Biohythane production from sugarcane bagasse and water hyacinth: A way towards promising green energy production

Journal of Cleaner Production 207 (2019) 689e701

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Biohythane production from sugarcane bagasse and water hyacinth: A way towards promising green energy production Sinu Kumari a, Debabrata Das b, * a b

Advanced Technology Development Centre, Indian Institute of Technology, Kharagpur 721302, India Department of Biotechnology, Indian Institute of Technology, Kharagpur 721302, India

a r t i c l e i n f o

a b s t r a c t

Article history: Received 5 March 2018 Received in revised form 8 September 2018 Accepted 6 October 2018 Available online 8 October 2018

The present study embarks the concept of developing continuous biohythane (biohydrogen followed by biomethane) production from renewable energy sources. Combination of sugarcane bagasse and water hyacinth were used to reduce the use of costly chemicals for fermentation process. The lignin content of sugarcane bagasse was reduced using alkaline hydrogen peroxide pretreatment. The maximum lignin reduction of 89 ± 3% (w/w) was observed at 50
C and 150 min pretreatment time. Scanning electron microscopy, X-ray diffraction and Fourier transform infrared spectroscopy analysis were performed to confirm the lignin removal after pretreatment. Further, the influence of the hydraulic retention time on two stage biohythane production was studied by using combination of pretreated sugarcane bagasse and water hyacinth (1:2 ratio) (soluble COD, 30 ± 2 g/L) in continuous stirrer tank bioreactor. The suitable hydraulic retention time for biohydrogen and biomethane production were found to be 8 h and 10 d, respectively, which gave the maximum hydrogen and methane yield of 303 mL/g COD and 142 mL/g COD, respectively. The continuous biohythane production process increased the overall substrate conversion efficiency up to 86% with the maximum gaseous energy recovery of 8.97 kJ/g COD. © 2018 Elsevier Ltd. All rights reserved.

Keywords: Biohythane Sugarcane bagasse Water hyacinth Lignin removal Hydraulic retention time Gaseous energy

1. Introduction In the conventional anaerobic digestion (AD) process, the decomposition of organic materials takes place by a series of bacteria in the oxygen free environment to produce biogas. During AD process various kinds of extracellular hydrolytic enzymes (cellulases, hemicellulases, lipases, proteases, amylases etc.) are produced which have ability to hydrolyse the complex substrates into their simpler form. The hydrolysed materials are subsequently utilized by the acidogenic bacteria to produce hydrogen (H2) and carbon dioxide (CO2) along with volatile fatty acids (VFAs). Further, the CO2 and H2 dissolved in the medium are used as energy source by hydrogenotrophic methanogens to produce methane (CH4), whereas acetoclastic methanogens convert acetic acid (CH3COOH) to CH4 and CO2 (Eqs. (1) and (2)) (Fig. 1) (Sikora et al., 2017). Since, the hydrogenotrophic methanogens are H2 scavengers the overall yield of H2 decreased in the AD process. Hence, the AD process can be oriented towards dark fermentation where H2 and CO2 are produced instead of CH4 by inhibiting the methanogens and enriching the acidogenic bacteria (Nath and Das, 2004). Further, the

* Corresponding author. E-mail addresses: [email protected], [email protected] (D. Das). https://doi.org/10.1016/j.jclepro.2018.10.050 0959-6526/© 2018 Elsevier Ltd. All rights reserved.

spent medium of dark fermentation which contains VFAs (mainly acetic acids, butyric acids and propionic acid), ethanol and other compounds can be used for methane production using methanogenic bacteria (Pakarinen et al., 2009). The two stage process (dark fermentation followed by biomethanation) has several advantages over single stage biomethanation process (Kumari and Das, 2015). 4H2 þ CO2 / CH4 þ 2H2O

(DGo ¼ 131 kJ/mol)

CH3COOH þ H2O / CH4 þ CO2 þ H2O

(1)

(DGo ¼ 36 kJ/mol) (2)

H2 energy seems to be attractive because of its high energy density (142 kJ/g) as compared to other fuels (Wang et al., 2016). It is easy to transport and produce no greenhouse gases after combustion (Ntaikou et al., 2010). After H2, CH4 is the 2nd highest energy content (55.5 kJ/g) gas (Pakarinen et al., 2009). Mixture of H2 (5e20%) and CH4 (80e95%) is called “Hythane®” and the production of hythane through biological process can be collectively called under the eponym of “Biohythane” (Liu et al., 2013). Under “Biohythane concept” the 2nd stage biomethane could be used separately as a fuel or could be mixed with biohydrogen in a certain ratio to make it suitable for IC (Internal combustion) engines. Also, the burning of hythane is cleaner than methane alone (Ueno et al., 2007).

