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Operational behavior of a hydrogen extractive membrane bioreactor (HEMB) during mixed culture acidogenic fermentation
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Operational behavior of a hydrogen extractive membrane bioreactor (HEMB) during mixed culture acidogenic fermentation Juan E. Ramı´rez-Morales a,*, Estela Tapia-Venegas a, Jose Luis Campos b, Gonzalo Ruiz-Filippi a Escuela de Ingenierı´a Bioquı´mica, Pontificia Universidad Catolica de Valparaı´so, Av Brasil 2085, 234-0950, Valparaıso, Chile b n ~ ez, Avda Padre Hurtado 750, Vin ~ a del Mar, Chile Faculty of Engineering and Science, Universidad Adolfo Iba a
highlights A
process
integrating
graphical abstract gas
separation-membranes and Bio-H2 production is presented. Membrane module was able to extract and partially separate H2 and CO2 generated. H2 partial pressure was reduced 11% in the bioreactor-headspace with a membrane. Decreasing H2 partial pressure on the mixed culture had a positive effect on H2 yield. An extractive membrane bioreactor can generate a H2 rich stream of 68% (v/v).
article info
abstract
Article history:
Fermentative hydrogen production requires a continuous products-removal and effective
Received 15 May 2019
upgrading steps to improve its general performance. Therefore, implementation of new
Received in revised form
technologies capable of achieving both requirements is essential. We present the opera-
14 July 2019
tional behavior of a new process concept based on integration of membranes for gas
Accepted 10 August 2019
separation and fermentation technology. This process, which we term as hydrogen extractive membrane bioreactor consists of coupling two dense polymeric membranes to a hydrogen producing culture. The process automatization of this system was essential to
Keywords:
maintain the proper operational pressures in the membrane module and in the bioreactor-
Biohydrogen separation
gas-phase. This system was able to extract and partially separate the hydrogen and carbon
Fermentative hydrogen upgrading
dioxide generated. The hydrogen partial pressure was reduced from 55.5 to 49 KPa, which
Hydrogen partial pressure
means
an
increase
of
hydrogen
yield
of
16.3%
* Corresponding author. E-mail address: [email protected] (J.E. Ramı´rez-Morales). https://doi.org/10.1016/j.ijhydene.2019.08.077 0360-3199/© 2019 Hydrogen Energy Publications LLC. Published by Elsevier Ltd. All rights reserved.
(1.1e1.28
mol-H2/mol-glucose).
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Polymeric membrane
Simultaneously, the implemented system generated a final hydrogen stream 13% (v/v)
Gas extractive fermentation
more concentrated than a conventional process. © 2019 Hydrogen Energy Publications LLC. Published by Elsevier Ltd. All rights reserved.
Introduction Fermentative hydrogen from mixed cultures has become a promising alternative for bioenergy generation using organic wastes [1]. In addition, its by-products can be considered as potential microbial metabolites within a biorefinery framework [2]. Although fermentative hydrogen achieves higher experimental hydrogen yields than other biological production processes, there are still challenges to improve its performance and efficiency [3]. Moreover, effective integration of strategies to increase simultaneously the yields of products and optimize their recovery and purity are still in an early stage of applied research [4]. Many factors influence the complex process of fermentative hydrogen production, such as type of substrate, inoculum, pH, temperature, reactor design, hydraulic retention time (HRT), substrate concentration, organic loading rate (OLR) and hydrogen (H2) partial pressure. Among them, the later seems to be one of the most important factor [5e9]. To alleviate the negative effect of H2 partial pressure, various strategies have been adopted: vacuum application and increasing the stirring rate [10], improve gas transfer from the liquid phase to the gas phase by changing reactor configuration [11], lowering the total pressure in the headspace [12], increasing surface area changing the size of the reactor [13] and gas sparging/flushing with different gases (N2, CO2, CH4 or internal biogas) [5,9,12,14e17]. In the past years, there has been some efforts for trying to establish a consensus about the positive effects of decreasing the H2 partial pressure on fermentative mixed cultures. For continuous cultures, where a stable system condition has been established, gas sparging/flushing has shown to improve the process performance. The general assumptions for explaining the increase of the hydrogen yields during a reduction in the H2 partial pressure are based on the thermodynamics of the biological reactions responsible for generation and consumption of H2 (lactate hydrogenase, NADH hydrogenase and homoacetogenesis reactions) [9] or the selection of active hydrogen bacteria by using CO2, which has inhibitory effect on other non-desirable microorganisms like acetogens [15]. Other authors have mentioned that the dissolved hydrogen concentration in the liquid media is much higher than the necessary limit to fall into the (H2) partial pressure regulatory zone due to critical supersaturation phenomena, and it seems that impractically high sparging rates would be needed to overcome that barrier [18,19]. Although continuous H2 extraction by gas sparging/flushing has shown to improve the process performance, from a practical perspective and full-scale implementation, this strategy would be energy intensive, due to the need for gas
compression and the high dilution of the final gas generated. Alternatively, membrane technology stands out as robust approach to extract continuously hydrogen and deal with the H2 partial pressure effect. Furthermore, using this technology, it would be possible to obtain a rich hydrogen stream feasible for direct application in fuel cell systems [20]. In recent years, membrane separation technology has grown rapidly, promoting the innovation in process intensification, purification and product recovery. It provides lower costs and power requirements, it is easily integrated to other processes, and thus, it is able to play a key role in biorefining and bioenergy production [21]. Nowadays, palladium (Pd) and silica based membranes systems are being considered as good candidates to separate the H2/CO2 gas mixture produced in thermo-catalytic processes carried out at high temperatures (200e700 C) [3,22]. However, such temperatures are not characteristic in biological systems for hydrogen production and the membranes to be used must be different. Alternatively, polymeric membranes with operating temperatures typically less than 100 C would be more appropriate. Most studies on biological hydrogen separation have been carried out using nonporous, polymeric and ionic liquid based membranes with synthetic mixtures, which simulate biohydrogen mixtures [23]. Investigations have focused on membrane contactors with moving liquid carriers [24,25], dense polyimide based membranes [26,27], supported ionic liquid membranes (SILMs) [28] and integrated systems of porous/non porous dense membranes [29,30]. However, in most of the cases the studies did not couple the effect of the gas extraction on the culture performance and the lab scale system setup had practical limitations to be implemented in continuous mode. Regarding the efforts for decreasing the H2 partial pressure using extractive membranes, some studies have evaluated the possibilities of gas extraction from the liquid and gas phase of the reactor [31,32]. Despite the potential of such submerged membranes to extract the dissolved gases directly from the liquid, they also have problems of biofouling and rapid deterioration over time. On the other hand, implementation of membrane gas extraction setups in contact with the gas phase could avoid some of these issues. However, they also would need a proper automatic control operation, which in many cases represents a technical challenge in bench-scale systems. For coupling the bioreactor to a membrane system, previous studies on membrane characterization are critical in order to find suitable operational parameters like the transmembrane pressure and its effect on the permeability, selectivity and recovery (stage-cut). We implemented the system called “hydrogen extractive membrane bioreactor (HEMB)”, introduced for first time in our
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previous study where a gas membrane module was selected and characterized for simultaneous extraction and separation of fermentative hydrogen [33]. Since its introduction, some approaches have tried to implement similar concepts using the same type of membranes for hydrogen upgrading or for returning an enriched CO2 stream back to the reactor [4,29]. However, these studies did not implemented the required automatic control for the integration of the continuous biological process with the membrane systems and there was not a clear effort to continuously stablish lower H2 partial pressures. For this particular integrated concept, process automatization is essential to avoid human assistance when maintaining simultaneously a proper transmembrane and atmospheric pressure in the membrane module and in the gas phase of the bioreactor, respectively. Our system contributes to stablish a simple and closed loop control system, in which it is possible to evaluate the positive effect of decreasing the H2 partial pressure on the mixed culture performance in a bench scale continuous stirred reactor tank reactor (CSTR). In this study, the behavior of the fermentative process is evaluated in terms of H2 productivity and fermentative metabolite production under different operational periods when the continuous hydrogen extraction led to stablish a lower H2 partial pressure inside the reactor. In addition, the possibility of obtaining a H2 rich stream at the outlet of the system using a second membrane module as additional upgrading step is also addressed.
