has an upper hand over the former method. Anaerobe fermentation by anaerobic bacteria has two distinct phases, where the first phase (called acidogenic phase) is characterized by the rapid growth and high hydrogen production along with acetic and butyric acid production, while second phase (called solventogenic phase) is characterized by slower growth with low hydrogen and solvent production. Determination of whether anaerobic bacteria utilize a solvent or acidic producing pathway is dependent on ATP and NADH levels. Established anaerobic digestion processes of wastewater are greatly facilitated by the development of dark-fermentation approach of hydrogen production by using various biomass resources as a feedstock, such as glucose, sugar cane, molasses, starch, potato residues and so on, Table 1 [14]. Over the years, great progress have already been made in the various aspects of fermentative H2 production like biomass immobilization, bioreactor design, and microbial community control; however, long-term and stable H2 production for practical wastewater treatment has not been satisfactorily achieved and are yet to be extensively explored further at molecular level [15].

2. Major applications of hydrogen The hydrogen is considered as carbon free fuel, as the only byproduct after its combustion is water. Supply of low-carbo energy for heat, balancing of electricity at national grid and application in combustive engine preferred hydrogen over other hydrocarbon based gaseous biofuels. From the statistical point of view, the fertilizers and petroleum companies are considered to be the largest users of H2 which almost for account for 50% and 37% respectively [8]. With the demanding of H2 engine, the H2 fuel cells demand is increased by six percent in last five years [9]. It is important to understand that H2 energy will be used alongside many other forms of energy and enhance the overall efficiency of delivering clean fuel for a variety of applications. How H2 will be used in the future depends on the specific needs of the community. There are some other major applications of current H2 utilization described as followed;

• H is utilized for hydration of substantial oils for fuel production, foods hydration, and alkali hydration for fertilizers production. • As H is the perfect electron donor, it is uses for diminishing nitrate, 2

2

perchlorate, selenite, and a suite of other oxidized water contaminations.

Currently, the industrial application of hydrogen is equivalent to only 3% of the total energy consumption, and it is expected to grow significantly in the years to come [10].

4. Enzymatic basis of microbial hydrogen production

3. Biomass as an alternative of fossil fuels for hydrogen production

Mainly bio-H2 production can be accomplished in two different ways: photosynthesis and fermentation. Fermentation is divisible into the dark fermentation and photo fermentation while on the other hand, photosynthesis is divided further direct and indirect photolysis [31]. The fundamental approach of microbial H2 production is that, the microorganisms can use protons (H+) as an electron (e−) sink for two electron equivalents [2H+ + 2e− → 2H2]. All above mentioned H2 production approaches differs from one another in terms of electron donor types, their redox potentials, and the microbial consortia that carry out the overall processes [32]. The hydrogen production using these approaches are summarized in Table 2. The processes of biological H2 production are fundamentally dependent upon the presence of two major H2-producing enzyme; hydrogenase and nitrogenase. These enzymes catalyze what is arguably the simplest chemical reaction: 2H++ 2e− ↔ H2. An overview of H2 pathway in bacterium by hydrogenase and nitrogenase are depicted in Fig. 2. The enzymes carrying out H2 production reaction are of three different classes known as; nitrogenase, Fe-hydrogenase and NieFe hydrogenase [34]. Microorganisms with Fe-hydrogenase and NieFe hydrogenase functions as the “uptake” hydrogenases, i.e. those hydrogenase whose normal metabolic function is to derive reductant from H2 [34]. Activities in the uptake direction are usually in the order of 300–400 μmol/min mg and rates of H2 evolution by the purified enzyme are lower i.e. about 65 μmol/min mg. Electrons derived from

Biomass are the product of photosynthesis and are the most versatile renewable sources that can be applied for sustainable biohydrogen production. The biomass resources includes agricultural wastes along with their lignocellulogic products, wood waste, aquatic plants, urban garbage and household effluents. Since biomass consumes atmospheric CO2 for its growth, so it possess negligible net CO impact as compared to the fossil fuels. For example, the global annual yield of ligno-cellulosic biomass residues is approximately 220 billion tons, which is equivalent to about 60–80 billion tons of crude, and was considered as a huge environmental burden initially due to lack of its proper management practices. Generally, biomass comprised of hydrocarbon materials and were used as a fuel to harness heat (like combustion of wood, dried plants). The potential applications of biomass is shown in Fig. 1. Biomasses like energy crops, agricultural waste, forestry waste and industrial and municipal waste are used for microbial assisted H2 production using. Microbial ability to decompose biomass has been extensively studied in terms of maximum hydrogen production [11]. Utilizing biomass as a feedstock, H2 production methods can be divided into two categories namely, thermochemical and biological or microbial processes. Thermo-chemical processes mainly involves pyrolysis, gasification, combustion and liquefaction, whereas on the other 28

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Table 1 Fermentative hydrogen production from various biomass. Substrate

Inoculum

Operating parameter Temperature

pH

Mode

Maximum H2 yield

References

1.7 mol H2/mol glucose 3821 ml/L (CUH) 302 mL/g glucose consumed i.e. 2.4 mol/mol 0.4 mol H2·mollactate−1 236 ml H2/g chemical oxygen demand (COD). 1.43 mol H2.molglucose−1 85.6 ml/g food waste

[16]