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Notation list AD AHP APHA CH4 CH3COOH C/N CO2 COD CrI D DBT F FTIR GC H2 HCl H2O2 HPR HRT IIT MMT/Y

Anaerobic digestion Alkaline hydrogen peroxide American public health association Methane Acetic acid carbon to nitrogen ratio Carbon dioxide Chemical oxygen demand Crystallinity index Dilution rate Department of Biotechnology Flow rate Fourier transform infrared Gas chromatography Hydrogen Hydrogen chloride Hydrogen peroxide Hydrogen production rate Hydraulic retention time Indian Institute of Technology Metric million ton/year

MNRE MPR NaOH NREL OLR P PSCB Rm R2 S So SCB SCOD SEM TS V VFAs VS WH XRD YE X

l

Ministry of new and renewable energy Methane production rate Sodium hydroxide National renewable energy laboratory Organic loading rate Hydrogen production potential pretreated sugarcane bagasse Rate of H2 production Correlation coefficient Substrate concentration Initial substrate concentration Sugarcane bagasse Soluble chemical oxygen demand Scanning electron microscopy Total solids Volume of reactor Volatile fatty acids Volatile solids Water hyacinth X-ray Diffractometer Yeast extract Biomass concentration Lag phase

Fig. 1. Schematic diagram of one stage biomethane and two stage biohythane process.

Continuous biohythane production has to be explored for the commercialization of gaseous energy. It has several advantages over batch process which includes, high productivity, no down time, can operate under steady state condition, can hold a particular phase of fermentation process for a longer period of time etc. (Chen et al., 2012a). Moreover, there are several factors affecting the continuous process viz. pH (Alexandropoulou et al., 2018), temperature (Alibardi and Cossu, 2016), reactor configuration

(DiStefano and Palomar, 2010), organic loading rate (OLR), hydraulic retention time (HRT) etc. (An Carrillo-Reyes et al., 2016) HRT is the most important parameter to determine the activity of acidogenic and methanogenic bacteria inside the bioreactor. It may affect the metabolic route of microorganism and also influence the composition of subdominant microorganism (Dareioti and Kornaros, 2014). Moreover, the composition of soluble metabolites and product yield (H2 and CH4) may be controlled by

S. Kumari, D. Das / Journal of Cleaner Production 207 (2019) 689e701

controlling the HRT (Zhang et al., 2006). Therefore, it is important to determine the suitable range of HRT for improved H2 and CH4 production. The other factor which affects the biohythane production is the selection of suitable feedstock. It should be cheap, renewable and easily available. Lignocellulosic wastes are the most promising feedstock considering its high availability and low cost (Sasaki et al., 2017). Therefore, sugarcane bagasse (SCB) and water hyacinth (WH) were selected in the present study on the basis of their availability in India. After Brazil, India is the 2nd largest producer of sugarcane in the world. The residue in the form of SCB (in India) is approximately 97.8 MMT/Y (metric million ton/year) (Kumari and Das, 2015). WH (the fast growing aquatic weed) is spread all over the world, and it is rich in nitrogenous compounds such as ammonical nitrogen (NH3-N), nitrate and nitrite (Rezania et al., 2015). The growing rate of WH in India is approximately 15 MMT/Y. Hence, this can be used as nitrogen source in place of synthetic nitrogen needed for fermentation process (Varanasi et al., 2018). Moreover, WH also contain various types of microelements which are necessary growth factors for anaerobic microorganism (Lay et al., 2013). Thus, the judicious use of SCB and WH for biohythane production with concurrent bioremediation is an attractive and effective way of trapping clean energy from renewable energy sources in a sustainable manner. However, gaseous energy production from lignocellulosic biomass required some pretreatment steps before fermentation process. This step will decrease the complexity of biomass by removing the lignin (Kumari and Das, 2015). A variety of pretreatment methods such as acid (Jonsson and Martín, 2016), alkali (Kumari and Das, 2015), ammonia fiber explosion (Teymouri et al., 2004), ultrasounds, acoustic cavitation
n Hilares et al., (Madison et al., 2017), hydrodynamic cavitation (Tera 2018b) etc. and in many cases combination of two have been used so far to remove the lignin and decrease the crystallinity of lignocellulosic biomass. It is observed that alkali along with hydrodynamic cavitation (Ter
an Hilares et al., 2017a, 2016) and other agents such as peracetic acid (CH3COOOH) or hydrogen peroxide (H2O2) effectively removes lignin from lignocellulosic biomass (Bensah and Mensah, 2013). In the hydrodynamic cavitation, microbubbles are formed, grown and collapsed within a confined fluid flow. This causes the water molecules to dissociate into reactive
n radicals (HO and O 2 ) which degrade the lignin bonds (Tera Hilares et al., 2017b). In case of alkaline hydrogen peroxide (AHP) pretreatment, H2O2 provides highly reactive radicals in the alkaline environment which helps in delignification process. High temperature accelerates the decomposition rate of H2O2. This leads to increase in reactive radicals (HO and O 2 ). These reactive radicals depolymerize the lignin bonds by attacking on aliphatic part of the lignin side chain (oxidative action) (Li et al., 2016). No reports are available on the use of carbon rich SCB and nitrogen and microelements rich WH in a proper combination for biohythane production in a sustainable manner. Moreover, very few reports are available to explore the effect and feasibility of AHP pretreatment of SCB for biohythane production. In the recent study,
n Hilares et al. used hydrodynamic cavitation-assisted AHP for Tera efficient removal of lignin from SCB before bioethanol production. They observed that the addition of H2O2 in sodium hydroxide (NaOH) accelerate the pretreatment of SCB and significantly
n Hilares et al., 2018a). Apart removed the lignin up to 63.3% (Tera from these, a very few reports are available on the selection of suitable HRT both for acidogenesis and methanogenesis using lignocellulosic wastes for continuous biohythane production. Therefore, the aim of the present study was divided into three parts: firstly to evaluate the efficiency of AHP pretreatment to