Materials and methods Inoculum and medium composition Granular anaerobic sludge from a full-scale UASB reactor treating tobacco wastewater was used as inoculum. The sludge granules were washed twice with tap water and settled at room temperature. To prevent clogging of the tubing, the granules were sieved through a 0.5 mm mesh. To establish a mixed culture composed of strict anaerobic and facultative anaerobic bacteria, the sludge was not pre-treated thermally according to Tapia-Venegas et al., [34]. The CSTR medium composition was based on a synthetic glucose wastewater and adapted from Tapia-Venegas et al. [11]. The media consisted of 10 g L-1 of glucose and the following nutrients (mg L-1): 1000 NH4Cl, 250 KH2PO4, 100 MgSO4$7H2O, 10 NaCl, 10 NaMoO4$2H2O, 10 CaCl2$2H2O, 9.4 MnSO4$H2O and 2.78 FeCl2. All components were dissolved in tap water and the final feed solution was refrigerated at 4 C to reduce the growth of undesirable microorganisms.
Continuous fermentative hydrogen production A 2.7 L glass-made CSTR with a working volume of 2.0 L was used and started up with 200 mL of inoculum. The agitation speed and hydraulic retention time (HRT) were set up at 100 rpm and 12 h, respectively. The mixed culture was maintained at 37 C and the pH was controlled at 5.5 (as set point) by adding NaOH (2 N) solution. The liquid level was controlled using a capacitive level switch (LP15 Series, Flowline®) and peristaltic pumps for influent feeding and effluent
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draw off were employed (Masterflex, Cole-Parmer, USA). The operational conditions for the CSTR were selected according to the maximum volumetric hydrogen productivity and yield obtained in a previous study [11]. Before the membrane coupling, the mixed fermentation was run until a steady state with respect to the hydrogen production and glucose consumption was reached. Simply, it was assumed that steady state occurred when coefficient of variation (calculated as standard deviation divided by the average) for hydrogen production rate and yield was less than 15%.
Continuous bioreactor-membrane integrated system The membranes used consisted of two lab-scale membrane modules commercially available (Permselect PDMS-XA 2500, MedArray Inc., USA). The same membrane module responsible for extracting and separating partially the biohydrogen generated was characterized in a previous study [33]. Information of the membrane module, such as structural characteristics, CO2 and H2 permabilities and CO2/H2 separation factor are available in the research paper. The membrane used as a second step of biohydrogen upgrading consisted of the same material as the above mentioned but with an area of 10 cm2 and 30 hollow fibers. The continuous experimental set-up is schematically shown in Fig. 1. Membrane (M1) was coupled to the CSTR reactor (R) once the hydrogen production of the mixed culture fermentation reached a steady state. The system was composed of peristaltic pumps, pressure sensors and traps in the different operational lines. The permeate gas stream coming from the membrane (M1) was return to the reactor headspace since it was enriched in CO2 [33]. The membrane (M1) was continuously fed with a peristaltic pump (B1). A cold trap (C) was located in this stream to condensate water vapor, avoiding the water layer formation on the membrane surface (resistance to mass transfer). A second peristaltic pump (B2) acted as a controlled valve, which, by means the peristaltic pump (B1), maintained the headspace reactor (permeate stream) and the feed stream of the membrane at atmospheric pressure (~101 kPa) and 180 kPa, respectively. These operational pressures were selected according to the previous characterization of the membrane modules. Taking into account that the H2 production rate can vary over time due to inherent fluctuations in the biological process, a control strategy was implemented to achieve a stable pressure in both streams. The control system was performed combining a data acquisition system (DAQ, National Instruments Co., USA), board mount gauge pressure sensors, a microcontroller board (Arduino), Labview 8.5 software (National Instruments Co., USA) and a peristaltic pump (Thermo Scientific FH15, UK). The peristaltic pump revolutions increased or decreased according to set pressure ranges based on discrete control steps. To avoid an erratic control, a moving average filter was implemented to counter noisy pressure data signal. In order to have a higher hydrogen composition and remove toxic compounds for direct gas application on a labscale fuel cell (FC), a second membrane (M2) and a H2S trap (S) based on iron hydroxide-based adsorbent were located after the peristaltic pump (B2). A 3-way valve led the continuous feeding of the membrane (M2) and H2 fuel cell. The
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Fig. 1 e Scheme (A) and picture (B) of the continuous experimental set-up (H2 extractive membrane bioreactor, HEMB). The final gas stream generated was applied in a lab-scale fuel cell to produce electricity as a proof of concept.
corresponding area (10 cm2) of the membrane (M2) was chosen to achieve a pressure drop of 80 kPa, taken into account the gas flow generated by the peristaltic pump (B2) and a stage-cut about 0.5. The drop pressure of 80 kPa were maintained as an adequate condition to separate the H2/CO2 gas
Table 1 e Features of different fermentative process periods studied. Periods of fermentative process P1 P2 P3
P4
Membrane configuration
Operational period days
Without membrane CSTR þ membrane system (M1) CSTR þ membrane system (M1) with an initial oxygen input disturbance CSTR þ membrane system (M1 and M2)
0 to 14 14 to 21 21 to 35
35 to 45
mixture generated with help of a needle valve [33]. The outlet gas flow of the system was daily measured by a water displacement system (W) adapted with an electronic balance. The fermentative process operation with or without membrane were divided into four periods P1, P2, P3 and P4. P1 corresponded to the period of CSTR operation without membrane, while in P2, P3 and P4 the system was running with the coupled membrane(s) (CSTR þ membrane system). P2 and P4 periods were similar and P3 had an initial oxygen input disturbance because an operation drawback (see Table 1). The peristaltic pump (B1) tubing was partially broken, which generated a leak and induced a vacuum, entering air into the head space of the reactor. Despite this drawback, the tubing was replaced, the operation was recovered and the process continued. The reactor operation was carried out for 44 days. Before coupling the extractive membrane (M1), the reactor was operated in batch mode for 24 h and then switched to continuous mode for enabling the activation of the microorganisms present in the initial inoculum.