Glucose

Clostridium sp. YM1

37 °C

6.5

Batch

Glucose monohydrate

Clostridium strains CWBI1009

30 °C

5.2

Lactate Mannose monohydrous

Microbial consortium Bacillus anthracis strain PUNAJAN 1

35 °C 35 °C

6 6.5

Sequenced batch Batch culture Batch

Glucose monohydrate Enzymatic hydrolyzed food waste Crude glycerol and apple pomace hydrolysate Sugar beet juice Mixed bio-wastes Concentrated sludge Waste peach pulp Glycerol Hydrosate of wheatstraw Vinasse-based medium supplemented with sugarcane juice Palm oil mill effluent

Clostridium butyricum CWBI1009 Immobilized sludge

30 °C –

7.3 –

Batch Continuous

Co-culture of Enterobacter aerogenes and Clostridium butyricum Sludge was preheated Mixed cultures Alkaline pre-treated sludge Anaerobic sludge Enriched mixed microflora Mixed extreme thermophiles Microbial consotorium > 50% Oxalobacteraceae

30 °C

6.5

Batch

37 °C 37 °C 35 °C 37 °C 37 °C 70 °C 37 °C

5.5 ± 0.2 7.0 9.5 5.9 5.0 6.5 7.0

Batch Batch Batch test Batch Continuous Batch mode Batch

Immobilize Clostridium butyricum EB6

37 °C

5.5

Palm oil mill effluent

Bacillus anthracis PUNAJAN 1

35 °C

6.5

Batch operation Batch

[17] [18] [19] [20] [21]

26.07 ± 1.57 mmol H2/L of medium 3.2 mol H2/mol hexose 84 L/kg TS 15.6 mL per gram/VSS 123.27 mLH2/gTOC (0.58 ± 0.13 molH2mol−1 glycerol 212.0 ± 6.6 mL-H2/g-sugars 1.59 ± 0.21 molH2/molglucos

[22] [23] [24] [25] [26] [27] [28] [29]

5.35 LH2/L-POME

[30]

2.42 mol H2/mol mannose

[19]

heterodimeric proteins with small (S) and large (L) subunits, where the smaller subunit contains three iron–sulfur clusters, two [4Fee4S] and one [3Fee4S] and the larger subunit contains a unique, complex nickel iron center with coordination to 2 CN and one CO, forming a biologically unique metallocenter [35]. The synthesis of NieFe hydrogenase is

H2 are used directly or indirectly through the quinone pool, to reduce NAD (P). The hydrogenases contain complex metallo-clusters as their active sites along with the active enzyme units which are synthesized in a complex processes further involving the auxiliary enzymes and protein maturation steps. Furthermore, the NieFe hydrogenases are

Table 2 Major three approaches of biological hydrogen production. [Reproduced from “Biological hydrogen production: prospects and challenges (2010)” article with permission from Elsevier.]. Biological hydrogen production

Background

Advantages

Challenges

Fermentative H2 production

The bacteria can produce hydrogen using proton as electron sink during the dark-fermentation of biomasses. The fermentative hydrogen pyruvate –ferredoxin-hydrogenase or pyruvate –formate lyase, and ultimate electron donor is a molecules of sugar. As the source of sugar is biomass or organic rich wastewater, fermentative hydrogen production is considered as renewable because biomass itself is the product of photosynthesis.

In compared to other process of biohydrogen production, one of the most prominent advantages of dark fermentation is that, the hydrogen production rate (H2 volume/reactor volume-time) can be order of magnitude larger than those achieved by other means.

Photo-synthesis

The oxygenic photosynthesis carried out by cyanobacteria, algae and plants. During this process water is oxidized in to O2 and electrons are used for light driven NADP reduction of redux carriers, such as NADP and Ferredoxin. The released proton during water splitting process, along with protons transported to photosynthetic membranes upon electron transport, are used for ATP production. The reducing equivalents in NADPH of ferredoxin also can be used for hydrogen production catalyzed by hydrogenases in various cyanobacteria. The MEC is a promising advanced technology in which microbial metabolism combines with electrochemistry to achieve higher hydrogen. In this process electrogenic bacteria are attached to the anode, where they oxidized organic acids and transfer the electrons to the conductive solid. By conducting through an external electric circuit, the electrons reached to the cathode, where they react with water to produce hydrogen.

The net reaction of oxygenic photosynthesis coupled with hydrogenase is conversion of water to hydrogen and oxygen with help of energy provided by light, which is an ultimate source of renewable energy. This scenario is very attractive because biohydrogen production does not involve any carbon. Therefore, oxygenic photosynthesis links biohydrogen production as renewable energy of planet

The major challenge for dark fermentative hydrogen production is low-hydrogen yield. For instance, if glucose is considered as substrate, 100% conversion of its e-equivalents to H2 could give rise to hydrogen yield of 12 mol H2/mol-glucose. However, Based on known fermentative reactions the maximum theoretical hydrogen yield is only 4 mol H2/ mol-glucose, when electron sinks are only hydrogen and acetate. The major challenges here is to sustain the biohydrogen production at high rate over times.

Microbial electrolysis cells (MECs)

The MECs can provide high hydrogen yield, as hydrogen capture efficiency ranged from 67 to 91% from diverse donor substrates. Hydrogen yield provides dual benefits of increasing the hydrogen productivity and minimizing the BOD of the effluents.

29

The key challenges of making MEC in practical is the requirement of external energy supply to increase the energy of the produced electrons. Energy losses at several point during MECs process and theses add up to determine the applied voltage. If the voltage that need to used becomes large, the energy value of the produced hydrogen gas is lower than the input of energy.