691

remove the lignin of SCB; secondly evaluation of pretreated SCB (PSCB) supplemented with WH towards biohythane production in both batch and continuous system and finally the material and energy recovery analysis of biohythane process to find out the feasibility and sustainability of the process. 2. Materials and methods 2.1. Substrate and inoculum The SCB was collected from local market in Indian Institute of Technology (IIT) Kharagpur campus and WH was harvested from the ponds situated near to IIT Kharagpur. The leaves of WH are the easiest to be degraded by the microorganisms because they contain mostly cellulose and hemicellulose and little lignin and ash. On the other hand, roots and stems contain mostly ash and heavy metals and lower amount of cellulose and hemicellulose, making them difficult to use as feedstock for bioenergy production (Lay et al., 2013). Therefore, only leaves parts of WH were considered in the present study. Biomasses were washed using tap water and dried in air. After drying the size of biomasses was reduced by grinding (using Mixer Grinder, Bajaj 500 W, India) and sieving (3 mm). The characteristics of SCB and WH are shown in Tables 1a and 1b. Acidogenic and methanogenic cultures were used for biohydrogen and biomethane production, respectively. The details of culture development were reported elsewhere (Kumari and Das, 2015). 2.2. Pretreatment and hydrolysis of SCB H2O2 in alkaline condition was used to pretreat the SCB. The solution of AHP was prepared by adding 1% (w/v) NaOH in the solution of 2.5% (v/v) H2O2. 10 g SCB was mixed with 100 mL AHP solution and kept at 50
C temperature for the time period of 30, 60, 90, 120 and 150 min (Wi et al., 2015). After pretreatment the residues were separated by filtration. The separated residues were washed with tap water and dried at room temperature till the weight became constant. The dried residues were further used for hydrolysis and chemical compositional analysis. The hydrolysis of PSCB (at suitable condition) was performed according to our previous study (Kumari and Das, 2015). The hydrolysed SCB was further used for biohydrogen production. 2.3. Biohydrogen production in batch system The hydrolysed SCB (10 g/L) was supplemented with different concentrations of WH (5e25 g/L, with the interval of 5 g/L) and used for biohydrogen production. 100 mL anaerobic serum bottles

Table 1a Compositional characterization of sugarcane bagasse and water hyacinth leaf. [Values correspond to mean ± standard deviation of the measurement, n ¼ 3]. Parameters

Sugarcane bagasse

Water hyacinth

Volatile solid Moisture content Ash content Cellulose Hemicellulose Lignin Carbon Nitrogen Hydrogen Oxygen C/N molar ratio Empirical formula

97.91 ± 1.50 6.83 ± 0.17 2.09 ± 0.14 42.3 ± 0.76 21 ± 0.40 17.4 ± 0.5 45.2 ± 0.86 1.72 ± 0.06 6.8 ± 0.10 45.4 ± 0.70 26 C30H56O23N

89.13 ± 1.25 9.75 ± 0.15 10.87 ± 0.76 24.8 ± 2.0 30 ± 1.75 5.6 ± 2.5 31.5 ± 0.76 2.80 ± 0.08 6.2 ± 0.15 31.7 ± 0.72 11 C13H31O14N

*All values are expressed in % w/w except molar ratio and empirical formula.

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S. Kumari, D. Das / Journal of Cleaner Production 207 (2019) 689e701 Table 1b Characterization of common elements present in water hyacinth leaf. [Values correspond to mean ± standard deviation of the measurement, n ¼ 3]. Elements

Quantity (mg/100 g)

Magnesium Aluminium Phosphorus Manganese Iron Cupper Zinc

2018 ± 59 560 ± 14 2089 ± 84 640 ± 27 100 ± 9.8 2.5 ± 0.1 10.5 ± 1.1

(working volume, 80 mL) were used to carry out the experiments. The initial pH of the media in each bottles were adjusted to 6.5 by using 1N hydrogen chloride (HCl) or 1N NaOH. Further, inoculum (acidogenic mixed consortia, 10% (v/v)) was added and the bottles were flushed with nitrogen gas (for 5 min) to make the environment anaerobic. The experiments were performed at 37
C and 180 rpm using shaker incubator (New Brunswick Scientific, Classic C-24). Gas production was measured after 24 h by water displacement method and the H2 content in the biogas was analysed using Gas chromatography (GC). Controlled experiment was also carried out in which hydrolysed SCB was supplemented with yeast extract (6 g/L). The suitable concentration of yeast extract was determined from our previous study (Kumari and Das, 2017). 2.4. Biohythane production in continuous system A 0.5 L double jacketed reactor was used for 1st stage H2 production (acidogenesis) while a tubular reactor made entirely of Borosil Glass (outer diameter  height, 126  280 mm) with working volume of 4 L was used for 2nd stage CH4 production (methanogenesis). The temperature and agitation of both the reactors were maintained at 37
C and 280 rpm using Grant circulating water bath and magnetic stirrer (IKA C-MAG HS7), respectively. Two peristaltic pumps (Watson Marlow 120 U/R) were provided at inlet and outlet lines of the reactors to draw feed into the reactor and effluent into the drain tank, respectively. The biogas produced during fermentation was collected using water displacement method. The acidogenic reactor was operated at HRTs of 40-7 h (by changing the dilution rate (D) from 0.025 to 0.15 h1, with the interval of 0.025). The spent medium remained after dark fermentation was used for 2nd stage continuous CH4 production. The initial pH of acidogenic reactor was maintained to 6.5 ± 0.14 while the initial pH of methanogenic reactor was maintained to 7.5 ± 0.16. Initially, 450 mL of SCB-WH mixture (1:2 ratio, soluble chemical oxygen demand (SCOD) 30 ± 2 g/L) and 50 mL of inoculum (acidogenic culture) was added into the acidogenic reactor and was operated anaerobically in batch mode until achieving the maximum H2 generation rate. This was followed by continuous mode to achieve the highest H2 yield. The continuous mode was operated at different HRTs as mentioned above. Similarly, continuous CH4 production was performed at various HRTs (14, 12, 10 and 8 d) using acidified effluent obtained after 1st stage dark fermentation. 2.5. Analysis The H2 and CH4 content of the biogas produced after dark fermentation and AD processes respectively were analysed by GC (Agilent Technology 7890A U.S.A). The details of GC operation was reported elsewhere (Kumari and Das, 2015). CHNS analyser (Vario MACRO cube CHNS, elementar) was used

