Recovery of succinic acid from fermentation broth by forward osmosis-assisted crystallization process

Journal of Membrane Science 583 (2019) 139–151

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Recovery of succinic acid from fermentation broth by forward osmosisassisted crystallization process

T

Jeng Yih Lawa,b,∗∗, Abdul Wahab Mohammada,∗, Zhao Kang Teea, Nadiah Khairul Zamana, Jamaliah Md Jahima, Jude Santanaraja, Mohd Shaiful Sajaba a

Department of Chemical and Process Engineering, Faculty of Engineering and Built Environment, Universiti Kebangsaan Malaysia, 43600 UKM Bangi, Selangor, Malaysia Process Engineering Technology Section, Universiti Kuala Lumpur, Malaysian Institute of Chemical & Bioengineering Technology, Lot 1988, Kawasan Perindustrian Bandar Vendor, Taboh Naning, 78000 Alor Gajah, Melaka, Malaysia

b

ARTICLE INFO

ABSTRACT

Keywords: Forward osmosis Succinic acid Fermentation broth Activated carbon Crystallization

In this study, osmotically driven forward osmosis (FO) was employed prior to crystallization process in the downstream recovery of bio-based succinic acid. The fermentation broth containing succinic acid was initially pretreated using activated carbon. Powdered activated carbon (PAC) showed its effectiveness for glucose, formic acid, and color removal while succinic acid concentration remained unaffected. The untreated and treated fermentation broths were then concentrated using the FO process. FO exhibited a remarkable enhancement of concentration factor (CF) by 3.9-fold for the treated broth, thus resulting in a final succinic acid concentration of 111.26 g/L. By contrast, higher flux loss and lower CF were observed for untreated broth, mainly due to the adverse effect of severe membrane fouling and cake layer formation. Succinic acid crystals were then successfully recovered from the FO-concentrated broth in the final crystallization step. The purity and yield of succinic acid crystals were 90.52% and 67.09%, respectively for treated broth. This work demonstrated the development of a feasible FO-crystallization process for the downstream recovery of bio-based succinic acid. The findings have important implications for practical applications of FO technology in the bioprocess industries.

1. Introduction Succinic acid, a four-carbon dicarboxylic acid, is one of the most important commodities which serves as precursor or starting material for many industrially valuable products [1–3]. The multiple applications and industrial potential of high-value succinic acid have been widely recognized. Conventionally, succinic acid is synthesized through chemical process using liquefied petroleum gas or petroleum oil as a starting material [2]. Nonetheless, there has been growing interest in the production of “green” succinic acid from renewable resources. Extensive research efforts have been made for developing a sustainable fermentation-based route through appropriate bacteria species selection. Among the various strains, Actinobacillus succinogenes and Actinobacillus succiniproducens have been considered as important potential producers for large scale production of succinic acid [4]. It is noteworthy that several companies have recently commercialized the biobased succinic acid production including Bioamber (2014), Myriant (2013), Reverdia (2011), and Succinity (2013) [5,6].

Downstream recovery of succinic acid is currently of key interest in the biorefinery approach for succinic acid production. Various separation and recovery technologies have been proposed in the past decade. The recovery cost generally accounts for 50–80% of the overall succinic acid production cost [7,8]. In view of that, downstream processes that are technically feasible and economically viable are highly desirable. To date, the recovery of bio-based succinic acid remains challenging. Fermentation broth typically contains low concentration of succinic acid. Additionally, the presence of other carboxylic acids (e.g. acetic acid, formic acid) as byproducts in the broth may affect the purity of final product [9,10]. In this regard, a number of studies exploring the downstream processing of succinic acid production have been reported. One of the classical methods to recover succinate from fermentation broth is calcium precipitation [11,12]. Ca(OH)2 or CaCO3 was added to precipitate succinate and simultaneously neutralize the broth. Calcium succinate was then filtered from the broth and treated with concentrated sulfuric acid to release free succinic acid. This method, however, may not be economically attractive due to the large

