Research perspectives on constraints, prospects and opportunities in biohydrogen production

i n t e r n a t i o n a l j o u r n a l o f h y d r o g e n e n e r g y x x x ( 2 0 1 7 ) 1 e1 1

Available online at www.sciencedirect.com

ScienceDirect journal homepage: www.elsevier.com/locate/he

Research perspectives on constraints, prospects and opportunities in biohydrogen production Bibi Shahine Firdaus Boodhun a, Ackmez Mudhoo a, Gopalakrishnan Kumar b, Sang-Hyoun Kim b, Chiu-Yue Lin c,d,* a

Department of Chemical & Environmental Engineering, Faculty of Engineering, University of Mauritius, Reduit 80837, Mauritius b Department of Environmental Engineering, Daegu University, South Korea c Green Energy Technology Research Group, Ton Duc Thang University, Ho Chi Minh City, Viet Nam d Faculty of Environment and Labour Safety, Ton Duc Thang University, Ho Chi Minh City, Viet Nam

article info

abstract

Article history:

Hydrogen gas can be formed from sewage sludge treatment via anaerobic digestion (AD) as

Received 1 February 2017

this sludge contains large amount of organic matters. In this review, a comprehensive

Received in revised form

attempt has been made to revisit the main updates, advantages and disadvantages sur-

10 April 2017

veyed in recent research (2012e2017) on fermentative hydrogen production from a variety

Accepted 12 April 2017

of biomass. The main findings of this review are now stated. The biological hydrogen

Available online xxx

production processes consist of indirect and direct biophotolysis, dark fermentation, twostage fermentation and photo-fermentation. To maximize hydrogen gas yield via such

Keywords:

technique, the activity of hydrogen-consuming bacteria should be inhibited at the acetate

Anaerobic digestion

and hydrogen formation stage to stop or reduce hydrogen consumption. The major con-

Biohydrogen

straints in biological hydrogen production processes are raw material cost, low hydrogen

Biological processes

evolution rate and yield at large scale. Lignocellulosic materials generate low yield of

Biomass

hydrogen gas due to the presence of refractory lignin while food waste containing carbo-

Fermentation

hydrates and starch yields more hydrogen gas. Effective pretreatment of substrates and inoculum can enhance hydrogen yield. In dark fermentation process, better performance can be obtained with pretreatment. Nitrogen sources such as yeast result in higher biohydrogen generation rate and cell growth from the presence of amino acids and proteins. In photo-fermentation, better results can be obtained by using a combination of photosynthetic bacteria and green microalgae, as it enhanced solar energy utilization. Future development such as genetic manipulation could be employed, which mainly focuses on the disruptive characteristics of endogenous genes. The efficiency of biohydrogen production can also be increased by lowering the costs of delivery, production, conversion, storage and practical applications. Apart from using biodegradable wastes, green wastes will be the mostly preferable targeted feedstock for hydrogen fermentation because of their large quantity and having simultaneous waste treatment benefit. © 2017 Hydrogen Energy Publications LLC. Published by Elsevier Ltd. All rights reserved.

* Corresponding author. Green Energy Technology Research Group, Ton Duc Thang University, Ho Chi Minh City, Viet Nam. E-mail addresses: [email protected], [email protected] (C.-Y. Lin). http://dx.doi.org/10.1016/j.ijhydene.2017.04.077 0360-3199/© 2017 Hydrogen Energy Publications LLC. Published by Elsevier Ltd. All rights reserved. Please cite this article in press as: Boodhun BSF, et al., Research perspectives on constraints, prospects and opportunities in biohydrogen production, International Journal of Hydrogen Energy (2017), http://dx.doi.org/10.1016/j.ijhydene.2017.04.077

2

i n t e r n a t i o n a l j o u r n a l o f h y d r o g e n e n e r g y x x x ( 2 0 1 7 ) 1 e1 1

Introduction From the beginning of the industrialized era, combustion of fossil fuel is still dominating the global energy consumption of about 80% [1,2]. Additionally, the worldwide energy consumption in the last decade has increased exponentially and will continue to grow over the next fifty years [3,4], due to population increase, prosperous lifestyle, civilization, industrialization, modernization and better air quality requirement [4e6]. Most of our energy requirements are heavily derived from fossil fuels with coal accounting for 27.2%, oil 32.8% and natural gas for 20.9% for transportation and heating [7,8]. €o € k and Tang [2] mentioned that after fossil fuels, 5.8% nuHo clear power, 2.3% hydroelectric dams and 10.2% combustible biomass and waste contribute to the worldwide energy system; however they account only for a minor share of the total primary energy requirements. Only a minor amount of global energy requirements of about 0.8% [2] is obtained from geothermal, wind and solar. Devabhaktuni et al. [9] reported that recently, the global population from one generation to another has augmented by nearly 2 billion in most developing countries. This has resulted in an increase in energy demand and a vast population living in poverty. Based on the fact that the energy demand is proportional to industrialization [5], some developing countries will need to double their installed generation capacity to satisfy the growing demand for electricity by year 2020. From 2006 to 2030, the total energy consumption is expected to increase by 44% according to Devabhaktuni et al. [9]. However, an excessive dependence on conventional resources poses a great challenge [3,10] both to the environment and human beings due to continual rising of oil prices and increasing environmental consequences such as global warming [11] as carbon dioxide and a large factor of air pollutants are emitted during the combustion of fossil fuels [1,12]. Therefore, Kapdan et al. [13] reported that the imminent shortage of energy resources has led to the introduction of more renewable energy sources. As a result, the renewable energy technologies of biofuels, wind, photovoltaics and solar thermal are finally showing some attractions [1].

Biofuels In particular, biofuels represent clean, eco-friendly, biodegradable, sustainable and cost competitive energy sources from renewable carbon resources. Among these, hydrogen is recognized as having the highest potential as a future energy carrier because of its reduced emission of air pollutants and greenhouse gases into the atmosphere [1,9]. Gupta [3] mentioned that hydrogen can be utilized for heating, transportation and power generation [14,15] and can replace all existing fuels which are being used nowadays. Hydrogen is generated from both renewable and non-renewable sources. However, research has so far been focused on the biohydrogen generation field, either by biological or physiochemical method [12]. Recently, the worldwide need on hydrogen is growing exponentially (12% annually) presently and contributing to a total energy market of 10% by 2025 [16].