to analyse the composition of elements present in lignocellulosic biomass. Lignin, cellulose and hemicellulose content were determined using National Renewable Energy Laboratory (NREL) standard protocol (Sluiter et al., 2004). American Public Health Association (APHA) standard protocol was used to determine the total solids (TS) and volatile solids (VS) content (Federation, 1999). Automatic Oxygen Bomb Calorimeter (6100, Parr Instruments, USA) and chemical oxygen demand (COD) measurement instrument set (DRB200 and DRB800 Portable Spectrophotometer, HACH, USA) were used to measure the calorific value and COD of samples, respectively. The concentrations of cell biomass were determined by gravimetric method (Bratbak and Dundas, 1984). Atomic absorption spectroscopy (Perkin-Elmer) was used to determine the elements present in water hyacinth. The samples were prepared as per the protocol reported by Suvardhan et al. (2003). The moisture content of sugarcane bagasse and water hyacinth were determined by drying at 60 ± 5
C in hot air oven. The ash content was determined by burning at 600
C for 3 h in muffle furnace (Federation, 1999). The morphological changes of SCB upon pretreatment were analysed by scanning electron microscopy (SEM) (ZEISS EVO 60). The crystallinity of SCB before and after pretreatment was determined by X-ray Diffractometer (XRD) (D8 Advance, Bruker, Germany). The crystallinity index (CrI) was calculated as per the empirical formula proposed by Segal et al. (1959). The change in the chemical composition of SCB after pretreatment was analysed using Fourier transform infrared (FTIR) spectroscopy (NEXUS-870, USA). The details of sample preparation for all the analyses were reported elsewhere (Kumari and Das, 2015). Cell growth kinetic parameters of acidogenic mixed consortia were determined using Monod model Eq. (3) (Mullai et al., 2013)

m¼

mmax S S þ Ks

(3)

Where, m is the specific growth rate of the cells, mmax is the maximum specific growth rate of the cell, S is limiting substrate concentration and KS is Monod constant (Gadhe et al., 2014). The H2 production profile in batch system was validated by using modified Gompertz equation (Eq. (4)).

   Rm  e ðl  tÞ þ 1 HðtÞ ¼ P exp  exp P

(4)

Where, H (t) denotes the cumulative product formation, Rm is the maximum rate of product formation, l is the lag time and P, the product formation potential. The value of “e” is 2.72 (Marone et al., 2014). 3. Results and discussion 3.1. Effect of AHP pretreatment on lignin reduction of SCB H2O2 in presence of alkali effectively removes lignin by partial solubilization of lignin bonds. The reduction in lignin content of SCB after AHP pretreatment was analysed and it is presented in Fig. 2. The delignification of SCB was directly proportional to pretreatment time. Up to 85 ± 2% (w/w) lignin reduction was observed after 120 min pretreatment at 50
C. No significant increase in lignin loss (89 ± 3% w/w) was observed with further increase in pretreatment time (150 min). Apart from lignin, the changes in the composition of cellulose and hemicellulose were also analysed. The maximum loss in hemicellulose after 120 min pretreatment time at 50
C was 22.3 ± 0.7% (w/w). The loss in cellulose was lower (4.75 ± 0.35% w/ w). Hemicellulose is the amorphous cellulose which is easily degraded at high temperature whereas cellulose is crystalline in

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approximately 40.5%. Upon AHP pretreatment, sequential removal of lignin was observed with increasing pretreatment time. This increased the CrI of SCB from 50 0.8% (30 min pretreatment) to 62.6% (150 min pretreatment). The increase in CrI value indicates the decrease in lignin content (Kim et al., 2013). Hence, the XRD analysis confirms the reduction in lignin content of SCB after AHP pretreatment.