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Analytical methods
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main liquid product followed by acetate and butyrate, both at similar concentrations (Fig. 2B). A similar behavior with ethanol and butyric acid-type fermentations has been found in different studies, where the initial inoculum was not pretreated with a heat shock (like in the current work) but it was aerated previously to the inoculation [35,36]. The membrane module was coupled to the gas-phase of the reactor on 14th day. The effect of the selective hydrogen extraction was observed after 72 h. The composition of hydrogen decreased from 55 ± 3.0 to 49.76 ± 0.40% v/v (Fig. 2C; P2). As the glucose consumption rate remained constant (Table 2), the increase of gas flow was the responsible for an increase on hydrogen yield from 1.1 (P1) to 1.28 mol-H2/molglucose (P2) (Fig. 2D). This implied a positive effect (yield improvement of 16.3%) due to the extractive membrane coupling on the process. This increment was also related to the change of by-products, where acetate and butyrate remained as the main liquid products of the fermentation and ethanol decreased (Fig. 2B). In the literature, this decrease in hydrogen production by increasing the ethanol production is non-obvious, in some cases with glucose as a substrate, the increase of ethanol has a direct relationship with the increases of hydrogen production [37,38]. The biomass concentration was also affected, decreasing from 0.96 ± 0.12 to 0.67 ± 0.16 g VSS/l (Fig. 2D). These average values where obtained from a short operation time where the system run without any disturbances. However, during the 21st day an operation drawback occurred. The peristaltic pump (B1) tubing broke, which generated a leak, induced a vacuum and air entered into the head space of the reactor. Despite this drawback, the tubing was replaced and the H2 extraction process continued. This disturbance generated a transitional operational stage that caused a decrease on productivity and yield (P3). During 9 days, the hydrogen concentration dropped to 42.15 ± 6.15% v/v and again the main fermentation byproduct was ethanol (Fig. 2B). Although the process performance was affected, the culture was slowly recovering and the hydrogen concentration reached 50.63 ± 2.35% v/v at the period defined as P4. Until this point, biomass and hydrogen yield were similar to the operational performance of the period P1 (Table 2). Mass balances of the corresponding periods counted for 80% of the inlet COD, which implies that
Gas sample compositions (hydrogen, nitrogen, methane, and carbon dioxide) were analyzed by injecting samples into a gas chromatograph (PerkinElmer Clarus 500) equipped with a Haysep Q 80/100 13’x 1/800 OD column (Alltech Co., USA) and a thermal conductivity detector (TCD). Injector and detector temperatures were 80 and 120 C, respectively. The initial temperature of the column was 30 C, followed with a ramp up to 80 C. The helium carrier gas flow rate was 15 ml/min. The hydrogen composition in the biogas (%H2) can be directly related to the hydrogen partial pressure. However, partial pressure of the gas component (Ppi) can be calculated as: Ppi ¼ PT Xi where PT is the total absolute pressure of the gas and Xi is the volume fraction of the gas component. Volatile fatty acids (VFA) were analyzed with a gas chromatograph (Shimadzu, Kyoto, Japan) fitted with a FID detector and a ID GP 60/80 Carbopack C/0,3% Carbowax 20 M/0,1% H3PO4 packaged column (Sigma Aldrich, St Louis, MO, US). During the ethanol measurements a gas chromatograph (PerkinElmer Clarus 500) equipped with a wide bore, semicapillary Equity-1 column (Sigma-Aldrich, St. Louis, MO, USA) was used. Volatile suspended solids (VSS) and glucose concentration were measured according to Tapia-Venegas et al. [11].
Results and discussion Operational performance of the HEMB Average values of operational parameters for the periods considered in steady state P1, P2 and P4 are presented in Table 2. P3 was assumed as a stage of transition. During period P1 a stable hydrogen production process was established after a start-up operation of 5 days. From this point, it was assumed a stable production until the 15th day, corresponding to a yield of 1.1 mol-H2/mol-glucose (this assumption was based on the coefficient of variation, as previously mentioned). During this period (P1), the fermentation was dominated by ethanol as the
Table 2 e Operational parameters during the fermentative process, before and after coupling the membrane M1 (averages). Operational parameter
Glucose consumption Biomass Hydrogen composition CO2 composition Methane composition Ethanol Total volatile fatty acids (VFAs) Yield Volumetric production rate COD balance
Unit
% g VSS/l % v/v % v/v % v/v mM mM mol-H2/mol-glu mmol-H2/l h %
Operational period P1
P2
P3
P4
99,6 ± 0,04 0.96 ± 0.12 55 ± 3.0 46.38 ± 2.36a ND 25.08 ± 3.31 24.44 ± 5.01 1.1 ± 0.1 4.97 ± 0.55 76.07 ± 14.43
99.65 ± 0.02 0.67 ± 0.16 49.76 ± 0.40 52.33 ± 1.00a 1.32 ± 0.95 11.13 ± 6.70 44.08 ± 5.48 1.28 ± 0.15 5.42 ± 0.80 77.33 ± 9.81
99,59 ± 0.14 1.1 ± 0.10 42.15 ± 6.15 57.47 ± 1.53 1.53 ± 0.31 28.34 ± 3.79 35.54 ± 4.08 0.85 ± 0.17 3.99 ± 0.61 78.01 ± 5.02
99.64 ± 0,02 0.91 ± 0.14 50.63 ± 2.35 49.48 ± 2.77 1.86 ± 0.57 20.73 ± 2.51 43.27 ± 3.47 1.08 ± 0.11 5.18 ± 0.30 82.55 ± 4.88
ND: not detected. a The carbon dioxide content of the periods P1 and P2 were examined for statistical significance. When comparing the two periods, the p-value was 0.042 and the result was significant at p < 0.05 (one-way ANOVA).
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Fig. 2 e Operational parameters before (CSTR) and after coupling the extractive membrane (HEMB). The fermentation time was carried out for 44 days, where continuous signals of pH and pressure were captured (A). It is also shown the concentration of different by-products (B), the biogas composition (C), hydrogen yield, volumetric production rate and biomass concentration (D). Dotted vertical lines mark the time of coupling of the extractive membrane. Grey horizontal lines mark steady states for the different periods.
other metabolites missed in the account. The fact that the recovered COD is similar for all the periods, indicates that ethanol or other volatile compounds did not extracted by the membrane process. The recovery period of the culture (P4) shown in Fig. 2D could be explained from the quality characteristics of the inoculum used in the start-up stage. The microbiological diversity of this inoculum was reported in the S0 period of Tapia et al. [20], (Prevotella 35,3%; Veillonellaceae 32%; Clostridium sp 7%; Acetobacter 16,8%, Enterobacteriaceae 1,7%). A disturbance related to an air inlet into the reactor can be addressed positively if the inoculum possesses facultative bacteria, which is responsible for consuming oxygen such as Acetobacter and Enterobacteriaceae family [38]. The inoculum in this case was not subjected to heat shock, which eliminates a high amount of facultative bacteria (i.e. those who cannot form spores). Some studies ensure that using facultative anaerobic bacteria contained in waste activated sludge (WAS) improved the fermentation robustness due to their high growth rate and capability to rapidly recover from an accidental oxygen intrusion [38,39]. Therefore, a culture composed by a consortium from facultative and strict anaerobes could develop a stable and robust process performance. The relationship of the biomass and ethanol concentration with respect to the hydrogen yield is shown in Fig. 3. This data correspond to the operational periods where the reactor operated adequately (P1, P2 and P4). The tendency responds to a decreasing behavior, which was expected as the culture
Fig. 3 e Biomass and ethanol concentrations related to the hydrogen yield during the operational periods P1, P2 and P4. The arrows show the data corresponding to the days of operation of the extractive membrane during P2. generally present higher yields when a butyrate production is preferred. A similar behavior was found by Ref. [40], where ethanol and hydrogen yield correlated negatively during an
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operation of a CSTR. The highest hydrogen yields in Fig. 3 fit to the lowest values of biomass and ethanol concentrations, which in turn correspond to the operational data for the period P2 (arrows in Fig. 3). During these days (6 hydraulic retention times) the membrane module was extracting selectively hydrogen without any operational drawback. It is interesting to note that low amounts of biomass are directly related to the best hydrogen yields when the membrane was coupled. In this case, more electrons coming from the substrate are being disposed as hydrogen, acetate and butyrate instead of biomass and ethanol [12]. This observation could be also related to a higher capacity of the mixed culture to maintain a suitable tendency for fermentative hydrogen production. The effect of CO2 composition can be an influencing factor too. The composition of CO2 increased from 46.38 ± 2.36 to 52.33 ± 1.00% (v/v) for the periods P1 and P2, respectively. The statistical significance was examined performing a one-way ANOVA followed by the least significant difference test (LSD) at a level of p < 0.05, resulting in a p value of 0.04. A CO2 increase in the gas phase had a positive effect on the hydrogen active bacteria, as it was found by Devi et al. [14], and Kim et al., [15]. They reported that CO2 had an inhibitory effect on non-hydrogen active microorganisms (i.e. competitive acetogens and lactic acid bacteria). In this manner, the separated and returned CO2 could have a positive effect on the hydrogen producing microflora and a negative effect on competitive ones. Future research studies focus on detailed analysis of the corresponding bacterial community would evidence enrichment of specific hydrogen producing populations as a result of the hydrogen membrane extraction. When comparing the improvement obtained in the hydrogen yield (increase in 16.3% during P2) with other studies using sparging/flushing, there is a considerable difference. They obtained higher improvements as they dilute the hydrogen content between 7 and 10 times more [15,41]. However, to the best of our knowledge, the current study set a precedent as the first continuous and self-controlled hydrogen-extractive system implemented in the phase gas. The process based on integration of gas membrane separation and fermentation technology could be improved using better membranes with higher selectivity [25,42], in order to reach lower concentrations of hydrogen in the gas-phase and get a richer hydrogen stream in the outlet. In addition, upcoming studies must extend the operation time and carry out analysis of other metabolic products like formate, lactate and ferredoxin, as suggested also by other authors [19].