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Fig. 3. An overview illustration of hydrogen production pathway in strict anaerobe. [Reproduced from “Fermentative hydrogen production: principles, progress, and prognosis (2009)” article with permission from Elsevier.].

sustainable sources such as wind or solar energy [42]. Meanwhile, the application of small external voltage on the MECs can provide the force to travel electrons to the cathode and combine with produce hydrogen [43]. Fig. 2. An overview of hydrogen pathway by hydrogenase and nitrogenase. (Dark fermentative hydrogen production catalyzes by hydrogenase enzymes which are classified as; hup encoded [NiFe]-uptake hydrogenase, hox encoded [NiFe] bidirectional hydrogenase, [FeFe] hydrogenase, [NiFeSe] hydrogenase. Photo-fermentative hydrogen production is catalyzed by mainly nitrogenase enzyme. Nitrogenase enzyme reduces the protons to produce hydrogen with the reduction of N to ammonia. Nitrogenase enzyme consists of; reductase subunit (FeeS protein) and dinitrogenase complex (MoeFe protein). Reproduced from “Fermentative hydrogen production: principles, progress, and prognosis (2009)” article with permission from Elsevier.

5. Dark fermentative hydrogen production Dark-fermentative production of bio-H2 by is accomplished by several fermentative bacterium (either obligate or facultative), which are capable to utilize a wide range of organic biomass or wastes as a substrate, Fig. 3 and Fig. 4. As the biomasses are the product of photosynthesis, they stored biochemical energy. The fermentative microbes acquires nutrition out of it, which further helps it to accomplish its various metabolic processes. Dark fermentation using pure carbon sources or other organic biomasses has been extensively studied, where biomass can be converted into H2 and simple organic acids. Table 1 enlisted all different types of biomass along with the pure and mix microbial consortia used for the dark-fermentative hydrogen production. Dark-fermentative bacteria can be classified into either obligate or facultative anaerobes on the basis of their anaerobic or anaerobic biomass degradation capability. Clostridium [46], Ethanoligenens [47] and Desulfovibrio species [48] are known as strict anaerobes, while Enterobacter [49], Citrobacter [50], Klebsiella [51], Escherichia coli [52] and Bacillus species [19] are well known as facultative anaerobes. Almost 70% of H2 production was investigated using strict anaerobes genus Clostridium. Furthermore, fermentative-catabolism in bacterial species can be sub-divided into two groups. Firstly, the “Saccharolytic fermenting bacteria” which ferments thee complex sugars such as oligosaccharides, cellulose and simple sugars. Secondly the “Proteolytic bacterium” hydrolyzes the proteins and ferments amino acids [53]. In dark

a complicated process requiring a number of accessory gene products including metal (nickel and iron) capturing, synthesis CO and CN− as well as cluster insertion and protein maturation. [FeeFe] hydrogenases are reported to be more effective than [NieFe] hydrogenases and both these hydrogenases are susceptible to deactivation by molecular oxygen [36]. Nitrogenases are the two component protein system that uses Mg, ATP and low-potential electrons (derived from reduced ferredoxin or bavodoxin) to reduce a variety of substrates. It resides in the photosystems where it reduces nitrogen to ammonia along with the evolution of hydrogen. In algal kingdom, only the blue-green algae (cyanobacteria) possess the nitrogenase enzyme. Notably, nitrogenases are metabolically an inefficient way to H2 production as requires a considerable amount of energy (ATP) inputs to catalyse the process [37]. This chemical reaction yields hydrogen production by a nitrogenasebased system (2e− + 2H+ + 4 ATP →H2 +4 ADP + 4 Pi), Where, ADP and Pi refer to adenosine diphosphate and inorganic phosphate, respectively. The third approach of hydrogen production is based on the development of MFCs concept to harvest energy in the form hydrogen and electricity, in an emerging technology for sustainable energy requirements [38]. The microbial hydrogen production via MFCs is related to the existence of different natural electron shuttles, mediator such as azurin, ferredoxin and cytochromes which could be used by redox enzymes for electron transfer system [39,40]. The electrons are release during the oxidation of glucose into pyruvate via glycolysis process by reducing NAD+ into NADH. Since the glycolysis takes place in the cytosol the rather than in the mitochondria, reduced NADH is easily accessible to a mediator molecule that is attached to the cell membrane. After liberating the electron by NADH to anode, oxidized back into the NAD+, the MFC which operates using electrogens extracts the energy using NADH/NAD+ redox cycle [41]. However, the MECs based system need a modest amount of electricity, which is easily available for

Fig. 4. Schematic representation of hydrogen production pathway in facultative anaerobe. [Reproduced from “Fermentative hydrogen production: principles, progress, and prognosis (2009)” article with permission from Elsevier.]. 30

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31

[58] [59] [60] [61] [62] [63] [64] Cheese wheySucrose-based synthetic wastewater Sodium formate Sucrose Sucrose Acid hydrolyzed wheat starch Acid hydrolyzed wheat starch Calcium alginate Polymethyl methacrylate Agar Ethylene-vinyl acetate copolymer Polyethylene–octene–elastomer Polyester fiber Metal mesh covered plastic scouring sponge pad

Substrate concentration

Table 3 Fermentative hydrogen production from various substrate using immobilized inoculum in different supportive materials.