Fig. 2. Material loss analysis in terms of cellulose, hemicellulose, lignin and dry weight during AHP pretreatment of sugarcane bagasse (error bar indicate the standard error of the individual measurements, n ¼ 3).

nature, and difficult to degrade. Solid recovery is also an important parameter in the pretreatment process. Therefore, the total solid recovered after pretreatment was determined. As expected, the solid recovery decreased with increasing pretreatment time. This is because of the solubilization of lignin derived compounds and hemicelluloses. The maximum solid recovered after 120 min pretreatment time was 74.7 ± 1.25% (w/w). Generally delignification efficiency is directly proportional to time at higher temperature. However, this process consumes more energy which is also an important factor to consider. Therefore, 120 min pretreatment time was considered for further study. 3.2. Analysis of untreated and pretreated SCB The changed in the morphological structure, CrI and chemical composition of SCB after pretreatment were analysed using SEM, XRD and FTIR spectroscopy, respectively. 3.2.1. SEM The morphological change of SCB after AHP pretreatment was analysed using SEM. Significant morphological changes were observed during pretreatment of SCB (Fig. 3). The morphology of untreated SCB was highly rigid and undamaged (Fig. 3A). Upon AHP pretreatment the SCB became distorted. As the pretreatment time increased the exposure of internal structure of SCB increased (Fig. 3B-F). The microfibrils looked more separated. This increased the porosity and the enzyme accessible surface area. The AHP pretreatment decreased the recalcitrant structure of SCB and exposed the internal cellulose. This confirms the degradation and removal of lignin from SCB. 3.2.2. XRD The crystallinity of SCB is the major parameter to determine the complexity of biomass. This affects the degradation efficiency of microorganism for bioenergy production. Fig. 4 shows the XRD pattern of untreated and AHP pretreated SCB. The diffraction peak at 2Ɵ of 22
represents the crystalline region whereas the peak at 2Ɵ of 18
represents the amorphous region (Chen et al., 2012b). The CrI denotes the amount of crystalline cellulose present in the lignocellulosic biomass and its value depends on the chemical composition of biomass. The CrI of untreated SCB was

3.2.3. FTIR The compositional change of SCB upon AHP pretreatment was analysed and it is presented in Fig. 5. Decrease in the intensity of bands related to cellulose, hemicellulose and lignin were observed after AHP pretreatment. The diffraction bands at 3383 cm1, 2928 cm1, 1253 cm1, 1054 cm1and 667 cm1 corresponds to O-H vibration, C-H vibration, ester absorbance, C]O vibration and C-OH bending deformation, respectively (Sun et al., 2000; Sun and Tomkinson, 2002). The transmittance peak at 3383 cm1 and 1054 cm1 was very sharp in spectrum of untreated SCB but it became blunt as the pretreatment time increased. The transmittance peak intensity related to carbohydrate-lignin linkage (1054 cm1) got decreased. The sharper peak at 2928 cm1 and 667 cm1 prove the removal of lignin after AHP pretreatment (Fig. 5). 3.3. Evaluation of PSCB supplemented with WH towards biohydrogen production Batch experiments were carried out to evaluate the potentiality of PSCB supplemented with WH towards biohydrogen production. The cumulative gas and H2 production of 111.6 ± 1.9 and 72.5 ± 1.3 mL/g COD, respectively were observed at PSCB-WH combination ratio of 1:2 (soluble COD, 30 ± 2 g/L). A further increase in PSCB-WH ratio (1:2.5) was found to decrease the H2 production (Fig. 6a). It is obvious that the H2 yield is directly proportional with the substrate concentration but increasing the substrate concentration at higher level would be detrimental to the cells (Antonopoulou et al., 2011). Lee et al. (2008) determined the suitable substrate concentration of 32 g COD/L for H2 production. Moreover, the suitable substrate concentration also depends on the type of substrate and microorganism used for fermentation process. In case of PSCB supplemented with yeast extract, the maximum gas and H2 production of 92 ± 2.1 and 67 ± 2.0 mL/g COD, respectively were observed whereas solely PSCB gave the maximum gas and H2 production of 47 ± 2.5 and 28 ± 1.5 mL/g COD, respectively (Table 2). In any fermentation process, a proper carbon to nitrogen (C/N) ratio is required for better microbial growth and product yield (Kumari and Das, 2017). In addition, some microelements viz. Fe, Cu, Zn P etc. are also required which serve as cofactor of different enzymes involved in fermentation process. In the present study the acidogenic mixed consortia used for biohydrogen production is dominated with Clostridium sp. (Kumari and Das, 2017). Clostridium sp. contain Fe-Fe hydrogenase enzyme which is the key enzyme for H2 production. Mg acts as a cofactor of several glycolytic enzymes and chelates with adenine nucleotide for cellular phosphate transfer reaction (Walker, 1994). Presence of Fe, Mg and other microelements in WH leaves (Table 1b) could be the major cause of high H2 yield. The VFAs composition also plays an important role in the fermentation process. Therefore, the effluent remained after biohydrogen production was analysed for VFAs content using GC. Predominance of acetate and butyrate were observed in all sets of experiments with the concentrations varied from 220 ± 25 mg/L to 370 ± 30 mg/L and 420 ± 35 mg/L to 620 ± 55 mg/L, respectively. Very low amount of propionate and ethanol were observed

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Fig. 3. Scanning electron microscopic image of untreated and AHP pretreated sugarcane bagasse.