Continuous upgrading of fermentative hydrogen Fig. 4 shows the hydrogen composition in the retentate of the extractive membrane (M1) and the second one (M2) coupled in series. Hydrogen compositions about 61% (v/v) were obtained in the retentate of M1 during the period P4, and it was possible to increase it using the membrane M2 up to 68% (v/v). Higher compositions could have been obtained if the system had produced hydrogen compositions of 71% (v/v) as it occurred during P2. The automatic control implemented for maintaining the set pressures of the reactor and membrane M1 was avoided this time and only a manual control of the pressure
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Fig. 4 e Hydrogen composition in the retentate stream of two polymeric membranes (M1 and M2) coupled to system. A fuel cell was connected to the retentate stream of the second membrane (M2) to produce electricity (data not shown).
was carried out using a common needle valve. However, as experienced by the operator, a constant human monitoring of the system was necessary, which highlight the importance of the implementation of automated control when the system becomes more complex. Future improvements could facilitate the total automated control of a simultaneous extraction and upgrading hydrogen of a process based on membrane module cascades. In addition, it could be interesting to study the different configurations with other membrane materials having a higher selectivity, in order to reach upper hydrogen compositions with a limited amount of equipment.
Comparison with other studies and perspectives Different systems have been studied to separate bio-hydrogen using membrane contactors with flat sheets and hollow fiber module configurations (Table 3). These approaches have been focused on membrane systems that use absorptiondesorption processes in dense polymeric membranes and separation of fermentative hydrogen using porous and dense materials. In some cases, synthetic mixtures have been used to simulate a gaseous stream produced in the biological process and others have coupled membrane modules to bioprocesses but with a manual or human assisted control. The current study stands out as the first implementation of an automated process for coupling a hydrogen extractive membrane into a continuous biological process. The automatization of membranes coupled to biological systems operated in continuous mode is critical, especially when the system is prone to suffer inherent and external disturbances, like is the case of a hydrogen fermentative process.
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Table 3 e Studies on upgrading bio-hydrogen (fermentative hydrogen in some cases) using different membrane technologies. Gas mixture/biological source
Feed composition (v/v)
Mixed culture Different biological processes Thermococcuslitoralis
67.8% H2 32.1% CO2 H2/CO2/CH4 ~40/35/ 25% H2/CO2/N2 (23% H2)
Synthetic
55% H2/45% CO2
Mixed culture
Mixed culture
51.3 v/v H2, 47.0 v/v CO2, 1.7 v/v undefined 55e58% H2 in biogas
Mixed culture
55% H2/45% CO2
Polymeric membranes/ Modules Dense (PDMS)/Hollow fiber Contactor (PVTMS)/flat sheets Porous (HDPE)þdense (PES/PI)/ Hollow fiber Dense (polyimide)/Hollow fiber
Dense membrane (PDMS)
Nonporous Polydimethylsiloxane (PDMS) membrane modules (PDMSXA-10) Two Dense (PDMS)/Hollow fiber
Liang et al. [31], coupled a silicone rubber membrane into the liquid-phase of a batch culture. They reported that the membrane reduced the biogas partial pressure and improved the hydrogen production rate and hydrogen yield by 10% and 15%, respectively. However, this mode of operation did not permit a continuous extraction of hydrogen from the culture and therefore the effect of the reduced partial pressure of the product gases was not evidenced for a prolonged period. lafi-bako et al. [30], coupled a fermentative hydrogen proBe cess with two polymeric membranes modules. Because the reactor operated in batch mode, the integrated system had to release, compress and store the biogas mixture (H2, CO2 and N2 from sparging) produced in an intermittent way. The final increase in hydrogen composition ranged from 23 up to 73% (v/v) by an integration of a polyethersulfone-polyimide (PESPI) and highly dense polyethylene (HDPE) membranes. Recently, Bakonyi et al. [29] installed a Permselect® (PDMS) gas separation membrane to an anaerobic membrane bioreactor. They used the same membrane module (M2) as it was operated in the current work. They tested its ability to separate hydrogen from the raw fermentation gaseous mixture that was accumulated in a gas bag (non-continuous process). They obtained a final hydrogen composition of 67.3% (v/v), very close to the obtained in this study. The last published approach was made by Bakonyi et al., [4]. They implemented a concept similar to the hydrogen extractive membrane bioreactor (HEMB), which was introduced for first time in our previous study when the same type of membrane was characterized [33]. However, they did an internal recirculation of the membrane streams, with no clear continuous gaseous extraction. They reported changes in the hydrogen productivity comparing different operational periods when CO2 and H2 rich streams were returned to the reactor. However, their microbial community analysis did not show a remarkable difference between periods. They suggested that certain constructional upgrades like the pressure control of the gas streams instead of using manual backpressure regulators would drive the system towards better feasibility. These recommendations were kindly implemented in our setup and the
Results obtained Yield increase (15%) Composition increase H2 (90%v/v), CO2 (99%v/v) CH4 (95%v/v) Composition increase (73% v/v H2)
Reference [31] [24] [30]
65% v/v H2/35%v/v H2/CO2, selectivity of 1.56, recovery factor of 0.72 Up to 67.3 v/v H2
[27]
59e60% H2 in biogas
[4]
H2 enriched biogas (68% H2/32% CO2) Yield improvement of 16.3%
This study
[29]
system was able to extract hydrogen in a continuous and automated mode. Improvements on gas membrane technology (i. e. new materials for higher selectivity to separate the mixture H2/ CO2) could drive the simultaneous extraction and the upgrading/recovery steps of a feasible system. To design an effective purification system based on membrane technology, it is also important to consider the negative impacts of tracelevel substances present in the raw gas mixture on the membrane behavior (e.g. H2S) [43]. Implementation and evaluation of the performance of chemical traps could lead to reach higher performances in the recovery and upgrading steps to ensure the requirements of a direct application of the gas (i.e. fuel cells systems). Thereby, it could be possible to accomplish a balance between recovery and purity of the hydrogen produced by the biological process. Finally, the extractive system should operate under the typical conditions required for the fermentation (adequate temperature and pressure), ensuring a non-intensive energy process.
Conclusion A hydrogen extractive membrane bioreactor (HEMB) setup was implemented. The system contributed to stablish a simple controlled process where we could evaluate the positive effect of decreasing the H2 partial pressure on the mixed culture performance in a bench scale continuous stirred reactor tank reactor (CSTR). The process automatization of this particular system was essential to maintain the proper operational pressures in the membrane module and in the gas phase of the bioreactor during a closed loop control system. The continuous and automated process increased the hydrogen yield in 16.3% and simultaneously generated a hydrogen rich stream of 68% v/v. Improvements on these parameters can be achieved upgrading the system with the new developments on membrane materials and cascade module configurations, driving the feasibility of this concept at higher scales.
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Acknowledgements The authors would like to acknowledge financial support from FONDECYT 3160219 project. This work is dedicated to the memory of our well esteemed and wonderful colleague Prof. Gonzalo Ruiz-Filippi who recently passed away.