In present scenario, several significant advancements have made in order to improve hydrogen yield. Such improvements involves the new advanced approaches like immobilization technique or metal ions and oxides nanoparticles, to improve the fermentative hydrogen production. Inoculum immobilization system have only been applied for improved hydrogen production at pilot scale. The immobilization includes entrapment of covalent bonding, physical absorption and encapsulation methods [54]. The physical adsorption was most common methods with aids in effective mass transfer and carbon source utilization at short HRT [55]. The immobilization of fermentative bacterium were found more effective than the free cells for hydrogen production [56]. The immobilized Clostridium sp. LS2 cells on a polyethylene glycerol resulted in improved hydrogen production rate of 336 mL H2/L/h at controlled pH of 5.5, a temperature of 37 °C and optimum values of 12 h HRT and an OLR of 5.0 g COD/L/h. Application of immobilized inoculum on continuous hydrogen production from palm oil mill effluent attended the maximum hydrogen yield of 0.35 L H2/g CODremoved [30]. In another study, the immobilized Clostridium sp. T2 strain (with mycelia pellets) was employed as biological carrier to enhance biohydrogen production from corn stalk hydrolysate which led to the maximum hydrogen production (14.2 mmol H2 L−1 h−1) at an optimized HRT of 6 h and influence concentration of 20 g/L and their yielding capacity is 2.6 times higher than its counterpart lacking mycelial pellets [57]. In addition to this varieties of materials have been used in recent years for immobilization of fermentative inoculum to get improved hydrogen production as shown in Table 3. The potential of nano-additive to the dark fermentative process and consequently on hydrogen productivity in considered as active area of research [65] in last few years. Zang et al. (2007) highlighted firstly (as claimed by authors) the impact of gold nanoparticles additive to artificial wastewater on fermentative hydrogen production. The additive of 5 nm gold nanoparticles as biocatalyst resulted in 46.0% enhanced hydrogen productivity as compared with the blank test [66]. Beckers et al. (2013) studied the effect of encapsulated silica (SiO2) nano-metallic oxides (Pd, Ag, Cu, and Fe) on fermentative hydrogen production from glucose using Clostridium butyricum as inoculum. The FexOy nanoparticles applied in 2.5 L sequenced batch reactor resulted no significant effect on hydrogen yields (stable on 2.2 mol H2. mol. glucose−1), while 113% enhancement in hydrogen production rate (HPR) was reported [67]. Taherdanak et al. (2016) studied the effect of zerovalent Fe and Ni verses Fe2+ and Ni2+ nanoparticles (0–50 mg/L) effect on biohydrogen production from glucose using heat-shock pretreated anaerobic sludge under the glucose concentration and initial pH of 5 g/

Inoculum

(2)

Substrate

(Butyrate Fermentation)

Supportive material

+ 2CO2

6.8 6 6.5 6.7 6 5.5–6 7

3.45 mol H2/mol lactose 2.25 mol H2/mol sucrose. 1 mol H2/mol formate 1.41 mol H2/mol sucrose 1.7 mol H2/mol sucrose 1.96 mol H2/mol glucose 2.1 mol H2/mol glucose

C6 H12 O6 + 2H2 O → CH3 CH2 CH2 COOH + 2H2

30 °C 35 °C 37 °C 40 °C 35 °C 55 °C 37 °C

(1)

Enterobacter aerogenes MTCC 2822 Acid pretreated acclimated sludge Escherichia coli SH5 Acid pretreated anaerobic sludge Acid pretreated anaerobic sludge Heat and acid pretreated anaerobic sludge Heat and acid pretreated anaerobic sludge

(Acetate Fermentation)

10 g lactose/L 20 g COD/L 100 mM 20 g COD/L 20 g COD/L 13 ± 1 g TS/L 10 g TS/L

C6 H12 O6 + 2H2 O → 2CH3 COOH + 4H2 + 2CO2

References Temperature

pH

fermentation, it is imperative to recover efficient hydrogen from biomasses. Although, fermentative H2 yield is dependent on the substrate type, inoculum, and process parameters including pH, temperature etc., the maximum hydrogen yield in dark fermentation is metabolicallyrestricted to process pathways. However, the stoichiometrically feasibility of dark fermentation yielded close to 12 mol of hydrogen as stored in a glucose molecule. The thermodynamic prospective of glucose metabolism produces 2 mol of acetate including 4 mol of hydrogen molecule during acetate-type of dark fermentative. However, based on Gibbs free energy change, butyrate-type fermentation is the more dominated the acetate reaction. It only produces 3.3 ATP molecules and the maximum H2 production of 2.5 mol of H2/mole glucose stoichiometrically, Eqs. (1) and (2). Indeed, the expectation of for maximum hydrogen yield is restricted lower than 4 and 2.5 mol of H2/mole glucose for acetate and butyrate-type fermentation respectively, as consumption of hydrogen by inoculum itself.

Maximum Hydrogen yield

P. Mishra et al.

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Rhodobacter capsulitis, Rhodobacter sphaeroides O.U001, R. sphaeroides RV etc. Hydrogenases and nitrogenase and found prominent in these PNS photo fermentative hydrogen production. However Nitrogenases are considered as the main enzyme responsible for molecular hydrogen production under anaerobic conditions. Nitrogenases generally fix the nitrogen into NH3 (for high energy demand), while in the absence of nitrogen nitrogenases uses reductant along with ATP to generate hydrogen (2H+ 2e− + 4 ATP→ H2 + 4ADP + Pi). Therefore, sufficient ATP supply becomes one of the major concerns for efficient photofermentative hydrogen production [80]. Because photo-fermentation hydrogen production process is light-dependent it required the light energy primarily at the wave length of 522, 805, and 850 nm [81]. The equation for photo fermentative hydrogen production from acetate is illustrated in Eq. (3). The positive free energy of the reaction shoes that the reaction is not spontaneous and requiring external energy in the form light. (artificial or natural). Theoretically 4 mol, of hydrogen can be produced from the 1 mol of acetate under sufficient physico-chemical condition provided.