Hydrogen as a cleaner fuel Hydrogen has wonderful properties as clean and green biofuel. At atmospheric temperature, hydrogen is a non-toxic, odourless, colourless, tasteless and highly combustible gas with a molecular formula H2. Being the lightest element on earth, hydrogen diffuses at a faster rate than other gases. The boiling point of hydrogen is 22.28 K, and hydrogen has a combustion energy of 120 MJ/kg and a heat capacity of 14.4 kJ/ kg K [3]. Hydrogen being a valuable, colourless, odourless, poisonous, tasteless [1] and clean fuel is used in different chemical process industries, since its only product is water, and does not emit other deleterious pollutants and CO2 in the environment when producing electricity and is truly a sustainable replacement for the dwindling fossil fuels [17,18]. Karthic and Shiny [16] outlined that in the year 2008, the total annual production of hydrogen fuel was 368 trillion cubic meters and was used mostly in the chemical industry (40%), in oil refineries (40%) and 20% in a huge variety of processes. Up to this moment, hydrogen being the most abundant element on the planet, is formed from water, biomass, natural gas and coal. Globally, the formation of hydrogen gas is obtained from conventional resources through thermochemical processes, thermal cracking processes of natural gas and splitting of water through electrolysis [18,19]. However, the different metabolites and by-products obtained from these methods might cause harm to the environment in equally different ways. Nowadays, steam reforming of natural gas is the cheapest way to form hydrogen gas where steam at temperatures of 700e1000
C, with a catalyst, is fed to a reactor at a pressure of 3e25 bars. It is deduced that at the end of the process, 4 mol of hydrogen gas are formed. Therefore, in order to produce minimum environmental effects in the formation of hydrogen gas, hydrogen can also be generated biologically [16,20e22]. Skarha [22] stated that biohydrogen is the hydrogen formation from resources such as biomass or organic wastes either biologically or photo-biologically. Biohydrogen fuel has significantly certain advantages, namely, the conversion of biohydrogen in power fuel cells is two times more efficient rather than burning a biofuel in combustion engine; no air pollutants are emitted during the combustion of biohydrogen gas compared to other biofuels; biohydrogen emits CO2 only during fermentation process, but it is more easily to be captured, hence making it carbon negative; and it has low investment cost [11,22].

Biohydrogen synthesis The means of achieving biohydrogen is biophotolysis, dark fermentation and photo fermentation. Unarguably, biohydrogen production falls within green chemistry and green engineering concepts, which make use of a set of principles, hence showing a better way to reduce or eliminate hazardous substances while designing, manufacturing and applying chemical products [13,23]. Green chemistry and engineering involve a lower use of energy when generating a chemical product and accounts less harm to the environment and is socially acceptable [13]. Thus, the purpose of this study is to present an overview of the different processes used to

Please cite this article in press as: Boodhun BSF, et al., Research perspectives on constraints, prospects and opportunities in biohydrogen production, International Journal of Hydrogen Energy (2017), http://dx.doi.org/10.1016/j.ijhydene.2017.04.077

i n t e r n a t i o n a l j o u r n a l o f h y d r o g e n e n e r g y x x x ( 2 0 1 7 ) 1 e1 1

generate biohydrogen using different types of organic waste and biomass. Brief comparisons of bioreactors used in the biohydrogen production, microorganisms available, and affecting factors have been highlighted. This study is to analyze different methods of generating biohydrogen gas, such as photo fermentation, dark fermentation and two-stage fermentation processes from several research works by critically summarizing their limitations and challenges based on their process parameters such as pH, temperature, anaerobic microorganisms, substrates, volatile fatty acids (VFAs), organic loading rate and hydraulic retention time. The various biomass selected for this study from different papers for producing biohydrogen are:  For dark fermentation processes: food wastes, palm oil mill effluent (POME), cheese whey, rice straw, vegetables and molasses.  For photo-fermentation processes: palm oil mill effluent combined with pulp and paper mill effluent, sugar beet, black molasses, lignocellulose-derived organic acids, beet molasses.  For two-stage fermentation processes: amino acids such as alanine acid, serine acid and aspartic acid and glucose.

Biohydrogen production processes Selected research analysis for dark fermentation processes Hay et al. [24] mentioned that during dark fermentation, fermentative bacteria convert the organic substrates to biohydrogen, VFAs (such as butyrate and acetate) and carbon dioxide without illumination [24]. In this part of review, biohydrogen production from POME was selected to critically assess their differences and similarity and identify possible ways for improving hydrogen generation efficiency. Chong et al. [25] have used POME with Clostridium butyricum EB6 with a nitrogen source in the form of 6 g/L of yeast extract and with a carbon source in the form of 10 g/L of glucose to generate biohydrogen gas and carbon dioxide. From the work of Chong et al. [25], it has been observed that the modified Gompertz equation had been used to estimate peak hydrogen generation potential, maximum hydrogen generation rate and lag phase time as 240 ml, 3210 ml/h and 0.229 h, respectively (Fig. 1(a)). The major limitation identified in this work was low hydrogen yield even when using a pretreated POME. Kargi et al. [26] have conducted experiments with cheese whey powder as raw materials to form biohydrogen gas under mesophilic (35
C) and thermophilic (55
C) dark fermentation conditions using anaerobic digester sludge as an inoculum. The concentrations of the initial bacteria and sugar in this work were kept constant. Kargi et al. [26] observed that higher hydrogen yields of about 110 ml H2/g total sugars and cumulating hydrogen gas of about 170 ml were obtained under the thermophilic conditions rather than in the mesophilic regime. Under the mesophilic conditions, an analysis of data by Kargi et al. [26] indicated that the peak hydrogen generation potential, maximum hydrogen generation rate and lag phase time were 100 ml, 27.3 ml/h and 22 h (Fig. 1(b)), respectively, as compared to the corresponding higher values of 192 ml, 52 ml/

3

h and 57 h, respectively, under thermophilic conditions (Fig. 1(c)). The main inferences from the work of Kargi et al. [26] were that the elimination of thermophilic hydrogenconsuming bacteria was evident in the mesophilic conditions and accounted for the lower hydrogen yield and hydrogen production rate, and the thermophilic conditions were more conducive for the synthesis of biohydrogen gas when using powder cheese whey substrates. Xiao et al. [27] have assessed the generation of biohydrogen from synthetic food wastes using nine different bacteria, and amongst which Enterobacter aerogenes and Escherichia cloacae gave the higher amounts of hydrogen gas. The anaerobic digestion conditions reported by Xiao et al. [27] were a pH of 7, mesophilic temperature of 37
C and 40 mg/l of FeSO4$7H2O (micronutrient). Besides giving specific biohydrogen generation of 155 ml/g of volatile solids metabolized, a very good fit to the modified Gompertz equation was obtained with both types of bacteria (R2 ¼ 0.96 for E. aerogenes and R2 ¼ 0.97 for E. cloacae). The peak hydrogen generation potential, maximum hydrogen generation rate and lag phase time for E. aerogenes were 234 ml, 482 ml/h and 9.6 h, respectively (Fig. 1(d)). The corresponding parameter values for E. cloacae were better at 305 ml, 1520 ml/h and 10.7 h, respectively (Fig. 1(e)). Xiao et al. [27] also reported that the neutral pH had an important bearing on the relatively low amount of biohydrogen produced and that the water to solid ratio had also affected biohydrogen gas production rate. Based on a number of observations, and also Xiao et al. [27] equally suggested, hydrogen production may be improved by ensuring a proper pH control between 5 and 6, and maintain relatively higher water to solids ratios that might gradually occasion the high synthesis of VFAs which will lower the pH within a favourable metabolic range of microbial biomass solubilization for biohydrogen synthesis. All the more, the significant variations in biohydrogen synthesis yield depicted in Table 1 may occur due to the fact that the biomass contains a number of different sugars potentially available for biohydrogen production. For example, corn stover is a lignocellulosic material consisting mostly of cellulose, hemicellulose and lignin, and about 70e80% carbohydrates [28,29]. Cellulose consists of sugars linked by b 1-4 glycosidic [30]. The lignin present in corn stover is arguably biodegradable, and hence gives relatively high hydrogen production [29]. Swine wastewater, for example, has a relative low yield because this biomass has different cellular wall structure as compared with lignocellulosic biomass and has a very low carbohydrate content and high protein content [31,32]. On the other hand, the amounts of biohydrogen gas yielded from rice straw, starch wastewater and de-oiled rice bran are high compared to that of swine wastewater due to high content of starch [33]. Starch being a polysaccharide, comprises glucose monomers joining in a 1,4 linkages [34]. The starch present in such lignocellulosic biomass is partly converted to glucose. Theoretically, a maximum amount of 4 mol of hydrogen per mole of glucose can be obtained. From Table 2, it is observed that the amounts of hydrogen yielded for sugar beet juice, cheese whey powder, vegetable waste, molasses, endof-life dairy products and raw cassava starch, for example, were less than 4 mol H2/mole substrates. For example,