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Operational behavior of a hydrogen extractive membrane bioreactor (HEMB) during mixed culture acidogenic fermentation Juan E. Ramı´rez-Morales a,*, Estela Tapia-Venegas a, Jose Luis Campos b, Gonzalo Ruiz-Filippi a Escuela de Ingenierı´a Bioquı´mica, Pontificia Universidad Catolica de Valparaı´so, Av Brasil 2085, 234-0950, Valparaıso, Chile b n ~ ez, Avda Padre Hurtado 750, Vin ~ a del Mar, Chile Faculty of Engineering and Science, Universidad Adolfo Iba a
highlights A
process
integrating
graphical abstract gas
separation-membranes and Bio-H2 production is presented. Membrane module was able to extract and partially separate H2 and CO2 generated. H2 partial pressure was reduced 11% in the bioreactor-headspace with a membrane. Decreasing H2 partial pressure on the mixed culture had a positive effect on H2 yield. An extractive membrane bioreactor can generate a H2 rich stream of 68% (v/v).
article info
abstract
Article history:
Fermentative hydrogen production requires a continuous products-removal and effective
Received 15 May 2019
upgrading steps to improve its general performance. Therefore, implementation of new
Received in revised form
technologies capable of achieving both requirements is essential. We present the opera-
14 July 2019
tional behavior of a new process concept based on integration of membranes for gas
Accepted 10 August 2019
separation and fermentation technology. This process, which we term as hydrogen extractive membrane bioreactor consists of coupling two dense polymeric membranes to a hydrogen producing culture. The process automatization of this system was essential to
Keywords:
maintain the proper operational pressures in the membrane module and in the bioreactor-
Biohydrogen separation
gas-phase. This system was able to extract and partially separate the hydrogen and carbon
Fermentative hydrogen upgrading
dioxide generated. The hydrogen partial pressure was reduced from 55.5 to 49 KPa, which
Hydrogen partial pressure
means
an
increase
of
hydrogen
yield
of
16.3%
* Corresponding author. E-mail address: [email protected] (J.E. Ramı´rez-Morales). https://doi.org/10.1016/j.ijhydene.2019.08.077 0360-3199/© 2019 Hydrogen Energy Publications LLC. Published by Elsevier Ltd. All rights reserved.
(1.1e1.28
mol-H2/mol-glucose).
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Polymeric membrane
Simultaneously, the implemented system generated a final hydrogen stream 13% (v/v)
Gas extractive fermentation
more concentrated than a conventional process. © 2019 Hydrogen Energy Publications LLC. Published by Elsevier Ltd. All rights reserved.
Introduction Fermentative hydrogen from mixed cultures has become a promising alternative for bioenergy generation using organic wastes [1]. In addition, its by-products can be considered as potential microbial metabolites within a biorefinery framework [2]. Although fermentative hydrogen achieves higher experimental hydrogen yields than other biological production processes, there are still challenges to improve its performance and efficiency [3]. Moreover, effective integration of strategies to increase simultaneously the yields of products and optimize their recovery and purity are still in an early stage of applied research [4]. Many factors influence the complex process of fermentative hydrogen production, such as type of substrate, inoculum, pH, temperature, reactor design, hydraulic retention time (HRT), substrate concentration, organic loading rate (OLR) and hydrogen (H2) partial pressure. Among them, the later seems to be one of the most important factor [5e9]. To alleviate the negative effect of H2 partial pressure, various strategies have been adopted: vacuum application and increasing the stirring rate [10], improve gas transfer from the liquid phase to the gas phase by changing reactor configuration [11], lowering the total pressure in the headspace [12], increasing surface area changing the size of the reactor [13] and gas sparging/flushing with different gases (N2, CO2, CH4 or internal biogas) [5,9,12,14e17]. In the past years, there has been some efforts for trying to establish a consensus about the positive effects of decreasing the H2 partial pressure on fermentative mixed cultures. For continuous cultures, where a stable system condition has been established, gas sparging/flushing has shown to improve the process performance. The general assumptions for explaining the increase of the hydrogen yields during a reduction in the H2 partial pressure are based on the thermodynamics of the biological reactions responsible for generation and consumption of H2 (lactate hydrogenase, NADH hydrogenase and homoacetogenesis reactions) [9] or the selection of active hydrogen bacteria by using CO2, which has inhibitory effect on other non-desirable microorganisms like acetogens [15]. Other authors have mentioned that the dissolved hydrogen concentration in the liquid media is much higher than the necessary limit to fall into the (H2) partial pressure regulatory zone due to critical supersaturation phenomena, and it seems that impractically high sparging rates would be needed to overcome that barrier [18,19]. Although continuous H2 extraction by gas sparging/flushing has shown to improve the process performance, from a practical perspective and full-scale implementation, this strategy would be energy intensive, due to the need for gas
compression and the high dilution of the final gas generated. Alternatively, membrane technology stands out as robust approach to extract continuously hydrogen and deal with the H2 partial pressure effect. Furthermore, using this technology, it would be possible to obtain a rich hydrogen stream feasible for direct application in fuel cell systems [20]. In recent years, membrane separation technology has grown rapidly, promoting the innovation in process intensification, purification and product recovery. It provides lower costs and power requirements, it is easily integrated to other processes, and thus, it is able to play a key role in biorefining and bioenergy production [21]. Nowadays, palladium (Pd) and silica based membranes systems are being considered as good candidates to separate the H2/CO2 gas mixture produced in thermo-catalytic processes carried out at high temperatures (200e700 C) [3,22]. However, such temperatures are not characteristic in biological systems for hydrogen production and the membranes to be used must be different. Alternatively, polymeric membranes with operating temperatures typically less than 100 C would be more appropriate. Most studies on biological hydrogen separation have been carried out using nonporous, polymeric and ionic liquid based membranes with synthetic mixtures, which simulate biohydrogen mixtures [23]. Investigations have focused on membrane contactors with moving liquid carriers [24,25], dense polyimide based membranes [26,27], supported ionic liquid membranes (SILMs) [28] and integrated systems of porous/non porous dense membranes [29,30]. However, in most of the cases the studies did not couple the effect of the gas extraction on the culture performance and the lab scale system setup had practical limitations to be implemented in continuous mode. Regarding the efforts for decreasing the H2 partial pressure using extractive membranes, some studies have evaluated the possibilities of gas extraction from the liquid and gas phase of the reactor [31,32]. Despite the potential of such submerged membranes to extract the dissolved gases directly from the liquid, they also have problems of biofouling and rapid deterioration over time. On the other hand, implementation of membrane gas extraction setups in contact with the gas phase could avoid some of these issues. However, they also would need a proper automatic control operation, which in many cases represents a technical challenge in bench-scale systems. For coupling the bioreactor to a membrane system, previous studies on membrane characterization are critical in order to find suitable operational parameters like the transmembrane pressure and its effect on the permeability, selectivity and recovery (stage-cut). We implemented the system called “hydrogen extractive membrane bioreactor (HEMB)”, introduced for first time in our
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previous study where a gas membrane module was selected and characterized for simultaneous extraction and separation of fermentative hydrogen [33]. Since its introduction, some approaches have tried to implement similar concepts using the same type of membranes for hydrogen upgrading or for returning an enriched CO2 stream back to the reactor [4,29]. However, these studies did not implemented the required automatic control for the integration of the continuous biological process with the membrane systems and there was not a clear effort to continuously stablish lower H2 partial pressures. For this particular integrated concept, process automatization is essential to avoid human assistance when maintaining simultaneously a proper transmembrane and atmospheric pressure in the membrane module and in the gas phase of the bioreactor, respectively. Our system contributes to stablish a simple and closed loop control system, in which it is possible to evaluate the positive effect of decreasing the H2 partial pressure on the mixed culture performance in a bench scale continuous stirred reactor tank reactor (CSTR). In this study, the behavior of the fermentative process is evaluated in terms of H2 productivity and fermentative metabolite production under different operational periods when the continuous hydrogen extraction led to stablish a lower H2 partial pressure inside the reactor. In addition, the possibility of obtaining a H2 rich stream at the outlet of the system using a second membrane module as additional upgrading step is also addressed.