L and 5.5, respectively. Results showed the highly significant enhancement on hydrogen yield by Ni2+ additives, improving hydrogen yield by 55%. The Fe zero-valent and Fe2+ enhanced the hydrogen yield by 37% and 15%, respectively [68]. Mishra et al. (2017) studied the effect of NiO and CoO additives on dark fermentative hydrogen production from palm oil mill effluent at concentration ranged from 0.25 to 3.0 mg/L. They found that hydrogen production from POME was affected by the addition of NiO and CoO nanoparticles. Results showed the a maximum HPR and hydrogen yield of 21 ml H2/L-POME/ h and 0.563 L H2/g-CODremoved, respectively with the additive of 1.5 mg/L concentration of NiO NPs. The additive of 1.0 mg/L of CoO produced the highest HPR of 18 ml H2/L-POME/h with a hydrogen yield of 0.487 L H2/g-CODremoved with 1.0 mg/L of CoO NPs. The study showed that the additive of optimal concentration of NiO and CoO nanoparticles have ability to accelerate the hydrogen production from POME wastewater [69]. In another study they also suggested that additive Ni/Co oxides ratio of 3:1 have performance on dark fermentative hydrogen production from POME [70]. In addition of this, various metal ions and oxides along with different carbon sources have been investigated and observed profound effect on hydrogen yield enhancement, Table 4. However the hydrogen yield enhancement is associated with nanoparticles concentration and properties, some metal NPs exhibited the negative effect on hydrogen production. For instance, additive Cu nanoparticle in range of 2.5–12.5 mg/L to the glucose containing medium has been reported the inhibitory effects on hydrogen production [71]. In addition effect of different nanoparticles additives to the fermentative medium to the hydrogen productivity is described in Table 4, of fermentative hydrogen production Overall, these information indicate the feasibility of immobilization as well as application nanoparticles towards dark fermentative hydrogen production as potential technology for coming future.

2CH3COOH + 2H2O → 4H2 + 2CO2, ΔGo = +104 kJ

(3)

Various studied has been reported towards the optimal light intensity using different type PNS culture for maximum hydrogen yield. For instance, Laocharoen et al. (2014), isolated a newly photo-fermentative bacteria identified as Rhodobactor sphaeroides KKU-PS5 from UASB used for methane production. They operated batch fermentation under the optimal conditions; Malate, 30 mmol/L; pH. 7.0, temperature 30 °C and light intensity of 6 klux. Under these condition the reported maximum hydrogen production rate and hydrogen yield was 11. 08 mlH2/L and 3.80 mol H2/mol-malate. In addition, they reported that the light intensity provided to the medium via dark/light decreases the hydrogen production rate and hydrogen yield in compared to continuous illumination [82]. In the recent study, Gokfiltz et al. (2017) investigated the effect of high light intensities on the physicochemical status of photo-fermentative hydrogen producing strain Rhodopseudomonas palustris 42OL. The hydrogen production experiment was conducted in RPN medium containing malate 4.0 g L−1, NH4Cl 0.5 g L−1, temperature of 30 °C and light intensity of 100 μmol photons m−2 s−1. They concluded that, the increase in light intensity significantly enhances the hydrogen production rate and a positive correlation with maximum electron transfer rate [63]. Luongo et al. (2017) investigated the operating conditions affecting the hydrogen production along with poly-β-hydroxybutyrate using dark fermented municipal waste under the operating conditions; initial pH 6.0, temperature of 25 °C, and illumination of 4000 lux. The experiment has been investigated using in two different inocula under the same physico-chemical condition. Firstly using Rhodobacter sphaeroides AV1b as inoculum and secondly by mixed consortium and observed the different hydrogen productivities of 364 and 559 N mL H2 L−1, respectively. The results concluded the

6. Photo fermentative way of H2 production Photosynthetic purple non-sulfur (PNS) bacteria have ability to produce hydrogen from organic acids (acetate, butyrate, malate, succinate etc. as carbon source) along with CO2 under anoxygenic conditions using light as energy source [78]. Therefore photo-fermentation raises the possibility to get hydrogen production from wide range of substrates including organic acids rich waste and wastewaters [79]. Depending on the carbon sources, maximum hydrogen yield of 80% and maximum light conversion efficiency of 9.3% has been reported in the literature [78]. Photo-fermentation has high theoretical hydrogen yield and high COD removal efficiencies, although the economic feasibility of hydrogen production is limited by activity hydrogen producing enzyme (nitrogenase) and light intensity [33]. There are various strain of PNS bacteria have studied for photo fermentative hydrogen production including Rhodopseudomonas palustris, Rhodobacter sulfidophilus Table 4 Impact of different nanoparticles on fermentation hydrogen production. Nano-particles

Feed

Inoculum

Temp.

pH

NPs Concentration

Maximum hydrogen yield

References

Hematite nanoparticles

Sucrose

Clostridium butyricum

35 °C

200 mg/L

Glucose

Enterobacter cloacae Mixed culture

37 °C

5.0 mg/L

Silver nanoparticles

Glucose

35 °C

8.0–9.4

20 nmol L−1

Cu-NPs

Glucose

37 °C

Inhibitory effect

[71]

Glucose Molasses-based distillery wastewater Sugarcane bagasse

35 °C 37 °C

7.0 6.0 5.61 6.0

2.5–12.5 mg/L

Nickel nanoparticles Iron oxide nanoparticle

Mixed culture dominated by Clostridium species Enterobacter cloacae Clostridium acetobutylicum Anaerobic microflora Mixed culture

3.21 mol H2/mol sucrose 3.57 mol H2/mol sucrose 1.48 ± 0.04 mol H2/mol glucose, 2.48 ± 0.09 mol H2/mol glucose, 2.48 mol/mol glucose

[72]

Pd-NPs

8.48 6.0 7.0.