Corresponding author. Corresponding author. Department of Chemical and Process Engineering, Faculty of Engineering and Built Environment, Universiti Kebangsaan Malaysia, 43600 UKM Bangi, Selangor, Malaysia. E-mail addresses: [email protected] (J.Y. Law), [email protected] (A.W. Mohammad). ∗

∗∗

https://doi.org/10.1016/j.memsci.2019.04.036 Received 25 July 2018; Received in revised form 17 January 2019; Accepted 17 April 2019 Available online 22 April 2019 0376-7388/ © 2019 Elsevier B.V. All rights reserved.

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constitutive consumption of Ca(OH)2/CaCO3 [11]. In addition, it produced large and equal amounts of solids and slurry waste product (e.g. CaSO4) which have no commercial value, thus requiring further treatment and disposal [13]. Crystallization is one of the promising methods for the recovery of organic acids from fermentation broths. Luque et al. [7] compared the performances of modified calcium precipitation coupling crystallization and direct crystallization for succinic acid recovery. Volatile byproduct acids including acetic, formic, and pyruvic acids in the broths were removed via vacuum distillation prior to crystallization. Compared to the modified calcium precipitation method, higher succinic acid crystal purity (90–97%) and yield (61–75%) were obtained through direct crystallization method for simulated broths. However, a significant reduction of purity (45%) and yield (28%) were observed when succinic acid was recovered from actual fermentation broths. Li et al. [14] proposed one-step recovery of succinic acid by direct crystallization. When the pH and temperature of the fermentation broth were adjusted to 2.0 and 4 °C, respectively, the solubility of the succinic acid was substantially decreased. Under such operating conditions, succinic acid crystals could be formed while other carboxylic acids remained miscible in the broth. The final yield and purity were 70% and 90%, respectively. Membrane-based process which is relatively environmentally benign, has received increasing attention in recent years. Recently, Sosa [10] proposed a new three-step membrane-based process to recover and purify succinic acid from simulated fermentation broths. Electrodialysis (ED) was used to concentrate and partially separate succinate ion under the driving force of an electrical potential difference. However, the economic feasibility of ED remains questionable due to high electricity or energy consumption [11,15]. To release a free succinic acid, the metallic cations in the succinate salts was replaced by H+ using Donnan dialysis installed with a cation-exchange membrane. This method also requires further purification steps to recover the succinic acid from the dilute fermentation broth. In recent work, Nguyen and Boontawan [16] reported an interesting multi-stage process integrating microfiltration (MF), nanofiltration (NF) and crystallization for succinic acid recovery. MF as the pretreatment step was mainly used for the rejection of the bacterial cells. The clarified broth containing numerous impurities was then treated by NF. The decolorization effect of NF permeate which corresponding to a 95.7% color removal could improve the quality of the final crystal product. The final purity of the succinic acid crystal reached 99.18%. However, the proposed method has some drawbacks or limitations. For instance, the water consumption was extremely high during diananofiltration mode. Furthermore, the use of thermal-driven evaporation for the concentration of succinic acid could result in high energy consumption [16]. The downstream process for organic acid recovery is usually associated with energy intensive concentration or dewatering processes (e.g. vacuum distillation, evaporation, and reverse osmosis (RO)) [10,16–19]. Conventional thermal-driven processes were reported to cause quality degradation problems such as loss of nutritious components and volatile agents, in addition to being uneconomical [20,21]. One of the possible methods to overcome these issues is by using forward osmosis (FO). FO is an attractive membrane technique which utilizes the natural phenomenon of osmosis. The water permeation from feed to draw solution (DS) across a semi-permeable membrane is a spontaneous process driven by osmotic pressure gradient. Several notable advantages have been highlighted including high salt and organic compounds rejection, high quality water recovery, ambient operating conditions, low energy consumption, and low fouling propensity which may prolong the membrane's lifespan [21–25]. Previously, the dewatering of organic acid solution using FO was proposed by Cho et al. [17]. Ruprakobkit et al. [26] developed a dynamic process model of FO targeting low concentration (10 mM) carboxylic acid (acetic acid, lactic acid, butyric acid and valeric acid) as feed solution. More recently, Law et al. [27] investigated the performance of FO for concentrating