Please cite this article in press as: Boodhun BSF, et al., Research perspectives on constraints, prospects and opportunities in biohydrogen production, International Journal of Hydrogen Energy (2017), http://dx.doi.org/10.1016/j.ijhydene.2017.04.077

4

i n t e r n a t i o n a l j o u r n a l o f h y d r o g e n e n e r g y x x x ( 2 0 1 7 ) 1 e1 1

ðbctÞ

Fig. 1 e Goodness-of-fit of cumulative biohydrogen generation to the modified Gompertz equation [Bio-H2 ¼ Pee with P ¼ maximum cumulative gas production (mL), b ¼ (lRme/P) þ 1 and c ¼ 2.718Rm/P] for different substrates: (a) POME, (b) cheese whey powder under mesophilic conditions, (c) cheese whey powder under thermophilic conditions, (d) food wastes digested with Enterobacter aerogenes, and (e) food wastes digested with Escherichia cloacae. The sigmoidal variations of cumulative biohydrogen production for the latter five cases were generated after mining the primary data reported in the corresponding sources (Chong et al. [25], Kargi et al. [26] and Xiao et al. [27], respectively for (a), (b) and (c), and (d) and (e)) and thereafter fitted to the modified Gompertz equation using the Table Curve 2D (trial version, v5.01) software. molasses contain sucrose [50] and account for a total sugar content of approximately 50% (32.2% sucrose, 15% fructose, 8.6% glucose) [50]. Sucrose and lactose [51] have same hydrogen yield, in principle, because both are disaccharides [50,52]. Lactose, being a reducible sugar, is made up of glucose and galactose while sucrose being a non-reducible sugar, is made up of glucose and fructose. Galactose has also been recently studied as a standalone substrate for hydrogen biosynthesis by fermentation. Workers in this specific area of biohydrogen have identified a good potential of galactose as a substrate but there are some refinement to be made to narrow the optimum operating conditions, which depend on the type of reactor design and operation mode employed. Sivagurunathan et al. [53] have studied the fermentation of galactose in a fixed bed type bioreactor configuration at 37
C, and reported a peak hydrogen generation of 65.5 L/L/d for a corresponding yield of 2.60 mol/mol hexose. One of the highlights Sivagurunathan et al. [53]

indicated was that the specific reactor configuration they studied could produce high biohydrogen turnover and equally curb the undesired effects of biomass wash-out and loss. Sivagurunathan et al. [54] later assessed the potential of biohydrogen production from galactose fermentation using pure and consortia of microbial cultures, and concluded that the specific type of mixed microbial inoculum had a strong bearing in biohydrogen generation. In this work, the reported biohydrogen yield was 1.09 mol H2/mol galactose fed to the reactor. Moreover, Sivagurunathan et al. [55] studied the feasibility of enriched mixed microbial cultures to mediate the anaerobic biohydrogen fermentative processes via a continuous operation mode and reported average maximum biohydrogen synthesis rate and biohydrogen yield of 770 ml H2/L day and 1.05 mol H2/mol galactose fed, respectively. The interesting portion of the work of Sivagurunathan et al. [55] was that the soluble final products contained acetate, lactate and butyrate as the main metabolites and with much lesser

Please cite this article in press as: Boodhun BSF, et al., Research perspectives on constraints, prospects and opportunities in biohydrogen production, International Journal of Hydrogen Energy (2017), http://dx.doi.org/10.1016/j.ijhydene.2017.04.077

5

i n t e r n a t i o n a l j o u r n a l o f h y d r o g e n e n e r g y x x x ( 2 0 1 7 ) 1 e1 1

Table 1 e Biohydrogen production from different substrates by dark fermentation process. Substrates Corn stover Swine wastewater Starch wastewater Waste peach pulp Acid hydrolyzed ground waste paper Organic portion of municipal solid wastes Cassava ethanol wastewater

Raw cassava starch End-of-life dairy products Molasses Vegetable waste Cheese whey powder Beverage wastewater substrate Sugar beet juice Starch wastewater

Microorganisms

Hydrogen yield

Thermoanaerobacterium thermosaccharolyticum W16 Acid and alkaline pre-treatment Mixed culture and Thermoanaerobacterium Anaerobic sludge sampled from an effluent treatment plant Anaerobic sludge derived from acidogenic stage of operation of an anaerobic effluent treatment plant Culture of Rhodobacter sphaeroides AV1b and a mixed culture of purple non sulphur bacteria Mixed consortium of hydrogen-giving bacteria enhanced from sludge generated during the anaerobic digestion of substrates in biogasproducting plant Mixed-culture of microorganisms Microorganisms operating under mesophilic conditions Mixed microbial culture Seed microflora Anaerobic seed sludge Anaerobic granular sludge sampled from a food effluent treatment facility cultured to promote hydrogen-producing microorganisms Anaerobic digested sludge an effluent treatment plant Inoculum taken from sludge sampled from an activated sludge effluent treatment unit

proportions of methanoic and propionic acids. Sivagurunathan et al. [56] also explored the performance of galactose fermentation in an upflow anaerobic sludge blanket bioreactor configuration at 37
C, and reported a peak biohydrogen generation rate of 56.8 L/L/day and a biohydrogen yield of 2.25 mol/ mol galactose fed at a hydraulic retention time (HRT) of a couple of hours. They also observed that the yield and biohydrogen generation rate were much susceptible to changes in HRT. These workers also concluded that the butyrate and ethanoate species were the main products of fermentation with the levels of propionate and lactate being significantly lower. Earlier, Kumar et al. [57] had studied the influence of HRT on biohydrogen generation, the extent of stability of a process and the way the microbial populations responded to the galactose substrate during fermentation in a continuously stirred tank reactor set-up. They obtained many important findings: a maximum biohydrogen synthesis rate of 25.9 L H2/L/ day for an HRT of 3 h and organic loading rate 120 g/L/day, peak biohydrogen yield reaching 2.2 mol H2/mol galactose added, butyrate being main metabolic product and biohydrogen yield being much sensitive to changes in lactate levels and HRT. Table 2 summarizes more findings of studies on fermentative hydrogen production using different substrates and microorganisms and provides additionally the process conditions applied. Table 3 then presents the core limitations and possible avenues for improving the biosynthesis kinetics for the case studies presented in Table 2. The main challenges encountered in dark fermentation are equally observed in Ref. [24]: accumulation of fermentation by-products which inhibit biohydrogen gas synthesis; end-products such as butyrate, propionate, ethanol, and others leading to low amount of biohydrogen gas; VFAs and organic products which are harmful to