5.67 mg/L 50 mgL−1

2.54 mol of H2/mol. glucose 44.28 ml H2/g COD.

[75] [76]

Heat treated sludge

30 °C

5.0

200 mg/L

1.211 mol mol−1

[77]

Magnetite nanoparticles

32

[73]

[74]

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[93]. The inadequate amount of hydrogen production during dark fermentation leads to the partial conversion of substrate to hydrogen, leading to the discharge of effluents with leftover soluble metabolites like volatile fatty acids (VFAs) (acetic acid, butyric acids, lactate, formate and propionic acids) that otherwise have been utilized for additional hydrogen production. PNS bacterias have the ability to assimilate those VFAs for their growth with the evolution of hydrogen [19,94]. Stoichiometry through dark fermentative process, the maximum feasible hydrogen production from 1 mol of glucose is only 4 mol H2/molglucose. So, the coupling of dark fermented effluent for photo-fermentative hydrogen production is considered as one of the feasible way to produce hydrogen to improve H2 yield, 12 mol H2/mol-glucose [95]. Hydrogen production via integrated process is mediated by nitrogenases and hydrogenases enzymes. The dark fermentative process can be performed by either using facultative (Enterobacter, Citrobacter, Klebsiella, Escherichia species etc.) or strict microbial inoculum (Clostridium, Ethanoligenens, Desulfovibrio species). Dark fermentative process mediated by Clostridium species, one molecule of glucose is can converted into two molecule of pyruvate molecule. Further, the pyruvate to acetyl-CoA and CO2 process is mediated through pyruvate ferredoxin oxidoreductase (PFOR). The pyruvate is oxidized by transferring its electrons to ferredoxin which in turn, transfers the electrons to protons to reduce them via ferredoxin dependent hydrogenase enzyme [96]. Furthermore, H2 can be produced by the oxidation of NADH produced during glycolysis (conversion of glucose to pyruvate). Transfer of electrons from NADH to ferredoxin leads to its oxidation and the reduction of ferredoxin is mediated by NADH:ferredoxin oxidoreductase (NFOR). The reduced ferredoxin is further oxidized by hydrogenase to generate H2. Thus, theoretically, the overall H2 yield 4 mol/mol of glucose can be achieved by the Clostridium sp. with simultaneous production of VFAs [97] In case facultative inoculum the pyruvate is further converted into acetyl Co-A and formate in the presence of enzyme by pyruvate formate lyase (PFL). H2 is produced from formate by the action of FHL complex [98]. Since, 2 molecules of formate is formed from 2 pyruvate molecules hence the theoretical maximum H2 yield of 2 mol/mol glucose is considered from, facultative anaerobes. The PNS bacterium uses these produce organic acids for H2 production with the requirement of ATP as driving energy. The required ATP is synthesizing by an oxygenic cyclic photo-phosphorylation, which involves a photosystem and electron transferring proteins. Light captured by the light harvesting complexes and further channeled into the reaction center which initiates a cyclic electron flow through electron carriers. During photosynthesis, a proton gradient is generated and finally, ATP synthase produce ATP using this gradient. Anaerobically, the electrons extracted from organic acids, are transferred to ferrodoxinoxi through number of membrane-bound, electron transport molecules. The electrons in ferredoxin to NH3 (Red) are primarily used to reduce nitrogen by the nitrogenase Fig. 2. However, nitrogenase catalyzes reduction of protons to produce H2 in case N is absent. The metabolism of dark- and photo-fermenting bacteria is complementary to each other. The byproducts produced during dark-fermentative H2 production could be utilized as substrate for photo-fermentation. Thus, by a combined dark and photo-fermentation system, H2 yield could be enhanced. Combined dark- and photo-fermentation can be divided into sequential two-stage and single stage (co-culture) process.

use of mix consortium is promising for scale-up the photo-fermentative hydrogen production from dark fermented effluent as well as COD removal [83]. The strict control of anaerobic environment is a prerequisite for an efficient hydrogen production [84]. The optimal temperature and pH for efficient photo-fermentative hydrogen production can range from 30 to 35 °C and 6.8–7.5, respectively [85] with light intensity of 6–6000 lux [85,86]. The recent advancement of bio-nanotechnology, especially the application of nano-metal ions and oxides in photo-fermentative hydrogen process came in the light. The comparative study of bulk Fe(SO4)OH (H2O)2 and nanoparticles of Fe(SO4)OH(H2O)2 on photo-fermentative hydrogen production using Rhodobacter sphaeroides NMBL-02 as inoculum has been studied by Doyy et al. (2015). They observed that the addition of nano particles of Fe (SO4) OH(H2O)2 (312.168 mg/L) to the malate containing medium (3.94 g/L) at pH 5.6 enhances the hydrogen production by 1.2 fold [87]. In another recent study, Lin et al. (2017) investigated the effects of TiO2, ZnO2, and SiO2 nanoparticles on photohydrogen production using Rhodopseudomonas sp. nov. Strain A7 as inoculum. They observe that under the respective optimal conditions presence of TiO2 (300 mg/L, size 25 nm), ZnO (100 mg/L) and SiC (200 mg/L) to the medium has ability to enhanced hydrogen production up to 18.6%. In addition, compared with TiO2 and ZnO2 the presence of SiC exhibited the greatest potential to accelerates photo-fermentative hydrogen production [88]. The suspended microbial system during photo fermentation allows good mass transfer between inoculum and substrate. However, maintaining microbial cell density at optimal level by continuous biomass recycling is a one of the limitation that still to be dealt with [30]. Although, the application of immobilized microbial culture has several advantages like tolerance to the metabolic shift (temperature, pH, OLR), increased granules formation to increase cell retention and stable hydrogen productivity during long term process [55]. The immobilization of microorganisms often leads to the biofilms formation with potentially more stable and catalytically more active [89]. Immobilized photo-fermentative microbes have reportedly more hydrogen production capacity as compare to the suspended one [30]. Moreover, Wang et al. (2010) investigated the photo-hydrogen production using photo bioreactor packed with sodium alginate/polyvinyl alcohol-124/ carrageenan granules containing Rhodopseudomonas palustris CQK 01. Under optimal conditions; pH, 7.0.; temperature 30 °C; substrate concentration of 60 mmol/L and illumination of 6000 lux reported the maximum hydrogen production rate of 2.61 mmol/L/h [90] In another related study, the immobilized Rhodobacter sphaeroides O.U. 001 in modified and non-modified porous glass (VitraPOR®Filter) with the thickness of 6.8 mm and diameter of 100 mm were applied in 200 cm3 photo-bioreactor. Results suggested that the porous glasses as matrix for immobilization are the appropriate to provides stability of to the microbial cultures [91]. The photo-fermentative hydrogen production process allows the stoichiometric bioconversion of substrate to hydrogen. Various studies have been investigated towards increasing the photo-hydrogen productivity including optimization of physicochemical parameters using different PNS culture, application advance technology including nanotechnology and immobilization technique. However a various number of issues like low light conversion efficiencies, low turnover number of nitrogenase and requirements of expensive photo-bioreactor are yet to be dealt with and whose potential solutions could be of great help in the scale-up of photo-hydrogen production on industrial scale.