succinic acid using multiple-solute DS, and observed that succinic acid in salt form could be effectively rejected by the FO membrane. Application of FO technology for the enrichment or concentration of succinic acid broth is still in its infancy and deserves further investigation. In FO process, DS plays a substantial role as the main source of driving force. The general characteristics of selecting a suitable draw solute include osmotic pressure, molecular weight, solubility, viscosity/ diffusivity, stability, toxicity, and DS concentration [22,28]. Numerous studies have reported that water flux could be enhanced at elevated DS concentration attributed to the increase in osmotic pressure driving force [29,30]. However, high DS concentration could adversely lead to non-linear water flux increment and enhanced reverse solute flux [31]. High DS viscosity and low diffusivity could contribute to a more pronounced effect of concentration polarization, thus leading to a reduction of water flux [32]. It is crucially important to ensure that the draw solute is chemically stable and non-toxic [28]. These criteria have posed great challenges in selecting a suitable draw solute. In recent years, the number of studies on novel draw solute development has increased significantly. Among the potential compounds include organic and inorganic salts, neutral compounds, magnetic nanoparticles, thermally responsive hydrogels, switchable polarity solvents and volatile compounds [22,28,33,34]. Additionally, a variety of recovery methods such as thermal separation, membrane separation (RO, NF, ED, membrane distillation), precipitation, stimuli–response, and combined processes have also been proposed for the regeneration of diluted DS [35]. Efficient recovery of bio-based succinic acid can be realized via introduction of new separation technologies, or improvement of existing technologies. The later can be directed towards integration of two or more major units/processes for product recovery. This study was initiated to integrate FO technology as an osmotic concentration step in the succinic acid downstream processing. With real fermentation broth as the feed solution, this work aimed at demonstrating a FO-crystallization process for the recovery of high-value succinic acid. Clarification of fermentation broth via activated carbon treatment was firstly investigated. The purpose of the pretreatment step is to decolorize the broth and to remove the residual glucose and other possible contaminants. Color intensity and HPLC analysis were performed to select the appropriate activated carbon dosage for effective pretreatment of fermentation broth. The feasibility of the subsequent FO concentration process was investigated by using two testing protocols (with and without activated carbon pretreatment). Effects of various performance parameters including water flux, concentration factor, feed solute rejection, and membrane fouling propensity were systematically studied. Lastly, crystallization was employed as the final purification step. Direct crystallization not only enables the recovery of desired product in solid form but also in reducing number of unit operations. The fermentation end product was obtained in succinic acid crystal form. 2. Materials and methods 2.1. Downstream recovery of succinic acid from fermentation broth The fermentation broth was provided by the Biohydrogen Research Group from the Department of Chemical and Process Engineering, Universiti Kebangsaan Malaysia. Actinobacillus succinogenes 130Z, a prominent strain that produces succinic acid, was obtained from the German Collection of Microorganisms and Cell Cultures (DSMZ, Brunswick, Germany). Oil palm frond (OPF) bagasse was hydrolyzed and used as the only carbon source for fermentative production of succinic acid. Fermentation was operated at neutral pH condition. The final organic acid products were almost in their salt forms rather than the free acid due to pH neutralization. The production details of succinic acid from OPF bagasse can be referred from previous work [36]. Fig. 1 illustrates the flow diagram of the succinic acid recovery process. The collected fermentation broth was centrifuged (Eppendorf 140