(Fig. 6b). The high butyrate concentration reveals that the fermentation pathway was dominated by butyrate type fermentation. This result also support our previous study (Kumari and Das, 2016). 3.4. Kinetic models: parameters estimation and validation of biohydrogen production process The kinetic parameters of microorganism depend on the type and amount of substrate used. Therefore, the cell growth kinetic parameters viz. mmax and Ks of acidogenic mixed consortia was determined using suitable concentration of PSCB-WH (soluble COD, 30 g/L) in batch system. The values of mmax and Ks were estimated as 0.189 ± 0.05 h1 and 7.8 ± 0.28 g COD/L, respectively. In the continuous system, the D depends on the flow rate (F) and the volume of reactor (V) (Eq. (5)). At a given D (under sterile

condition), the rate of accumulation of bacteria inside the reactor (dx/dt) is determined by the rate of growth of cells minus rate of loss of bacteria through the outlet (Eq. (6)). Under steady state condition, the rate of accumulation of cells inside the reactor is zero. Hence, the rate of growth of cells is equal to the D (Eq. (8)). So, the equation of dilution rate can be written in terms of Monod equation (Eq. (9))

D¼

F V

      dx dx dx ¼  : dt accumulation dt growth dt cellwashout

(5)

(6)

S. Kumari, D. Das / Journal of Cleaner Production 207 (2019) 689e701

Dwashout ¼

Fig. 4. X-ray diffraction pattern of untreated and AHP pretreated sugarcane bagasse at 50
C for 30, 60, 90, 120 and150 min.





 dx ¼ mX  DX dx accumulation

D¼

mmax  S Ks þ S

Ks þ So

(10)

At Dwashout, the effluent substrate concentration (S) becomes equal to the initial substrate concentration (So). The Dwashout for the present system was determined to be 0.15 h1 (Eq. (10)). Hence, dilution range should be decided below critical value (D < Dwashout) for continuous system to increase the H2 production rate. Further, the kinetic parameters of batch fermentative H2 production viz. Pmax, Rm and l were estimated by numerical simulation of experimental data using MATLAB 6 software. The l, Rm and P value were determined as 1.9 h, 7.3 mL/g COD.h & 87.3 mL/g COD respectively. l value signifies the lag phase, Rm rate of H2 production and P is the maximum H2 production potential of acidogenic mixed consortia. The correlation coefficient (R2) value was greater than 0.99. This shows the validation of modified Gompertz equation for hydrogen production using PSCB co-supplemented with WH (Fig. S1). 3.5. Continuous biohydrogen production using PSCB cosupplemented with WH

(7)

 dx ¼ 0 ðunder steady state conditionÞ dx accumulation

Hence;m ¼ Dðat steady state conditionÞ

mmax  So

695

(8)

(9)

If the D is too high the cells cannot grow fast enough to reach steady state. This leads to washout of the cells

In batch process, 1:2 ratio of PSCB:WH (soluble COD, 30 ± 2 g/L) was found to be suitable for H2 production. Therefore, this substrate concentration was used for continuous H2 production in CSTR. The effect of HRT on hydrogen production rate (HPR), effluent pH, biomass concentration and effluent COD concentrations under steady state condition were investigated and are shown in Fig. 7a. After reactor start up, the initial D was set at 0.025 h1 (HRT 40 h). D was then increased to 0.05, 0.075, 0.1, 0.125 and 0.15 h1 to achieve the desired HRT of 20, 14, 10, 8 and 7 h, respectively. As the HRT decreased the HPR and H2 yield increased and it reached the maximum HPR and H2 yield of 18.9 ± 1.5 mL/g COD.h and 303 ± 10.6 mL/g COD, respectively at HRT 8 h (D 0.125 h1). However, a remarkable decrease in HPR (6.47 ± 0.76 mL/g COD.h) and H2

Fig. 5. FTIR patterns of untreated (raw) and AHP pretreated sugarcane bagasse at 50
C for 30, 60, 90, 120 and150 min.

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However, Antonopoulou et al. (2008) used sweet sorghum for fermentative biohydrogen production under different HRTs and observed that the pH value between 5.0 and 5.7 is suitable for high H2 yield. Valdez-vazquez et al. (2009) used mixture of food waste (60%) and paper (40%) for biohydrogen production in semicontinuous mode and observed that the reactor pH of 6.4 was optimum for H2 production. This means that the performance of bioreactor depends on the type of substrates, kind of inoculum, reactor type etc. Biohydrogen production is always accompanied with soluble metabolites formation. Hence, the distribution of soluble metabolites at each HRT under steady state condition was monitored and it is presented in Fig. 7b. Significant production of acetate and butyrate were observed at each HRT. Propionate and ethanol were also measured with the concentration range of 8.5 ± 1.0 to 19.6 ± 2.5 mg/L and 35 ± 3.2 to 107.4 ± 7.8 mg/L, respectively. As the HRT decreased, the concentration of acetate and butyrate increased with the concentration range varied from 277 ± 18 mg/L to 610 ± 23 mg/L and 335 ± 15 mg/L to 896 ± 28 mg/L, respectively. The high concentration of acetate and butyrate is positively related with high H2 production rate (Alexandropoulou et al., 2018). Angeriz-Campoy et al. (2015) also reported that lower HRT and higher OLR leads to dominance of acetate-butyrate type fermentation pathway (Angeriz-Campoy et al., 2015). 3.6. Second stage continuous biomethane production