Materials and methods Inoculum and medium composition Granular anaerobic sludge from a full-scale UASB reactor treating tobacco wastewater was used as inoculum. The sludge granules were washed twice with tap water and settled at room temperature. To prevent clogging of the tubing, the granules were sieved through a 0.5 mm mesh. To establish a mixed culture composed of strict anaerobic and facultative anaerobic bacteria, the sludge was not pre-treated thermally according to Tapia-Venegas et al., [34]. The CSTR medium composition was based on a synthetic glucose wastewater and adapted from Tapia-Venegas et al. [11]. The media consisted of 10 g L-1 of glucose and the following nutrients (mg L-1): 1000 NH4Cl, 250 KH2PO4, 100 MgSO4$7H2O, 10 NaCl, 10 NaMoO4$2H2O, 10 CaCl2$2H2O, 9.4 MnSO4$H2O and 2.78 FeCl2. All components were dissolved in tap water and the final feed solution was refrigerated at 4 C to reduce the growth of undesirable microorganisms.
Continuous fermentative hydrogen production A 2.7 L glass-made CSTR with a working volume of 2.0 L was used and started up with 200 mL of inoculum. The agitation speed and hydraulic retention time (HRT) were set up at 100 rpm and 12 h, respectively. The mixed culture was maintained at 37 C and the pH was controlled at 5.5 (as set point) by adding NaOH (2 N) solution. The liquid level was controlled using a capacitive level switch (LP15 Series, Flowline®) and peristaltic pumps for influent feeding and effluent
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draw off were employed (Masterflex, Cole-Parmer, USA). The operational conditions for the CSTR were selected according to the maximum volumetric hydrogen productivity and yield obtained in a previous study [11]. Before the membrane coupling, the mixed fermentation was run until a steady state with respect to the hydrogen production and glucose consumption was reached. Simply, it was assumed that steady state occurred when coefficient of variation (calculated as standard deviation divided by the average) for hydrogen production rate and yield was less than 15%.
Continuous bioreactor-membrane integrated system The membranes used consisted of two lab-scale membrane modules commercially available (Permselect PDMS-XA 2500, MedArray Inc., USA). The same membrane module responsible for extracting and separating partially the biohydrogen generated was characterized in a previous study [33]. Information of the membrane module, such as structural characteristics, CO2 and H2 permabilities and CO2/H2 separation factor are available in the research paper. The membrane used as a second step of biohydrogen upgrading consisted of the same material as the above mentioned but with an area of 10 cm2 and 30 hollow fibers. The continuous experimental set-up is schematically shown in Fig. 1. Membrane (M1) was coupled to the CSTR reactor (R) once the hydrogen production of the mixed culture fermentation reached a steady state. The system was composed of peristaltic pumps, pressure sensors and traps in the different operational lines. The permeate gas stream coming from the membrane (M1) was return to the reactor headspace since it was enriched in CO2 [33]. The membrane (M1) was continuously fed with a peristaltic pump (B1). A cold trap (C) was located in this stream to condensate water vapor, avoiding the water layer formation on the membrane surface (resistance to mass transfer). A second peristaltic pump (B2) acted as a controlled valve, which, by means the peristaltic pump (B1), maintained the headspace reactor (permeate stream) and the feed stream of the membrane at atmospheric pressure (~101 kPa) and 180 kPa, respectively. These operational pressures were selected according to the previous characterization of the membrane modules. Taking into account that the H2 production rate can vary over time due to inherent fluctuations in the biological process, a control strategy was implemented to achieve a stable pressure in both streams. The control system was performed combining a data acquisition system (DAQ, National Instruments Co., USA), board mount gauge pressure sensors, a microcontroller board (Arduino), Labview 8.5 software (National Instruments Co., USA) and a peristaltic pump (Thermo Scientific FH15, UK). The peristaltic pump revolutions increased or decreased according to set pressure ranges based on discrete control steps. To avoid an erratic control, a moving average filter was implemented to counter noisy pressure data signal. In order to have a higher hydrogen composition and remove toxic compounds for direct gas application on a labscale fuel cell (FC), a second membrane (M2) and a H2S trap (S) based on iron hydroxide-based adsorbent were located after the peristaltic pump (B2). A 3-way valve led the continuous feeding of the membrane (M2) and H2 fuel cell. The
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Fig. 1 e Scheme (A) and picture (B) of the continuous experimental set-up (H2 extractive membrane bioreactor, HEMB). The final gas stream generated was applied in a lab-scale fuel cell to produce electricity as a proof of concept.
corresponding area (10 cm2) of the membrane (M2) was chosen to achieve a pressure drop of 80 kPa, taken into account the gas flow generated by the peristaltic pump (B2) and a stage-cut about 0.5. The drop pressure of 80 kPa were maintained as an adequate condition to separate the H2/CO2 gas
Table 1 e Features of different fermentative process periods studied. Periods of fermentative process P1 P2 P3
P4
Membrane configuration
Operational period days
Without membrane CSTR þ membrane system (M1) CSTR þ membrane system (M1) with an initial oxygen input disturbance CSTR þ membrane system (M1 and M2)
0 to 14 14 to 21 21 to 35
35 to 45
mixture generated with help of a needle valve [33]. The outlet gas flow of the system was daily measured by a water displacement system (W) adapted with an electronic balance. The fermentative process operation with or without membrane were divided into four periods P1, P2, P3 and P4. P1 corresponded to the period of CSTR operation without membrane, while in P2, P3 and P4 the system was running with the coupled membrane(s) (CSTR þ membrane system). P2 and P4 periods were similar and P3 had an initial oxygen input disturbance because an operation drawback (see Table 1). The peristaltic pump (B1) tubing was partially broken, which generated a leak and induced a vacuum, entering air into the head space of the reactor. Despite this drawback, the tubing was replaced, the operation was recovered and the process continued. The reactor operation was carried out for 44 days. Before coupling the extractive membrane (M1), the reactor was operated in batch mode for 24 h and then switched to continuous mode for enabling the activation of the microorganisms present in the initial inoculum.