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using activated carbon adsorption for the removal of residual glucose and coloring impurities. The pretreated fermentation broth was then concentrated using FO process. The FO-concentrated broth was acidified to pH 2.0 and the crystal of succinic acid was obtained via crystallization. 2.2. Activated carbon treatment Currently, membrane-based process (e.g. UF, MF) was reported as one of the promising methods for the pretreatment or clarification of fermentation broth [9,16,17]. Nevertheless, membrane fouling propensity has been the main concern when dealing with untreated succinic acid fermentation broth. Activated carbon adsorption which is known as an effective, non-toxic and economic method for removal of impurities and pollutants [37,38], can potentially serve as an alternative to the existing technologies. To date, only a few studies have reported on the removal of impurities from fermentation broth by activated carbon treatment, of which very limited information was provided [7,14,37]. In that regard, activated carbon adsorption has been selected as the pretreatment step in this work. Different amounts of powdered activated carbon (PAC), between 0.02 and 0.06 g activated carbon/g broth, were added to the fermentation broth in Erlenmeyer flasks for removing organic impurities and colors [7,14]. Flasks were kept well mixed at 30 °C in an incubator shaker (Ecotron, Infors AG, Bottmingen, Switzerland) at 200 rpm for 24 h. After the adsorption treatment, the broth was centrifuged for the removal of activated carbon. Filtration was performed once again using vacuum filtration (Whatman cellulose nitrate membrane filters, plain, sterile, 0.45 μm pore size, 47 mm circle) to ensure the removal of any suspended residues from the broth. The surface characteristics of activated carbon (Table 2) were determined by adsorption isotherm of nitrogen obtained at 77.3 K (Micromeritics ASAP2020, TRISTAR II 3020 Kr). The specific surface area was determined based on Brunauer-Emmett-Teller (BET) technique. The morphology structure was determined using high resolution field emission scanning electron microscopy (FESEM) (Gemini SUPRA 55VPZEISS, Oberkochen, Germany). Color of the broth samples was analyzed using DR3900 benchtop spectrophotometer (Hach, USA) for both the optical density (OD) at 420 nm [16] and Platinum-Cobalt (PtCo) color scale. The decolorization ratio (η) was calculated using Eq. (1) [37].

(%) =

Molecular weight (Da)

pKa

Concentration (g/ L)

Succinic acid Acetic acid Formic acid Glucose

C4H6O4 C2H4O2 CH2O2 C6H12O6

118.09 60.05 46.03 180.16

4.21; 5.64 4.70 3.84 –

29.16 ± 0.90 3.74 ± 0.37 0.25 ± 0.04 3.35 ± 0.30

× 100%

(1)

2.3. Forward osmosis 2.3.1. FO membrane The asymmetric CTA membrane (HTI, Albany, OR, USA) specifically developed for FO process was used in this work. It was made of a dense cellulose triacetate active layer with embedded polyester screen mesh support. The effective membrane area of the tested membrane coupon was 42 cm2. The characteristics and operating limits of the membrane are shown in Table 3. The membrane was submerged in UP water

Table 1 Properties [14] and concentrations of main components present in the fermentation broth (pH = 6.8). Molecular formula

At A0

where A0 is the absorbance of the fermentation broth before decolorization, At is the absorbance of the fermentation broth after decolorization. The equation can also be applied based on Platinum-Cobalt color scale.

Fig. 1. Flow diagram of the downstream recovery process of bio-based succinic acid production.

Component

A0

Table 2 Characterization of the activated carbon.

Centrifuge 5804) for 20 min at 8000 rpm to separate the cell biomass and macromolecules. The composition of broth sample was analyzed using high performance liquid chromatography (HPLC) (Table 1). The fermentation broth containing succinic acid was initially pretreated 141

Properties

Activated carbon (PAC)

BET surface area (m2/g) Pore size (Å) Total pore volume (cm3/g)

659.6 25.15 0.4147

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Table 3 Characteristics and operating limits of FO membrane. Membrane properties