References

153 ml H2/g substrates 75 ml H2/g substrates 92 ml H2/g substrates 123 ml H2/g total organic carbon 140 ml H2/g total sugar

Cao et al. [35] Xu and Deshusses [36] Zhang et al. [37] Argun and Dao [38]

364 Nml H2/l with pure R. sphaeroides, 559 Nml H2/l with mixed culture 23.6 ml/g sCOD

Luongo et al. [40]

1.72 mol H2/mol glucose 0.84 mol H2/mol carbohydrate metabolized 3.47 mol/mol substrate 2.2 mol/mol substrate 1.03 mol/mol substrate 20 L H2/L/day

Wang et al. [42] Stavropoulos et al. [43]

3.2 mol H2/mol hexose added in the system Maximum yield at an average value of 3.05 L/day

Dhar et al. [48]

Eker and Sarp [39]

Lin et al. [41]

Guo et al. [44] Marone et al. [45] Kargi et al. [46] Lin et al. [47]

Tawfik et al. [49]

the environment conditions; accumulation of VFAs reducing pH away from favourable lower limits; and biohydrogen being easily altered into undesired products before harvesting due to the presence of biohydrogen-oxidizing methanogens and home-acetogens. Based on these latter sets of data, the main improvement and process control aspects to be considered are marinating the pH in the of range 6.5e7.5 for having favourable ATP levels; ensuring optimum C/P and C/N ratios closing to 600 and 74, respectively, to yield maximum hydrogen gas; keep the HRT in the range of 18e24 h; using consortia of microorganisms or mixed culture which may cover a wider spectrum of substrates and make the process less costly; employing a suitable pretreatment such as alkaline or acid to augment bioavailability of lignin; and finally maintaining an optimal temperature of 36 ± 1
C. Further avenues where the process limitations may be addressed are reducing butyrate concentration during the process by using a two-stage process; treating organic effluents to reduce BOD loading; utilizing a seed pretreatment method to eliminate methanogens and homo-acetogens growth; removing dissolved oxygen from the reactor; enhancing the hydrogen production rate by restricting or terminating the methanogenesis to form hydrogen gas in metabolic flow; adding yeast extract or peptone to the substrates as a nitrogen source and finally improving biohydrogen evolution by ensuring a strict anaerobic environment.

Main limitations and possible improvements of photofermentation processes There are many limitations in producing biohydrogen from various biomasses via photo-fermentation (Table 4). However, many possible improvement methods have been reported.

Please cite this article in press as: Boodhun BSF, et al., Research perspectives on constraints, prospects and opportunities in biohydrogen production, International Journal of Hydrogen Energy (2017), http://dx.doi.org/10.1016/j.ijhydene.2017.04.077

6

i n t e r n a t i o n a l j o u r n a l o f h y d r o g e n e n e r g y x x x ( 2 0 1 7 ) 1 e1 1

Table 2 e Hydrogen production from different substrates and microorganisms for variable environmental/process conditions in dark fermentation process. Case study number

Substrate and microorganisms

1

POME þ Suspended mixed culture

2

Molasses þ Mixed microbial culture

4

Swine wastewater þ Anaerobic digester sludge

5

Food waste þ Co-digestion of kitchen wastewater and municipal food waste

6

Cheese whey powder þ Anaerobic seed sludge

7

Rice straw hydrolysate þ Clostridium pasteurianum

8

Vegetable waste þ Seed microflora

Process conditions

H2 yield

Temperature 55
C pH 5.5 HRT 4 days VSS 8.0 kg/m3 TSS 11.4 kg/m3 Bioreactor CSTR Agitation 200 rpm C/N ratio 25 with soluble Fe and P at 0.05 and 0.25 kg/m3, respectively. Temperature 35
C pH 4.2e4.4 COD 2000 mg/L HRT 6 h OLR 8 kg COD/m3 d Bioreactor ¼ EGSB reactor Temperature 35
C Inoculum preparation time ¼ 5 d COD 1.29 g pH 5.5e8.5 Bioreactor ¼ Glass bottles Temperature 26
C pH 6.8 Inoculum preparation time 2.0 d HRT 1.6 d OLR 29e47 g CODtotal/L/d VSS concentration 38 g VS/L Bioreactor ¼ ABR Temperature 55
C pH 5.5 Inoculum preparation time 30 min Agitation 8000 rpm HRT 360 h Bioreactor ¼ serum bottle Modified Gompertz equation determined the volume of hydrogen gas. Temperature 37
C pH 5.5 Agitation 50 rpm Bioreactor ¼ CSABR. Temperature 28 and 37
C pH 6.7 Inoculum preparation and startup ¼ 48 h Agitation 120 rpm Bioreactor ¼ Serum bottles (batch)

Based on the literature and the selected datasets presented in Table 4, the following main limitations have been surveyed for photo-fermentation processes used for biohydrogen production:  Growth of bacteria does affect photo-fermentation as the bacterial growth is directly proportional to the rate of biohydrogen production.  A metabolism of biohydrogen generation may vary due to polyhydroxybutyrate (PHB) synthesis.  High nitrogen content can decrease biohydrogen production.  The darker the wastewater, the lesser the light flux.

Production performance

Reference

146 cm3/h

2.64 m3/m3 day

Ismail et al. [58]

3.47 mol/mol sucrose

0.71 L/L h and 3.16 mmol H2/g VSSh

Guo et al. [44]

75 ml H2/g

Xu and Deshusses [36]

Increasing in OLR leads to a decrease in hydrogen gas yield from 6.0 ± 0.52 to 5.4 ± 0.87 L H2/d 1.03 mol H2/mol glucose

Tawfik and ElQelish [59]

0.44 mol H2/mol T-sugar

1.6e2.2 mol H2/ mol glucoseadded

2.55 ml/h

Kargi et al. [46]

97.30 ± 0.17 ml Hydrogen production rate ¼ 10 ± 1.17 L/d/L e

Liu et al. [60]

Marone et al. [45]

 Pre-treatment or dilution method of the waste should be applied to eliminate the dark colour of the waste.  There are scenarios when there is not enough effective light distribution.  Minimal and maximal activity of hydrogenase and nitrogenase should be maintained, respectively.  A better C/N molar ratio should be adjusted.  In order to enhance hydrogen production yield, two-stage processes can be used.  A mix of green microalgae and photosynthetic bacteria also can be used, as this is expected to improve solar energy use (in the range from 400 to 950 nm).

Please cite this article in press as: Boodhun BSF, et al., Research perspectives on constraints, prospects and opportunities in biohydrogen production, International Journal of Hydrogen Energy (2017), http://dx.doi.org/10.1016/j.ijhydene.2017.04.077

i n t e r n a t i o n a l j o u r n a l o f h y d r o g e n e n e r g y x x x ( 2 0 1 7 ) 1 e1 1

7

Table 3 e Limitations and improvements of process parameters for the selected case studies outlined in Table 2. Case study 1

2

Limitations

Improvements

 Low amount of biohydrogen was generated due to the fact that crude POME was used.  Low hydrogen yield was obtained due to low C/N/P ratio in POME  Low HRT caused low amount of biohydrogen gas.  Adding Fe2þ at 0.26 kg/m3 to the raw POME resulted in an increase in H2S generation  The presence of high amount of VSS yielded in long hydrolysis time reduces the time taken for carbohydrate to degrade.  From stoichiometry, 12 mol of hydrogen gas were obtained but in this study only 1.72 mol H2/mole hexose was obtained  High HRT generates less amount of hydrogen gas as some amount of bacteria was removed from the serum bottle.