Fig. 6. a. Hydrogen production study using PSCB co-supplemented with WH (with varying concentration) in batch system (error bars indicate the standard error of individual measurements, n ¼ 3) [Soluble COD (substrate) concentration: 15 g/L (PSCB:10 g/L & WH:5 g/L), 20 g/L (PSCB:10 g/L & WH:10 g/L), 25 g/L (PSCB:10 g/L & WH:15 g/L), 30 g/L (PSCB:10 g/L & WH:20 g/L), 35 g/L (PSCB:10 g/L & WH:25 g/L)]. 6b. Soluble metabolites formed after dark fermentation in batch system (error bars indicate the standard error of individual measurements, n ¼ 3).

yield (86 ± 4.7 mL/g COD) were observed when the HRT further decreased to 7 h (D 0.15 h1). As the HRT decreases, the S increase and the biomass concentration (X) decrease. The Dwashout value for this system was determined to be 0.15 h1 (section 3.4). Hence, the washout of the H2 producing bacteria at D 0.15 h1 might be the reason of decrease in HPR. Moreover, the low X was also observed at D 0.15 h1 (0.27 ± 0.02 g/L) (Fig. 7a). The effluent pH (reactor pH) at each HRTs varied between 4.48 and 4.56 (Fig. 7a). According to Wang et al. (2010), the pH range of 4.4e4.8 is ideal for biohydrogen production in CSTR mode.

In order to assess the rate of CH4 production and extent of methanogenesis at different HRTs viz. 14, 12, 10 and 8 d, the continuous methanogenic reactor was fed with acidified effluent (COD, 19.5 ± 1.5 g/L) obtained from the acidogenic reactor operating at HRT 8 h in continuous mode. The rate of methane production (MPR) at different HRTs was analysed and it is presented in Fig. 8a. Initially, the MPR increased from 14.6 mL/g COD.d to 29.2 mL/g COD.d with decrease in HRT from 14 d to 10 d. Lower HRTs resulted in an increased in OLR inside the reactor which is essential for growth and activity of the microorganism as well as for better product yield. A further decrease in HRT to 8 d resulted in a significant decrease in MPR (11.1 mL/g COD.d). Hence, in the present study HRT of 10 d was found to be suitable for better CH4 yield in continuous system using acidified effluent of dark fermentation. The effluent pH at each HRT was varied between 8.0 and 9.05 (Fig. 8a). The ammonia concentration after biomethanation process was found to be in the range of 0.075 ± 0.0042 g/L to 1.28 ± 0.82 g/L which is below the reported inhibitory range (Prochazka et al., 2012). The concentration and composition of soluble metabolites after biomethanation is the key factor to determine the performance of bioreactor. Acetic acid is the main substrate which is being converted to CH4 by acetoclastic bacteria whereas butyric acid first converted to acetic acid and further to CH4. Ethanol does not produce CH4. The decreasing concentration of acetic and butyric acid was observed at each HRT (Fig. 8b). This indicates an efficient consumption of acetic and butyric acid during CH4 production.

Table 2 Total gas productions, hydrogen production & characteristics of soluble metabolites formed after dark fermentation in batch system using solely pretreated sugarcane bagasse and pretreated sugarcane bagasse supplemented with yeast extract. Parameters

Using solely PSCB

PSCB supplemented with YE

Total gas production (mL/g COD) Total hydrogen production (mL/g COD) Effluent pH Acetate (mg/L) Butyrate (mg/L)

47 ± 2.5 28 ± 1.5 4.18 ± 0.02 159 ± 8.5 215 ± 9.2

92.0 ± 2.1 67.0 ± 2.0 4.21 ± 0.03 352.5 ± 12.5 599.0 ± 11.0

*PSCB: pretreated sugarcane bagasse; YE: yeast extract, SCB 10 g/L, YE 6 g/L.

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Fig. 7. a. Effects of HRT on hydrogen production rate, cell mass concentration, COD concentration and effluent pH under steady state condition in continuous system (continuous stirrer tank reactor) using mixture of PSCB and WH (soluble COD, 30 ± 2 g/L) (error bars indicate the standard error of individual measurements, n ¼ 3). 7b. Composition of soluble metabolites after dark fermentation in CSTR (under steady state condition) at different dilution rates (error bars indicate the standard error of individual measurements, n ¼ 3).

The H2 and CH4 yield obtained from the present study was compared with the reported data (Table 3). From Table 3, it can be observed that, the rate of hydrogen production obtained in the 1st stage of continuous biohythane production process using mixture of SCB and WH is comparatively higher than other reported data whereas the rate of 2nd stage methane production is higher than the data reported by Zhu et al. (2008) and Lay et al. (2016) but lower than the data reported by Liu et al. (2006), Venetsaneas et al. (2009), Luo et al. (2011), Micolucci et al. (2014) and Dareioti and Komaros (2014). The variation in the product yield might be due to the variation in the type of substrate and microorganism used for continuous biohythane production process. 3.7. Material analysis, energy recovery and COD mass balance of the continuous biohythane production Material and energy analysis of bioprocess is essential to find