7.1. Sequential two-stage system for H2 production Sequential dark and photo-fermentation systems are considered to be the more efficient way of hydrogen production in comparison to the single stage usage of dark- or photo-fermentation. In this system, the fermentation process is carried out in sequential manner in two separate bioreactors to run these processes under respective optimal conditions [78]. This process yields more H2 as it utilize the leftover VFAs in dark fermentation effluents. For instance, acetic acid generated during dark fermentation is utilized by photo-fermentative bacterium

7. Integrated approach of fermentative hydrogen production Despite being the prime method of hydrogen production, dark fermentation have several disadvantages like low energy recovery, low hydrogen yield and high production cost [92,93]. However, low energy recovery, low hydrogen yield and high production cost was identified as the major disadvantages of dark-fermentative hydrogen production 33

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appropriate for H2 production [107]. In this quest, using facultative anaerobes as a co-culture help in consuming the undesired O2 present in medium, and is a far better option for a stable and high-yield H2 production [111]. Since the PNS photosynthetic bacteria utilize the organic acids produces as byproduct of dark fermentation, therefore addition of PNS with fermentative bacteria is said to considerably produce high H2 yield [111]. In addition, sequential dark and photo fermentation requires individual reactors for each stage, which enhances the operating cost. Hence, operating of both systems in single reactor using co-culture of dark and photosynthetic bacteria provides a better opportunity to maximize H2 yield in a cost effective manner. The single stage dark and photo fermentation (co-culture) mode has advantage as it allowed to occur simultaneous in single bioreactor in contrary to two stage sequential dark and photo fermentation which requires two separate reactor for operation [93]. The integrated dark and photo fermentation using co-culture of dark and photo-fermentative using various substrate are illustrated in Table 6. The noteworthy advantages of combination is that, dark fermentative inoculum consume organic waste as substrate and produces hydrogen along with VFAs which is further utilizes by insitu photo fermentative bacteria for hydrogen production [112]. In addition no requirement of external pH adjustment, substrate inhibition and reduced operational time (as the process is carried out in single stage) are the noteworthy advantages of co-culture system over the two stage sequential dark photo fermentation production [84].

as a substrate and gives overall H2 yield to 12 mol/mol glucose. Earlier, researchers performed two stage sequential dark and photo fermentation using glucose as substrate in dark fermentation, while the fermented effluent (rich in VFAs) used as a substrate for photo fermentative bacterium or consortium [95]. Up-till now, various agricultural and industrial waste have been investigated for two stage dark and photo fermentation for hydrogen production [55]. Zong et al. (2009) demonstrated the feasibility of hydrogen production via two stage sequential dark and photo fermentation process using cassava and food waste as substrate. First stage fermentation of cassava and food waste was found 199 ml H2 g−1 and 220 ml H2 g−1, respectively. While the subsequent photo-fermentation of Dark fermented effluent yielded hydrogen of 611 ml H2 g−1 and 451 ml H2 g−1. The overall hydrogen yield using two stage sequential dark and photo fermentation was increased by4.08 and 3.05 fold for cassava and food waste as compared to single stage dark fermentation [99]. Enhanced hydrogen yield using two stage sequential dark photo-fermentation reported using pretreated corncob. In first stage (dark-fermentation) maximum hydrogen yield of 120.3 mL H2/g-corncob while after two stage sequential dark and photo-fermentation it increases to 713.6 mL H2/g-corncob, which account for ∼ 6 fold increased hydrogen yield [100]. In the recent related study, Mishra et al. (2016), investigated the application of two stage sequential dark and photo-fermentation using palm oil mill effluent as substrate. They reported the hydrogen yield of 0.784 ml H2/ml POME in first stage (dark-fermentation) carried out using Clostridium butyricum LS2 as inoculum. The hydrogen yield increased to 3.064 ml H2/ml POME when dark fermented effluent subjected to photo-fermentation using Rhodopseudomonas palustris as inoculum in optimal physico-chemical conditions [101]. The possibility of enhanced H2 yield from pure carbon sources as well as agro-industrial wastewater using sequential two stages dark and photo fermentation has been adapted by various researchers as enlisted in Table 5. However, the theoretical H2 yield using sequential dark-fermentation and photo-fermentation should be 12 mol/mol glucose but practically it is hard to achieve that value. Such invariability can be explained by suggesting the glucose uptake by bacterium for their metabolic process [102]. Inappropriate operational process (pH, temp. etc.) and performance parameters (conversion efficiency of inoculum) could be the possible constraints that limits to achieve theoretical H2 yield.