CTA

Manufacturer Active layer materialsa Contact angle (°) Active layer Support layer Zeta potential at pH 7 (mV) Active layer Support layer pH rangea Maximum operating temperaturea (°C) Maximum transmembrane pressurea (kPa) Membrane thickness (μm) Average pore diameterb (nm) Pure water permeability coefficientc, A (10−7 m/s.bar) Salt (NaCl) permeability coefficientc, B (10−7 m/s)

HTI Inc., USA Cellulose triacetate

a b c

57.6 ± 1.2 60.2 ± 3.2 −21.8 ± 5.1 −18.6 ± 5.8 3–8 71 70 < 95 0.74 0.858 0.195

Provided by the manufacturer. Adapted from Ref. [25]. Adapted from Ref. [39].

overnight prior to its use to remove the glycerin coating. Contact angles of both sides of the membrane were measured by a contact angle goniometer (DSA100, Kruss GmbH, Germany) using the standard sessile drop technique. The micrograph of the contact angle was captured and analyzed using the Drop Shape Analysis software. Membrane coupon was submerged into UP water overnight before drying for contact angle measurement. In order to reduce the measurement errors, multiple locations of membrane sample were tested. Membrane zeta potential was measured using streaming potential and streaming current electrokinetic analyzer (Zetasizer Nano ZS, Malvern Instruments, UK). The measurements were performed in a background solution containing 10 mM NaCl at pH 7, observed by 300–350 nm tracer particles. Three replicates were taken. The surface and cross-sectional morphology of the membrane were examined and photographed using high resolution FESEM. To analyze the cross-sectional morphology, each membrane was cryo-fractured by immersing in liquid nitrogen and broken in intact state immediately. Membrane samples were then mounted on an aluminium stub and sputter coated with a thin layer of platinum under vacuum to provide electrical conductivity. The membrane specimens were observed under the electron microscope at 3.0 kV. To obtain conspicuous comparison results, the SEM micrographs of the virgin and used membranes were presented in this work.

Fig. 2. Testing protocols for evaluating the influence of pretreated fermentation broth on FO process.

fermentation broth enrichment experiments except for shorter experimental duration (3 h). UP water and NaCl (5 M) were used as the feed solution and DS, respectively. FO performances were evaluated in terms of water flux, feed solute rejection, and concentration factor. An electronic balance (GF-6100, A& D Company Limited, Japan) was used to measure the variation of DS mass. The data collected for the initial 20 min was discarded, in consideration of the stabilization of the water permeability. The water flux (Jw) was determined using Eq. (2).

Jw =

m . × Am × t

(2)

where Δm is the mass variation of DS over a time interval of Δt, ρ is the density of water, and Am is the effective membrane area. To investigate the feed solute transport, sampling of the DS was taken at the end of the experiments or time t. Since the permeate concentration is being diluted by permeate volume of water to the DS, the calculated rejection value is higher than the actual rejection performance. Hence, an adjustment on the concentration of target solute can be performed by taking into account the dilution factor [40]:

2.3.2. Bench-scale experimental set-up FO was introduced as a concentration step in the recovery of succinic acid. A bench-scale crossflow FO system as described in our previous study was employed [27]. A FO cell (Sterlitech CF042 Cell) with channel outer dimensions measuring 12.7 × 10 × 8.3 cm and effective membrane area of 42 cm2 was utilized. The flat sheet membrane was placed in the center of FO cell with the orientation of active layer of the membrane facing the feed solution (AL-FS orientation). The testing protocols of FO performance assessment are described in Fig. 2. Fermentation broths were fed as feed solution in the study. For protocol A, the centrifuged broth bypassed the activated carbon treatment. A DS of 5 M NaCl (Merck, Darmstadt, Germany) was used to induce osmotic pressure driving force for the FO experiments. The osmotic pressure and viscosity of 5 M NaCl were simulated using OLI Stream Analyzer 9.2.2 (OLI Systems Inc., Morris Plains, NJ, USA). The initial volumes of feed solution and DS were 0.65 L and 2 L, respectively. During the FO process, the feed solution and DS were circulated on each side of the cell channel at a flow rate of 533.3 mL/min in closed loop counter-current mode. The experiments were conducted at ambient temperature (25 ± 2 °C) and lasted for at least 12 h. Baseline experiment was conducted using the same experimental conditions as that for the

Cfs (t ) = Cfs (DC ) ×

VDS (t ) VP

.