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Analytical methods
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main liquid product followed by acetate and butyrate, both at similar concentrations (Fig. 2B). A similar behavior with ethanol and butyric acid-type fermentations has been found in different studies, where the initial inoculum was not pretreated with a heat shock (like in the current work) but it was aerated previously to the inoculation [35,36]. The membrane module was coupled to the gas-phase of the reactor on 14th day. The effect of the selective hydrogen extraction was observed after 72 h. The composition of hydrogen decreased from 55 ± 3.0 to 49.76 ± 0.40% v/v (Fig. 2C; P2). As the glucose consumption rate remained constant (Table 2), the increase of gas flow was the responsible for an increase on hydrogen yield from 1.1 (P1) to 1.28 mol-H2/molglucose (P2) (Fig. 2D). This implied a positive effect (yield improvement of 16.3%) due to the extractive membrane coupling on the process. This increment was also related to the change of by-products, where acetate and butyrate remained as the main liquid products of the fermentation and ethanol decreased (Fig. 2B). In the literature, this decrease in hydrogen production by increasing the ethanol production is non-obvious, in some cases with glucose as a substrate, the increase of ethanol has a direct relationship with the increases of hydrogen production [37,38]. The biomass concentration was also affected, decreasing from 0.96 ± 0.12 to 0.67 ± 0.16 g VSS/l (Fig. 2D). These average values where obtained from a short operation time where the system run without any disturbances. However, during the 21st day an operation drawback occurred. The peristaltic pump (B1) tubing broke, which generated a leak, induced a vacuum and air entered into the head space of the reactor. Despite this drawback, the tubing was replaced and the H2 extraction process continued. This disturbance generated a transitional operational stage that caused a decrease on productivity and yield (P3). During 9 days, the hydrogen concentration dropped to 42.15 ± 6.15% v/v and again the main fermentation byproduct was ethanol (Fig. 2B). Although the process performance was affected, the culture was slowly recovering and the hydrogen concentration reached 50.63 ± 2.35% v/v at the period defined as P4. Until this point, biomass and hydrogen yield were similar to the operational performance of the period P1 (Table 2). Mass balances of the corresponding periods counted for 80% of the inlet COD, which implies that
Gas sample compositions (hydrogen, nitrogen, methane, and carbon dioxide) were analyzed by injecting samples into a gas chromatograph (PerkinElmer Clarus 500) equipped with a Haysep Q 80/100 13’x 1/800 OD column (Alltech Co., USA) and a thermal conductivity detector (TCD). Injector and detector temperatures were 80 and 120 C, respectively. The initial temperature of the column was 30 C, followed with a ramp up to 80 C. The helium carrier gas flow rate was 15 ml/min. The hydrogen composition in the biogas (%H2) can be directly related to the hydrogen partial pressure. However, partial pressure of the gas component (Ppi) can be calculated as: Ppi ¼ PT Xi where PT is the total absolute pressure of the gas and Xi is the volume fraction of the gas component. Volatile fatty acids (VFA) were analyzed with a gas chromatograph (Shimadzu, Kyoto, Japan) fitted with a FID detector and a ID GP 60/80 Carbopack C/0,3% Carbowax 20 M/0,1% H3PO4 packaged column (Sigma Aldrich, St Louis, MO, US). During the ethanol measurements a gas chromatograph (PerkinElmer Clarus 500) equipped with a wide bore, semicapillary Equity-1 column (Sigma-Aldrich, St. Louis, MO, USA) was used. Volatile suspended solids (VSS) and glucose concentration were measured according to Tapia-Venegas et al. [11].
Results and discussion Operational performance of the HEMB Average values of operational parameters for the periods considered in steady state P1, P2 and P4 are presented in Table 2. P3 was assumed as a stage of transition. During period P1 a stable hydrogen production process was established after a start-up operation of 5 days. From this point, it was assumed a stable production until the 15th day, corresponding to a yield of 1.1 mol-H2/mol-glucose (this assumption was based on the coefficient of variation, as previously mentioned). During this period (P1), the fermentation was dominated by ethanol as the
Table 2 e Operational parameters during the fermentative process, before and after coupling the membrane M1 (averages). Operational parameter
Glucose consumption Biomass Hydrogen composition CO2 composition Methane composition Ethanol Total volatile fatty acids (VFAs) Yield Volumetric production rate COD balance
Unit
% g VSS/l % v/v % v/v % v/v mM mM mol-H2/mol-glu mmol-H2/l h %
Operational period P1
P2
P3
P4
99,6 ± 0,04 0.96 ± 0.12 55 ± 3.0 46.38 ± 2.36a ND 25.08 ± 3.31 24.44 ± 5.01 1.1 ± 0.1 4.97 ± 0.55 76.07 ± 14.43
99.65 ± 0.02 0.67 ± 0.16 49.76 ± 0.40 52.33 ± 1.00a 1.32 ± 0.95 11.13 ± 6.70 44.08 ± 5.48 1.28 ± 0.15 5.42 ± 0.80 77.33 ± 9.81
99,59 ± 0.14 1.1 ± 0.10 42.15 ± 6.15 57.47 ± 1.53 1.53 ± 0.31 28.34 ± 3.79 35.54 ± 4.08 0.85 ± 0.17 3.99 ± 0.61 78.01 ± 5.02
99.64 ± 0,02 0.91 ± 0.14 50.63 ± 2.35 49.48 ± 2.77 1.86 ± 0.57 20.73 ± 2.51 43.27 ± 3.47 1.08 ± 0.11 5.18 ± 0.30 82.55 ± 4.88
ND: not detected. a The carbon dioxide content of the periods P1 and P2 were examined for statistical significance. When comparing the two periods, the p-value was 0.042 and the result was significant at p < 0.05 (one-way ANOVA).
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Fig. 2 e Operational parameters before (CSTR) and after coupling the extractive membrane (HEMB). The fermentation time was carried out for 44 days, where continuous signals of pH and pressure were captured (A). It is also shown the concentration of different by-products (B), the biogas composition (C), hydrogen yield, volumetric production rate and biomass concentration (D). Dotted vertical lines mark the time of coupling of the extractive membrane. Grey horizontal lines mark steady states for the different periods.
other metabolites missed in the account. The fact that the recovered COD is similar for all the periods, indicates that ethanol or other volatile compounds did not extracted by the membrane process. The recovery period of the culture (P4) shown in Fig. 2D could be explained from the quality characteristics of the inoculum used in the start-up stage. The microbiological diversity of this inoculum was reported in the S0 period of Tapia et al. [20], (Prevotella 35,3%; Veillonellaceae 32%; Clostridium sp 7%; Acetobacter 16,8%, Enterobacteriaceae 1,7%). A disturbance related to an air inlet into the reactor can be addressed positively if the inoculum possesses facultative bacteria, which is responsible for consuming oxygen such as Acetobacter and Enterobacteriaceae family [38]. The inoculum in this case was not subjected to heat shock, which eliminates a high amount of facultative bacteria (i.e. those who cannot form spores). Some studies ensure that using facultative anaerobic bacteria contained in waste activated sludge (WAS) improved the fermentation robustness due to their high growth rate and capability to rapidly recover from an accidental oxygen intrusion [38,39]. Therefore, a culture composed by a consortium from facultative and strict anaerobes could develop a stable and robust process performance. The relationship of the biomass and ethanol concentration with respect to the hydrogen yield is shown in Fig. 3. This data correspond to the operational periods where the reactor operated adequately (P1, P2 and P4). The tendency responds to a decreasing behavior, which was expected as the culture
Fig. 3 e Biomass and ethanol concentrations related to the hydrogen yield during the operational periods P1, P2 and P4. The arrows show the data corresponding to the days of operation of the extractive membrane during P2. generally present higher yields when a butyrate production is preferred. A similar behavior was found by Ref. [40], where ethanol and hydrogen yield correlated negatively during an
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operation of a CSTR. The highest hydrogen yields in Fig. 3 fit to the lowest values of biomass and ethanol concentrations, which in turn correspond to the operational data for the period P2 (arrows in Fig. 3). During these days (6 hydraulic retention times) the membrane module was extracting selectively hydrogen without any operational drawback. It is interesting to note that low amounts of biomass are directly related to the best hydrogen yields when the membrane was coupled. In this case, more electrons coming from the substrate are being disposed as hydrogen, acetate and butyrate instead of biomass and ethanol [12]. This observation could be also related to a higher capacity of the mixed culture to maintain a suitable tendency for fermentative hydrogen production. The effect of CO2 composition can be an influencing factor too. The composition of CO2 increased from 46.38 ± 2.36 to 52.33 ± 1.00% (v/v) for the periods P1 and P2, respectively. The statistical significance was examined performing a one-way ANOVA followed by the least significant difference test (LSD) at a level of p < 0.05, resulting in a p value of 0.04. A CO2 increase in the gas phase had a positive effect on the hydrogen active bacteria, as it was found by Devi et al. [14], and Kim et al., [15]. They reported that CO2 had an inhibitory effect on non-hydrogen active microorganisms (i.e. competitive acetogens and lactic acid bacteria). In this manner, the separated and returned CO2 could have a positive effect on the hydrogen producing microflora and a negative effect on competitive ones. Future research studies focus on detailed analysis of the corresponding bacterial community would evidence enrichment of specific hydrogen producing populations as a result of the hydrogen membrane extraction. When comparing the improvement obtained in the hydrogen yield (increase in 16.3% during P2) with other studies using sparging/flushing, there is a considerable difference. They obtained higher improvements as they dilute the hydrogen content between 7 and 10 times more [15,41]. However, to the best of our knowledge, the current study set a precedent as the first continuous and self-controlled hydrogen-extractive system implemented in the phase gas. The process based on integration of gas membrane separation and fermentation technology could be improved using better membranes with higher selectivity [25,42], in order to reach lower concentrations of hydrogen in the gas-phase and get a richer hydrogen stream in the outlet. In addition, upcoming studies must extend the operation time and carry out analysis of other metabolic products like formate, lactate and ferredoxin, as suggested also by other authors [19].