8. Concluding remarks and future prospects The biomasses is considered as the largest source of energy in the word and accounting for 38% of the primary energy consumption in the developing countries. The increased interest in biological hydrogen production using various biomasses represents an exciting area of developed technology for energy generation. The present review reports the current finding of fermentative hydrogen production through different approaches including, dark, photo and integrated dark-photo fermentation systems. It is found that the organic-rich biomass has great potential as the substrate for dark, photo and integrated dark-photo fermentative hydrogen production. In spite of single stage dark and photo fermentative hydrogen, the integrated approach of dark-photo fermentation has many advantages including maximum conversion of substrate to the hydrogen (12 mol H2/mol-glucose). Moreover, the review suggests that the fermentative hydrogen production is not only restricted to the key operational parameters including pH and temperature, the development of advanced technology including immobilization and application nanotechnology has also perceived boosting impact to the fermentative hydrogen production. The immobilized inoculum has the efficiency to provide a better stability to the biological hydrogen production process when wide ranges of wastes or wastewaters are subjected to substrates. In addition, the additive of nanoparticles of different metal oxides to the fermentative medium

7.2. Combined or single stage (co-culture) fermentation process Saccharolytic fermentative bacterium such as Clostridium sp are well known H2 producers. However, they are also extremely sensitive to oxygen; therefore, their H2-producing abilities are inhibited by the presence of slight presence of O2 in the fermenter. To resolve this problem, researchers have used L-cysteine, as a reducing agent in a medium. However, it make the process quite expensive, so the procedure without the reducing agent is preferably considered more

Table 5 Hydrogen production from various sources via two stage sequential dark and photo-fermentation system. Feed

Dark-fermentative inoculum

Photo-fermentative inoculum

Maximum hydrogen yield

References

Glucose

E. cloacae strain DM11

R. sphaeroides O.U.001

[103]

Potato stem peel Beet molasses Glucose

Caldicelluluiruptor saccharolyticus Caldicelluluiruptor saccharolyticus Clostridium saccharoperbutylacetonicum N14 ATCC13564 Clostridium butyricum E. aerogenes Clostridium butyricum LS2 Mixed culture (C. butyricum & E.2 aerogenes) Mixed culture Mixed culture Mixed culture

R. capsulatus R. capsulatus R. sphaeroides NCIMB 8253

1.86 mol/mol glucose 1.52–1.72 mol/mol acetic acid 5.81 mol/mol hexose 13.7 mol/mol hexose 3.10 mol/mol glucose 1.10–1.25 mol/mol acetic acid 3.6 mol/mol glucose 2.04 mol/mol lactose 3.064 ml H2/ml POME 7 mol/mol hexose 840 ml/g starch 10 mol/mol lactose 714 ml/g COD

Starch Cheese whey Palm oil mill effluent Sweet potato starch Cassava starch Cheese whey Corn cob

Rhodobacter sp. M-19 Rhodopseudomonas BHU 01 Rhodopseudomonas palustris Rhodobacter sp. R. palustris R. palustris R. sphaeroides

34

[104] [105] [106] [107] [58] [101] [108] [109] [110] [100]

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Table 6 Integrated dark and photo fermentation in combined mode using various substrate. Feed

Dark-fermentative inoculum/Photo-fermentative inoculum

Operational parameter pH; temperature; light intensity

Maximum hydrogen yield

References

Wheat starch Wheat starch Sugarcane effluent Starch Algal biomass (starch) Wheat starch Algal biomass (starch)

Clostridium beijerinkii/Rhodobacter sphaeroides Activated Sludge/Rhodobacter sphaeroides Citrobacter freundii and E. aerogenes/R. palustris Clostridium butyricum/Rhodobacter sp. M-19 Vibrio fluvialis/Rhodobium marinum Mixed culture/Rhodobacter sp. Lactobacillus amylovorus/Rhodobium marinum

7.0–7.5; 32 ± 2 °C; 10 klux 7.0; 30 °C; 5 klux 7.0; 37 °C; 7klux pH 6.5; 30 °C, 5 klx na; 30 °C; 330 w/m2 7.3; 30 °C; 9.5 klux 6.5; 30 °C; 170 w/m2

0.60 mol/mol hexose 3.40 mol/mol hexose 2.76 mol/mol hexose 4.5 mol H2/mol glucose 6.2 mol H2/mol hexose 176 ml H2/g starch 7.2 mol H2/mol hexose

[113] [114] [115] [107] [116] [117] [118]

found increased hydrogen productivity of up to ∼6 fold compared to non-additive fermentative medium. The review suggests that application of immobilized inoculum and addition of nanoparticles is a promising technology towards the single stage dark and photo fermentative hydrogen production system. Moreover, different efforts have been made to improve hydrogen production rate and its ultimate hydrogen production yield. Significant improvements can be expected through the devolvement genetically engineered fermentative microorganism, advancement in bioreactor designing etc., which will ultimately succeed in sustainable hydrogen production at a commercial level.

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