out the potentiality of an energy generation system. This section deals with the biogas recovery, COD removal efficiency and total gaseous energy recovery efficiency of biohythane production using PSCB co-supplemented with WH (SCOD, 30 ± 2 g/L) (Fig. 9). 1 kg COD was considered as the basis of initial substrate concentration. After 1st stage dark fermentation process (operated at HRT 8 h), the maximum H2 (hydrogen content in the gas: 60 %v/v) and CO2 production of 27 ± 2.7 g and 398 ± 15 g, respectively with COD removal of 35% (effluent COD, 650 ± 15 g) were observed. Biomethanation process (operated at HRT 10 d) using spent medium of dark fermentation gave the maximum CH4 (methane content in the gas: 48% v/v) and CO2 production of 92.67 ± 3.4 g and 303.5 ± 17.6 g, respectively. This increased the COD removal efficiency up to 86% (effluent COD, 140 ± 5 g) (Fig. 9a). The COD mass balance of biohythane production process was also performed. The COD mass balance closer to 88.6% and 85.5% proves the sustainability of the process (Fig. 9b).

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Fig. 8. a. Effects of HRT on methane production rate, ammonia concentration and effluent pH after biomethanation process (using spent of dark fermentation operated at HRT 8 h) under steady state condition in continuous system (continuous stirrer tank reactor) (error bars indicate the standard error of individual measurements, n ¼ 3). 8b. Soluble metabolites concentration (under steady state condition) after biomethanation process (operated at different HRTs in continuous system) (error bars indicate the standard error of individual measurements, n ¼ 3).

The total gaseous energy recovery using two stage biohythane production was calculated based on the heating value of H2 (142 MJ/kg) and CH4 (55.5 MJ/kg) and the calorific value of substrate (14.7 MJ/kg COD). In the 1st stage dark fermentation process, 3.83 MJ energy was recovered as H2 and after 2nd stage biomethanation process, 5.14 MJ energy was recovered as CH4 considering 1 kg COD as the initial feed. This corresponds to the maximum gaseous energy recovery of approximately 61% of the substrate energy input (excluding the process energy). However, the energy recovery analysis including all the input process energy is required to determine the cost of biohythane production process. 4. Conclusion Use of mixture of SCB and WH revealed an useful approach for

biohythane production which could be sustainable and environment friendly. AHP pretreatment was found to be an effective method to remove the lignin of SCB as confirmed by SEM, XRD and FTIR analyses. The continuous biohythane production using pretreated SCB and WH gave the maximum H2 and CH4 yield of 27 g/kg COD (HRT, 8 h) and 92.64 g/kg COD (HRT, 10 d), respectively in CSTR. This corresponds to the total gaseous energy recovery of 8.97 MJ/kg COD (61% of substrate energy input) with maximum COD reduction of 86%. However, the input cost and the cost of operation of each process need to be evaluated. Moreover, the operation cost may be reduced by reducing the pretreatment time using some newly emerging technique such as hydrodynamic cavitation. Nevertheless, the scalability of the whole process is the major challenge. The conditions followed during shake flask or lab fermentation may not suit for high volume cultivation. The recovery of the product is also

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Table 3 Comparison of biohythane production in continuous system using different lignocellulosic wastes. Substrate

Hydrogen production stage Inoculum

House hold solid waste Potato waste Cheese whey Ethanol stillage Food waste

pH Temp. (
C)

Methane production stage HRT (h)

HPR (mL/ L.h)

Inoculum

e e 35 Anaerobic digester 5.5 35 sludge Indigenous microflora 5.2 35

48 6

43 119

24

120.8

Anaerobic digested 6.0 55 manure Indigenous microflora e e

72

69a

e

60a

6.0 37

18

72

6.5 45 6.5 37

24 8

1.1 568

e Anaerobic sludge Anaerobic sludge Anaerobic manure Anaerobic sludge Anaerobic sludge e Anaerobic sludge

Mixture of OMW, CW and e LCM WH Pig slurry SCB þ WH Cow dung

References

pH

Temp. (
C)

HRT (d)

MPR (mL/ L.d)

digester

e 7.0

35 35

15 1.25

500 187

(Liu et al., 2006) (Zhu et al., 2008)

digester

e

35

20

1000

digested

e

55

12

1300

(Venetsaneas et al., 2009) (Luo et al., 2011)

digester

e

e

e

e

(Micolucci et al., 2014)

digested

7.78 e

25

330

digested

e 7.5

e 10

82.4 300

(Dareioti and Kornaros, 2014) (Lay et al., 2016) Present study

e 37

a Unit in “mL/g-vs”; SCB: sugarcane bagasse, WH: water hyacinth; OMW: olive mill wastewater; CW: cheese whey; LCM: liquid cow manure; HPR: hydrogen production rate; MPR: methane production rate; HRT: hydraulic retention time.

Fig. 9. a. Material and energy recovery analysis of two stage continuous biohythane production operated for 8 h (1st stage H2 production, CSTR) and 10 d (2nd stage CH4 production, CSTR) using PSCB and WH (1:2 ratio) (soluble COD, 30 ± 2 g/L). 9b. Material analysis in terms of COD for two stage continuous biohythane production operated for 8 h (1st stage H2 production, CSTR) and 10 d (2nd stage CH4 production, CSTR) using PSCB and WH (1:2 ratio) (soluble COD, 30 ± 2 g/L).

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