 Use treated fresh treated POME instead of crude POME.  A gravity settler can be used after the CSTR bioreactor to maintain high biomass retention in the system and eliminate biomass washout.  Hydrolysis pre-treatment together with CSTR and membrane bioreactor (coupled together) could enhance biohydrogen production rate and yield.  Optimum C/P and C/N ratios should be maintained at 599 and 74, respectively, to yield maximum hydrogen gas.  pH level should be maintained in the range 6.5e7.0 for maintaining ATP level.  Optimum pH should be adjusted to 7 for better result.  The optimum HRT can be maintained in the range of 18e24 h  CSTR bioreactor could be used to achieve high hydrogen yield and a gravity settler can be used after the CSTR bioreactor to maintain high biomass retention in the system and eliminate biomass washout.  Microorganisms such as mixed culture can be used as it uses a wider spectrum of substrates and process will not be costly.  The optimum pH should be in the range of 5.5e7.0 for better result.  Microorganisms such as mixed culture can be used as it uses a wider spectrum of substrates and process will not be costly.  CSTR bioreactor could be used to achieve high hydrogen yield.  Maintain the optimum pH at 5.5 for high hydrogen yield and ATP level.  CSTR bioreactor could be used to achieve high hydrogen yield.  Microorganisms such as mixed culture can be used as it uses a wider spectrum of substrates and process will not be costly.  Addition of yeast enhances the biohydrogen yield.  Phosphate medium may be used to maintain pH at 6.05 and the temperature should be adjusted at 36
C for better result.

3

 No hydrogen gas was observed at pH 5.  Growing C. butyricum was impossible at pH 5.0

4

 Low amount of hydrogen gas was yielded at pH 7.5 due to the fact that single culture and acclimatization of culture caused rapid hydrogen production.

5

 Low amount of hydrogen gas was yielded as POME contains high amount of cellulosic and lignocellulosic materials and all the carbohydrates in the POME cannot be utilized by C. butyricum.  High pH value resulted in low hydrogen yield.  Low amount of hydrogen gas obtained from calcium hydroxide at 35
C  High HRT resulted in low amount of hydrogen gas.

7

9

 Inverse relation between OLR and hydrogen yield. Further increase in OLR leads to a reduction in the hydrogen yield.  High concentration of biomass leads to low amount of biohydrogen gas.

10

 Low hydrogen gas yield was obtained due to high temperature 55
C.  Hydrogen generation rate declined rapidly at high HRT as a high number of bacteria were removed.  Low biohydrogen yield was obtained due to the fact that no buffer medium was present.  Low amount of hydrogen gas was generated when nonchemical treatment organic waste was used.

12

 Photosynthetic bacteria produce organic nitrogen through their nitrogenase and this process has to be controlled.

Membrane bioreactors and bioelectrochemical systems In recent years, membrane bioreactors for the separation of produced H2 gas and also for the enrichment of the H2 gas

 High amount of hydrogen gas can be yielded at T ¼ 20
C  A short HRT of 18e24 h can be applied to enhance hydrogen yield.  The by-products carbon dioxide could be used to increase the pH after alkali pre-treatment method.  The net yield may be enhanced if a second stage process is used to yield more biohydrogen gas since VFA generated from dark fermentation process is consumed by photofermentation bacteria.  The concentration of biomass must be maintained at 35 g COD/L of carbohydrate.  Maintain the optimal temperature at 35
C and HRT at 12 h to eliminate methanogenesis under acidic environment

 High performance can be obtained with phosphate as buffer medium and CSTR bioreactor.  Alkali based treatment improves the generation of hydrogen and upgrades efficiency.

stream has been proposed [65e67]. In these studies, mostly hydrogen purification has been demonstrated outside the reactor rather than a combining system. Many parameters such as moisture and pressure have to be analyzed well before the integration of such systems [68]. There has been one such demonstrative system with the integration possibilities [69]. This could be whereby researchers moved towards the other direction of electrochemical systems integrations with the conventional H2 fermenter either by

Please cite this article in press as: Boodhun BSF, et al., Research perspectives on constraints, prospects and opportunities in biohydrogen production, International Journal of Hydrogen Energy (2017), http://dx.doi.org/10.1016/j.ijhydene.2017.04.077

8

i n t e r n a t i o n a l j o u r n a l o f h y d r o g e n e n e r g y x x x ( 2 0 1 7 ) 1 e1 1

Table 4 e Hydrogen production from different substrates and microorganisms through photo-fermentation processes. Case study

Substrate þ Microorganism

1

Glucose þ Rhodovulum sulfidophilum P5

2

Acetate and butyrate þ mixed culture

3

POME combined with paper and pulp mill effluent þ R. sphaeroides NCIMB8253

4

Lignocellulose-derived organic acids þ R. sphaeroides ZX-5

Process conditions


Temperature 30 C pH 8.0 Light for photosynthesis 150-W tungsten lamp Intensity of light 100 mmol photons/m2s. Substrate concentration 20 mmol/L of glucose Batch process Mesophilic temperature 34
C, pH ¼ 7 Vitamin solution, initiator substrate Carrier gas was nitrogen and argon gas Light for photosynthesis from fluorescent light Inoculation time was 48 h, Intensity of light used was 4 Klux, Batch process Temperature at 30
C Light for photosynthesis from fluorescent lamps Intensity of light of 4 Klux Inoculation time of 24 h, Batch process Temperature of 30
C pH 7.0 Light for photosynthesis from two 60 W tungsten lamps Intensity of light of 4500 lux Inoculation time of 18 h Batch process; Agitation at 180 rpm

utilizing the effluent streams or the left over organic part from the H2 reactor to generate electricity and also various value-added products [70e72]. In these integrative systems, authors have mentioned about various limiting factors and also over coming opportunities towards up-scaling these systems. They have been demonstrated in lab-scale and in near future the possibilities toward large scale production would be the new research and advancement in dark fermentation. Detailed information towards the start-up issues on the bioelectrochemical systems with the sustainable biohydrogen has been reviewed [73].