Continuous upgrading of fermentative hydrogen Fig. 4 shows the hydrogen composition in the retentate of the extractive membrane (M1) and the second one (M2) coupled in series. Hydrogen compositions about 61% (v/v) were obtained in the retentate of M1 during the period P4, and it was possible to increase it using the membrane M2 up to 68% (v/v). Higher compositions could have been obtained if the system had produced hydrogen compositions of 71% (v/v) as it occurred during P2. The automatic control implemented for maintaining the set pressures of the reactor and membrane M1 was avoided this time and only a manual control of the pressure
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Fig. 4 e Hydrogen composition in the retentate stream of two polymeric membranes (M1 and M2) coupled to system. A fuel cell was connected to the retentate stream of the second membrane (M2) to produce electricity (data not shown).
was carried out using a common needle valve. However, as experienced by the operator, a constant human monitoring of the system was necessary, which highlight the importance of the implementation of automated control when the system becomes more complex. Future improvements could facilitate the total automated control of a simultaneous extraction and upgrading hydrogen of a process based on membrane module cascades. In addition, it could be interesting to study the different configurations with other membrane materials having a higher selectivity, in order to reach upper hydrogen compositions with a limited amount of equipment.
Comparison with other studies and perspectives Different systems have been studied to separate bio-hydrogen using membrane contactors with flat sheets and hollow fiber module configurations (Table 3). These approaches have been focused on membrane systems that use absorptiondesorption processes in dense polymeric membranes and separation of fermentative hydrogen using porous and dense materials. In some cases, synthetic mixtures have been used to simulate a gaseous stream produced in the biological process and others have coupled membrane modules to bioprocesses but with a manual or human assisted control. The current study stands out as the first implementation of an automated process for coupling a hydrogen extractive membrane into a continuous biological process. The automatization of membranes coupled to biological systems operated in continuous mode is critical, especially when the system is prone to suffer inherent and external disturbances, like is the case of a hydrogen fermentative process.
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Table 3 e Studies on upgrading bio-hydrogen (fermentative hydrogen in some cases) using different membrane technologies. Gas mixture/biological source
Feed composition (v/v)
Mixed culture Different biological processes Thermococcuslitoralis
67.8% H2 32.1% CO2 H2/CO2/CH4 ~40/35/ 25% H2/CO2/N2 (23% H2)
Synthetic
55% H2/45% CO2
Mixed culture
Mixed culture
51.3 v/v H2, 47.0 v/v CO2, 1.7 v/v undefined 55e58% H2 in biogas
Mixed culture
55% H2/45% CO2
Polymeric membranes/ Modules Dense (PDMS)/Hollow fiber Contactor (PVTMS)/flat sheets Porous (HDPE)þdense (PES/PI)/ Hollow fiber Dense (polyimide)/Hollow fiber
Dense membrane (PDMS)
Nonporous Polydimethylsiloxane (PDMS) membrane modules (PDMSXA-10) Two Dense (PDMS)/Hollow fiber
Liang et al. [31], coupled a silicone rubber membrane into the liquid-phase of a batch culture. They reported that the membrane reduced the biogas partial pressure and improved the hydrogen production rate and hydrogen yield by 10% and 15%, respectively. However, this mode of operation did not permit a continuous extraction of hydrogen from the culture and therefore the effect of the reduced partial pressure of the product gases was not evidenced for a prolonged period. lafi-bako et al. [30], coupled a fermentative hydrogen proBe cess with two polymeric membranes modules. Because the reactor operated in batch mode, the integrated system had to release, compress and store the biogas mixture (H2, CO2 and N2 from sparging) produced in an intermittent way. The final increase in hydrogen composition ranged from 23 up to 73% (v/v) by an integration of a polyethersulfone-polyimide (PESPI) and highly dense polyethylene (HDPE) membranes. Recently, Bakonyi et al. [29] installed a Permselect® (PDMS) gas separation membrane to an anaerobic membrane bioreactor. They used the same membrane module (M2) as it was operated in the current work. They tested its ability to separate hydrogen from the raw fermentation gaseous mixture that was accumulated in a gas bag (non-continuous process). They obtained a final hydrogen composition of 67.3% (v/v), very close to the obtained in this study. The last published approach was made by Bakonyi et al., [4]. They implemented a concept similar to the hydrogen extractive membrane bioreactor (HEMB), which was introduced for first time in our previous study when the same type of membrane was characterized [33]. However, they did an internal recirculation of the membrane streams, with no clear continuous gaseous extraction. They reported changes in the hydrogen productivity comparing different operational periods when CO2 and H2 rich streams were returned to the reactor. However, their microbial community analysis did not show a remarkable difference between periods. They suggested that certain constructional upgrades like the pressure control of the gas streams instead of using manual backpressure regulators would drive the system towards better feasibility. These recommendations were kindly implemented in our setup and the
Results obtained Yield increase (15%) Composition increase H2 (90%v/v), CO2 (99%v/v) CH4 (95%v/v) Composition increase (73% v/v H2)
Reference [31] [24] [30]
65% v/v H2/35%v/v H2/CO2, selectivity of 1.56, recovery factor of 0.72 Up to 67.3 v/v H2
[27]
59e60% H2 in biogas
[4]
H2 enriched biogas (68% H2/32% CO2) Yield improvement of 16.3%
This study
[29]
system was able to extract hydrogen in a continuous and automated mode. Improvements on gas membrane technology (i. e. new materials for higher selectivity to separate the mixture H2/ CO2) could drive the simultaneous extraction and the upgrading/recovery steps of a feasible system. To design an effective purification system based on membrane technology, it is also important to consider the negative impacts of tracelevel substances present in the raw gas mixture on the membrane behavior (e.g. H2S) [43]. Implementation and evaluation of the performance of chemical traps could lead to reach higher performances in the recovery and upgrading steps to ensure the requirements of a direct application of the gas (i.e. fuel cells systems). Thereby, it could be possible to accomplish a balance between recovery and purity of the hydrogen produced by the biological process. Finally, the extractive system should operate under the typical conditions required for the fermentation (adequate temperature and pressure), ensuring a non-intensive energy process.
Conclusion A hydrogen extractive membrane bioreactor (HEMB) setup was implemented. The system contributed to stablish a simple controlled process where we could evaluate the positive effect of decreasing the H2 partial pressure on the mixed culture performance in a bench scale continuous stirred reactor tank reactor (CSTR). The process automatization of this particular system was essential to maintain the proper operational pressures in the membrane module and in the gas phase of the bioreactor during a closed loop control system. The continuous and automated process increased the hydrogen yield in 16.3% and simultaneously generated a hydrogen rich stream of 68% v/v. Improvements on these parameters can be achieved upgrading the system with the new developments on membrane materials and cascade module configurations, driving the feasibility of this concept at higher scales.
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Acknowledgements The authors would like to acknowledge financial support from FONDECYT 3160219 project. This work is dedicated to the memory of our well esteemed and wonderful colleague Prof. Gonzalo Ruiz-Filippi who recently passed away.
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