Concluding remarks Hydrogen is a clean fuel compared to natural gas because it forms only water during combustion. The biggest benefit of hydrogen is that it can be used as a transportation and vehicular fuel. In this study, investigations on the limitation and improvements on biohydrogen production processes were carried out. High hydrogen yield can be obtained both from photo-fermentation and dark fermentation processes by controlling optimum temperature, pH, HRT, C/N ratio and organic loading rate of each substrates used, where the optimum pH of food wastes should be kept between 5 and 6, crop

Yield

Reference

7.07 mol H2/mol glucose

Cai and Wang [61]

With acetate at 3.51 mol/kg CODRday With butyrate at 3.33 mol/kg CODRday

Srikanth et al. [62]

4.67 ml H2/ml medium

Budiman et al. [63]

Acetic acid at 1.36 mL H2/mL-media formic acid at 0.67 mL H2/mLmedia

Zhu et al. [64]

residues and animal manure should be around 7 and for hydrogenase activity should be between 6.5 and 7.5. Moreover, hydrogen gas obtained through biological processes exemplified a promising area for bioenergy production. However, a number of issues are related to the safe and sound implementation of the hydrogen economy. The issues refer to up-scaling pilot-scale processes and safety at all stages of the distribution usage, and any disposal hydrogen gas. Therefore, tremendous amount of research should be made so that hydrogen gas can be considered as a promising fuel in the near future through different technologies such as dark fermentation, photo-fermentation and water electrolysis, and focus more on high generation rate, high sustainability, low energy demand and easy operation. Some studies show that dark fermentation is the best option to achieve high biohydrogen yield. However, in practice, this technology exhibits considerably low hydrogen yields. Moreover, with an CSTR process, low amount of biohydrogen gas is obtained and high levels of biohydrogen-generation biomass cannot be maintained at a short HRT, due to its innate structure. Currently, the cost of biologically formedhydrogen appears to be higher than other biofuels. Therefore, many engineering and technical challenges need to be solved before economic obstacles can be considered. However, during dark fermentation valuable products such as

Please cite this article in press as: Boodhun BSF, et al., Research perspectives on constraints, prospects and opportunities in biohydrogen production, International Journal of Hydrogen Energy (2017), http://dx.doi.org/10.1016/j.ijhydene.2017.04.077

i n t e r n a t i o n a l j o u r n a l o f h y d r o g e n e n e r g y x x x ( 2 0 1 7 ) 1 e1 1

alcohols and VFAs (such as butyrate, acetate and propionate) are formed. Biohydrogen follows the green chemistry concept as the wastes generated from food, vegetable and manure are not released into the environment but are treated and used to generate hydrogen gas from a green perspective and biohydrogen emits CO2 only during fermentation process, but it is easier to capture the emission of CO2 at this time, hence making it carbon negative. The CO2 generated from fermentation process is captured by chemical absorption which includes amine scrubbing and water washing, physical and membrane adsorption such as pressure swing adsorption or temperature adsorption.

Acknowledgements The data presented in this review are partly from a dissertation completed by the first author. The authors appreciated a financial support from Ton Duc Thang University, Ho Chi Minh City, Vietnam.

references

[1] Chen CY, Yang MH, Yeh KL, Liu CH, Chang JS. Biohydrogen production using sequential two-stage dark and photo fermentation processes. Int J Hydrogen Energy 2008;33:4755e62. http://dx.doi.org/10.1016/ j.ijhydene.2008.06.055. €o € k M, Tang X. Depletion of fossil fuels and anthropogenic [2] Ho climate change e a review. Energy Policy 2013;52:797e809. http://dx.doi.org/10.1016/j.enpol.2012.10.046. [3] Gupta RB. Hydrogen fuel: production, transport, and storage. New York: CRC Press and Taylor and Francis Group; 2008. [4] Lucas SDM, Peixoto G, Mockaitis G, Zaiat M, Gomes SD. Energy recovery from agro-industrial wastewaters through biohydrogen production: kinetic evaluation and technological feasibility. Renew Energy 2015;75:496e504. http://dx.doi.org/10.1016/j.renene.2014.10.025. [5] Wolfram C, Shelef O, Gertler PJ. How will energy demand develop in the developing world? 2012. [6] Ohimain EI, Izah SC. Estimation of potential biohydrogen from palm oil mills' effluent in Nigeria using different microorganisms under light pendent fermentation. J Environ Treat Tech 2015;3:97e104. [7] Forsberg CW. Future hydrogen markets for large-scale hydrogen production systems. Int J Hydrogen Energy 2007;32:431e9. http://dx.doi.org/10.1016/ j.ijhydene.2006.06.059. [8] Demirbas A. Biohydrogen: for future engine fuel demands. 1st ed. New York: Springer-Verlag; 2009. [9] Devabhaktuni V, Alam M, Shekara Sreenadh Reddy Depuru S, Green RC, Nims D, Near C. Solar energy: trends and enabling technologies. Renew Sustain Energy Rev 2013;19:555e64. http://dx.doi.org/10.1016/j.rser.2012.11.024. [10] Guo WQ, Ren NQ, Chen ZB, Liu BF, Wang XJ, Xiang WS, et al. Simultaneous biohydrogen production and starch wastewater treatment in an acidogenic expanded granular sludge bed reactor by mixed culture for long-term operation. Int J Hydrogen Energy 2008;33:7397e404. http://dx.doi.org/ 10.1016/j.ijhydene.2008.09.039.

9

[11] Hallenbeck PC, Ghosh D, Skonieczny MT, Yargeau V. Microbiological and engineering aspects of biohydrogen production. Indian J Microbiol 2009;49:48e59. http:// dx.doi.org/10.1007/s12088-009-0010-4. [12] Rupprecht J. From systems biology to fuel-Chlamydomonas reinhardtii as a model for a systems biology approach to improve biohydrogen production. J Biotechnol 2009;142:10e20. http://dx.doi.org/10.1016/ j.jbiotec.2009.02.008. [13] Kapdan IK, Kargi F, Oztekin R, Argun H. Bio-hydrogen production from acid hydrolyzed wheat starch by photofermentation using different Rhodobacter sp. Int J Hydrogen Energy 2009;34:2201e7. http://dx.doi.org/10.1016/ j.ijhydene.2009.01.017. [14] Peppas L. Ocean, tidal, and wave energy: power from the sea. 1st ed. London: Crabtree Publishing Company; 2008. [15] Johnstone N, Hascic I, Popp D. Renewable energy policies and technological innovation: evidence based on patent counts. Environ Resour Econ 2010;45:133e55. http://dx.doi.org/ 10.1007/s10640-009-9309-1. [16] Karthic P, Shiny J. Comparison and limitations of biohydrogen production processes. Res J Biotechnol 2012;7:59e71. [17] Tao Y, Chen Y, Wu Y, He Y, Zhou Z. High hydrogen yield from a two-step process of dark- and photo-fermentation of sucrose. Int J Hydrogen Energy 2007;32:200e6. http:// dx.doi.org/10.1016/j.ijhydene.2006.06.034. [18] Jain IP. Hydrogen the fuel for 21st century. Int J Hydrogen Energy 2009;34:7368e78. http://dx.doi.org/10.1016/ j.ijhydene.2009.05.093. [19] Schlapbach L. Technology: hydrogen-fuelled vehicles. Nature 2009;460:809e11. http://dx.doi.org/10.1038/460809a. [20] Tamburic B, Zemichael FW, Maitland GC, Hellgardt K. Parameters affecting the growth and hydrogen production of the green algae Chlamydomonas reinhardtii. Int J Hydrogen Energy 2011;36(13):7872e6. [21] Lu GQ, Diniz da Costa JC, Duke M, Giessler S, Socolow R, Williams RH, et al. Inorganic membranes for hydrogen production and purification: a critical review and perspective. J Colloid Interface Sci 2007;314:589e603. http:// dx.doi.org/10.1016/j.jcis.2007.05.067. [22] Skarha J. Hydrogen as a renewable energy source from the biophotolysis of water using recombinant DNA. ESSAI 2012;10:107e10. [23] Argun H, Kargi F, Kapdan IK, Oztekin R. Biohydrogen production by dark fermentation of wheat powder solution: effects of C/N and C/P ratio on hydrogen yield and formation rate. Int J Hydrogen Energy 2008;33:1813e9. http://dx.doi.org/ 10.1016/j.ijhydene.2008.01.038. [24] Hay JXW, Wu TY, Juan JC, Md. Jahim J. Biohydrogen production through photo fermentation or dark fermentation using waste as a substrate: overview, economics, and future prospects of hydrogen usage. Biofuels Bioprod Biorefining 2013;7:334e52. http://dx.doi.org/10.1002/ bbb.1403. [25] Chong M-L, Abdul Rahman NA, Rahim RA, Aziz SA, Shirai Y, Hassan MA. Optimization of biohydrogen production by Clostridium butyricum EB6 from palm oil mill effluent using response surface methodology. Int J Hydrogen Energy 2009;34:7475e82. http://dx.doi.org/10.1016/ j.ijhydene.2009.05.088. [26] Kargi F, Eren NS, Ozmihci S. Bio-hydrogen production from cheese whey powder (CWP) solution: comparison of thermophilic and mesophilic dark fermentations. Int J Hydrogen Energy 2012;37:8338e42. http://dx.doi.org/10.1016/ j.ijhydene.2012.02.162. [27] Xiao L, Deng Z, Fung KY, Ng KM. Biohydrogen generation from anaerobic digestion of food waste. Int J Hydrogen

Please cite this article in press as: Boodhun BSF, et al., Research perspectives on constraints, prospects and opportunities in biohydrogen production, International Journal of Hydrogen Energy (2017), http://dx.doi.org/10.1016/j.ijhydene.2017.04.077

10

[28]

[29]

[30]

[31]

[32]

[33]

[34]

[35]

[36]

[37]

[38]

[39]

[40]

[41]

[42]

[43]

[44]

i n t e r n a t i o n a l j o u r n a l o f h y d r o g e n e n e r g y x x x ( 2 0 1 7 ) 1 e1 1

Energy 2013;38:13907e13. http://dx.doi.org/10.1016/ j.ijhydene.2013.08.072. Kumar R, Mago G, Balan V, Wyman CE. Physical and chemical characterizations of corn stover and poplar solids resulting from leading pretreatment technologies. Bioresour Technol 2009;100:3948e62. http://dx.doi.org/10.1016/ j.biortech.2009.01.075. Lau MW, Dale BE. Cellulosic ethanol production from AFEXtreated corn stover using Saccharomyces cerevisiae 424A(LNH-ST). Proc Natl Acad Sci U S A 2009;106:1368e73. http://dx.doi.org/10.1073/pnas.0812364106.  n JI, Alvarez VA, Cyras VP, Va  zquez A. Extraction of Mora cellulose and preparation of nanocellulose from sisal fibers. Cellulose 2008;15:149e59. http://dx.doi.org/10.1007/s10570007-9145-9. Wagner RC, Regan JM, Oh SE, Zuo Y, Logan BE. Hydrogen and methane production from swine wastewater using microbial electrolysis cells. Water Res 2009;43:1480e8. http:// dx.doi.org/10.1016/j.watres.2008.12.037. Diaz LA, Botte GG. Electrochemical DE ammonification of synthetic swine wastewater. Ind Eng Chem Res 2012;51:12167e72. Banks W, Muir DD. Structure and chemistry of the starch granule. In: Stumpf PK, Conn EE, editors. Biochem plants; 2014. p. 321e70. Ben Bettaı¨eb N, Jerbi MT, Ghorbel D. Gamma radiation influences pasting, thermal and structural properties of corn starch. Radiat Phys Chem 2014;103:1e8. http://dx.doi.org/ 10.1016/j.radphyschem.2014.05.011. Cao G, Ren N, Wang A, Lee DJ, Guo W, Liu B, et al. Acid hydrolysis of corn stover for biohydrogen production using Thermoanaerobacterium thermosaccharolyticum W16. Int J Hydrogen Energy 2009;34:7182e8. http://dx.doi.org/10.1016/ j.ijhydene.2009.07.009. Xu J, Deshusses MA. Fermentation of swine wastewaterderived duckweed for biohydrogen production. Int J Hydrogen Energy 2015;40:7028e36. http://dx.doi.org/10.1016/ j.ijhydene.2015.03.166. Zhang T, Liu H, Fang HHP. Biohydrogen production from starch in wastewater under thermophilic condition. J Environ Manage 2003;69:149e56. http://dx.doi.org/10.1016/ S0301-4797(03)00141-5. Argun H, Dao S. Bio-hydrogen production from waste peach pulp by dark fermentation: effect of inoculum addition. Int J Hydrogen Energy 2016;42(4):2569e74. Eker S, Sarp M. Hydrogen gas production from waste paper by dark fermentation: effects of initial substrate and biomass concentrations. Int J Hydrogen Energy 2017;42(4):2562e8. Luongo V, Ghimire A, Frunzo L, Fabbricino M, D'Antonio G, Pirozzi F, et al. Photofermentative production of hydrogen and poly-b-hydroxybutyrate from dark fermentation products. Bioresour Technol 2016;228:171e5. Lin R, Cheng J, Yang Z, Ding L, Zhang J, Zhou J, et al. Enhanced energy recovery from cassava ethanol wastewater through sequential dark hydrogen, photo hydrogen and methane fermentation combined with ammonium removal. Bioresour Technol 2016;214:686e91. Wang S, Ma Z, Zhang T, Bao M, Su H. Optimization and modeling of biohydrogen production by mixed bacterial cultures from raw cassava starch. Front Chem Sci Eng 2017:1e7. Stavropoulos KP, Kopsahelis A, Zafiri C, Kornaros M. Effect of pH on continuous biohydrogen production from end-of-life dairy products (EoL-DPs) via dark fermentation. Waste Biomass Valorization 2016;7(4):753e64. Guo WQ, Ren NQ, Wang XJ, Xiang WS, Meng ZH, Ding J, et al. Biohydrogen production from ethanol-type fermentation of molasses in an expanded granular sludge bed (EGSB) reactor.

[45]

[46]

[47]

[48]

[49]

[50]

[51]

[52]

[53]

[54]

[55]

[56]

[57]

[58]

[59]

[60]

Int J Hydrogen Energy 2008;33:4981e8. http://dx.doi.org/ 10.1016/j.ijhydene.2008.05.033. Marone A, Izzo G, Mentuccia L, Massini G, Paganin P, Rosa S, et al. Vegetable waste as substrate and source of suitable microflora for bio-hydrogen production. Renew Energy 2014;68:6e13. http://dx.doi.org/10.1016/j.renene.2014.01.013. Kargi F, Eren NS, Ozmihci S. Hydrogen gas production from cheese whey powder (CWP) solution by thermophilic dark fermentation. Int J Hydrogen Energy 2012;37:2260e6. http:// dx.doi.org/10.1016/j.ijhydene.2011.11.018. Lin CY, Leu HJ, Lee KH. Hydrogen production from beverage wastewater via dark fermentation and room-temperature methane reforming. Int J Hydrogen Energy 2016;41(46):21736e46. Dhar BR, Elbeshbishy E, Hafez H, Lee HS. Hydrogen production from sugar beet juice using an integrated biohydrogen process of dark fermentation and microbial electrolysis cell. Bioresour Technol 2015;198:223e30. Tawfik A, El-Bery H, Kumari S, Bux F. Use of mixed culture bacteria for photofermentive hydrogen of dark fermentation effluent. Bioresour Technol 2014;168:119e26. Zhang FF, Wang W, Yuan SJ, Hu ZH. Biodegradation and speciation of roxarsone in an anaerobic granular sludge system and its impacts. J Hazard Mater 2014;279:562e8. http://dx.doi.org/10.1016/j.jhazmat.2014.07.047. Yang P, Zhang R, McGarvey JA, Benemann JR. Biohydrogen production from cheese processing wastewater by anaerobic fermentation using mixed microbial communities. Int J Hydrogen Energy 2007;32:4761e71. http://dx.doi.org/10.1016/ j.ijhydene.2007.07.038. Edrisi Sormoli M, Imtiaz Ul Islam M, Langrish TAG. The effect of chitosan hydrogen bonding on lactose crystallinity during spray drying. J Food Eng 2012;108:541e8. http://dx.doi.org/ 10.1016/j.jfoodeng.2011.09.011. Sivagurunathan P, Anburajan P, Park JH, Kumar G, Park HD, Kim SH. Mesophilic biogenic H2 production using galactose in a fixed bed reactor. Int J Hydrogen Energy 2017a;42(6):3658e66. Sivagurunathan P, Anburajan P, Kumar G, Arivalagn P, Bakonyi P, Kim SK. Improvement of hydrogen fermentation of galactose by combined inoculation strategy. J Biosci Bioeng 2017b;123:353e7. Sivagurunathan P, Kumar G, Park JH, Park JH, Park HD, Yoon JJ, et al. Feasibility of enriched mixed cultures obtained by repeated batch transfer in continuous hydrogen fermentation. Int J Hydrogen Energy 2016a;41:4393e403. Sivagurunathan P, Anburajan P, Kumar G, Kim SH. Effect of hydraulic retention time (HRT) on biohydrogen production from galactose in an up-flow anaerobic sludge blanket reactor. Int J Hydrogen Energy 2016b;41:21670e7. Kumar G, Sivagurunathan P, Park JH, Park HD, Yoon JJ, Kim SK. HRT dependent performance and bacterial community population of granular hydrogen-producing mixed cultures fed with galactose. Bioresour Technol 2016;206:188e94. Ismail I, Hassan MA, Abdul Rahman NA, Soon CS. Thermophilic biohydrogen production from palm oil mill effluent (POME) using suspended mixed culture. Biomass Bioenergy 2010;34:42e7. http://dx.doi.org/10.1016/ j.biombioe.2009.09.009. Tawfik A, El-Qelish M. Continuous hydrogen production from co-digestion of municipal food waste and kitchen wastewater in mesophilic anaerobic baffled reactor. Bioresour Technol 2012;114:270e4. http://dx.doi.org/10.1016/ j.biortech.2012.02.016. Liu C-M, Chu C-Y, Lee W-Y, Li Y-C, Wu S-Y, Chou Y-P. Biohydrogen production evaluation from rice straw hydrolysate by concentrated acid pre-treatment in both

Please cite this article in press as: Boodhun BSF, et al., Research perspectives on constraints, prospects and opportunities in biohydrogen production, International Journal of Hydrogen Energy (2017), http://dx.doi.org/10.1016/j.ijhydene.2017.04.077

i n t e r n a t i o n a l j o u r n a l o f h y d r o g e n e n e r g y x x x ( 2 0 1 7 ) 1 e1 1

[61]

[62]

[63]

[64]

[65]

[66]

batch and continuous systems. Int J Hydrogen Energy 2013;38:15823e9. http://dx.doi.org/10.1016/ j.ijhydene.2013.07.055. Cai J, Wang G. Hydrogen production from glucose by a mutant strain of Rhodovulum sulfidophilum P5 in singlestage photofermentation. Int J Hydrogen Energy 2014;39:20979e86. http://dx.doi.org/10.1016/ j.ijhydene.2014.10.094. Srikanth S, Venkata Mohan S, Prathima Devi M, Peri D, Sarma PN. Acetate and butyrate as substrates for hydrogen production through photo-fermentation: process optimization and combined performance evaluation. Int J Hydrogen Energy 2009;34:7513e22. http://dx.doi.org/10.1016/ j.ijhydene.2009.05.095. Budiman PM, Wu TY, Ramanan RN, Md. Jahim J. Improvement of biohydrogen production through combined reuses of palm oil mill effluent together with pulp and paper mill effluent in photofermentation. Energy & Fuels 2015;29:5816e24. Zhu Z, Shi J, Zhou Z, Hu F, Bao J. Photo-fermentation of Rhodobacter sphaeroides for hydrogen production using lignocellulose-derived organic acids. Process Biochem 2010;45:1894e8. http://dx.doi.org/10.1016/j.procbio.2010.08.017.  thy N, Be lafi-Bako  K. Biohydrogen Bakonyi P, Nemesto purification by membranes: an overview on the operational conditions affecting the performance of non-porous, polymeric and ionic liquid based gas separation membranes. Int J Hydrogen Energy 2013a;38(23):9673e87.  thy N, Lin CY, Be lafi-Bako  K. Bakonyi P, Kumar G, Nemesto Biohydrogen purification using a commercial polyimide

[67]

[68]

[69]

[70]

[71]

[72]

[73]

11

membrane module: studying the effects of some process variables. Int J Hydrogen Energy 2013b;38(35):15092e9.  thy N, Ramı´rez-Morales JE, Tapia-Venegas E, Nemesto lafi-Bako  K, Ruiz-Filippi G. Evaluation of two gas Bakonyi P, Be membrane modules for fermentative hydrogen separation. Int J Hydrogen Energy 2013b;38(32):14042e52.  thy N, Simon V, Be lafi-Bako  K. Bakonyi P, Nemesto Fermentative hydrogen production in anaerobic membrane bioreactors: a review. Bioresour Technol 2014;156:357e63. lafi-Bako  K, Bakonyi P, Nemesto  thy N, Pientka Z. Be Biohydrogen production in integrated system. Desalination Water Treat 2010;14(1e3):116e8.  k L, Nemesto  thy N, Bakonyi P, Zhen G, Kumar G, Lu X, Koo et al. Performance evaluation of microbial electrochemical systems operated with Nafion and supported ionic liquid membranes. Chemosphere 2017;175:350e5.  n G, Valdez-Vazquez I, Nemesto  thy N, Bakonyi P, Buitro lafi-Bako  K. A novel gas separation integrated membrane Be bioreactor to evaluate the impact of self-generated biogas recycling on continuous hydrogen fermentation. Appl Energy 2017;190:813e23.  n G, Bakonyi P, Nemesto  thy N, Be lafi-Bako  K. Rivera I, Buitro Hydrogen production in a microbial electrolysis cell fed with a dark fermentation effluent. J Appl Electrochem 2015;45(11):1223e9.  k L, Kumar G, Bakonyi P, Zhen G, Sivagurunathan P, Koo Kim SH, et al. Microbial electrochemical systems for sustainable biohydrogen production: surveying the experiences from a start-up viewpoint. Renew Sustain Energy Rev 2017;70:589e97.

Please cite this article in press as: Boodhun BSF, et al., Research perspectives on constraints, prospects and opportunities in biohydrogen production, International Journal of Hydrogen Energy (2017), http://dx.doi.org/10.1016/j.ijhydene.2017.04.077