(3)

where Cfs(t) is the corrected concentration of target solute in the DS compartment at time t, Cfs(DC) is the measured concentration of target solute in the DS compartment at time t, VDS(t) is the volume of the DS at time t, and VP is the permeate volume of water to the DS at time t. Subsequently, the feed solute rejection (RFO) was calculated using Eq. (4) as below [25]:

Cfs (t )

RFO (%) = 1

Ci (t )

× 100%.

(4)

where Ci(t) is the concentration of target solute in the feed solution at time t. Feed solute flux (Jfs) was determined using Eq. (5) [41].

Jfs =

mfs Am × t

.

(5)

where mfs is the mass of target solute in the DS compartment at time t, and Am is the effective membrane area. The mass of target solute (mfs) was determined by multiplying the measured concentration of target solute (Cfs(DC)) by the volume of the DS (VDS(t)). 142

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The concentration factor (CF) of target solute in the feed solution at time t was calculated by the following equation.

CF =

Ci (t ) Ci (0)

.

(6)

where Ci(0) is the initial concentration of target solute in the feed solution. 2.4. Crystallization The crystallization process was performed using both the synthetic succinic acid and actual fermentation broth solutions. Succinic acid supplied by Acros Organics (New Jersey, USA) was used to prepare the synthetic feed solution. Succinic acid solutions (Synthetic A - 60 g/L, Synthetic B - 110 g/L) were prepared by dissolving the solutes in ultrapure (UP) water obtained from lab water system (arium® pro ultrapure water systems, Sartorius, Germany). The pH of concentrated broth obtained from FO system was adjusted to 2.0. Sulfuric acid, H2SO4 (98%, JT Baker, USA), a diprotic acid that comprises of two acidic protons, was employed in this work for effective acidification of fermentation broth [42]. Succinic acid was crystallized at 4 °C with 150 rpm agitation rate for 24 h. After crystallization, the succinic acid crystals were separated from the mother liquor by simple filtration, and washed with cold UP water (4 °C) for removing any impurities on the surface of the crystals. Lastly, succinic acid crystals were obtained by drying at 50 °C for 24 h. The crystals recovered were weighed and dissolved in UP water for HPLC analysis. The purity and the yield of the crystals recovered are represented by Eqs. (7) and (8) as follows [7,37]:

Purity (%) =

Yield (%) =

CSA WC / V

× 100 %

WSA × 100 % W0

Fig. 3. Decolorization ratio of fermentation broth using different dosage of activated carbon.

fermentation broth at increasing PAC loading. Accordingly, PAC exhibited high decolorization ratio ranging from 86.6 to 96.7% indicating high clarification degree of fermentation broth. SEM analysis allows the direct viewing of the surface morphology which provides important insights of activated carbon properties such as pore shapes and structures as well as the extent of adsorption. Fig. 4 shows the surface morphology of PAC before and after broth adsorption. The PAC particles were found in varied shapes and sizes, and consisted of both rough and smooth surfaces. Fig. 4(a) and (b) show the presence of various sizes of pores that were mainly oval in shape on the surface of PAC. It can therefore be postulated that the pore structure of the PAC was cylindrical capillary shaped pores. The different pore sizes play the important role of providing rich adsorption sites for adsorbing a diverse range of molecules [38]. From Fig. 4(c) and (d), it can be seen that the pores were densely filled with adsorbate molecules after the broth adsorption. This is in contrast to the SEM micrographs of virgin PAC. Further evidence of this is shown in Fig. 4(e) and (f) indicating high extent of adsorption on the surfaces and pores at different sections of PAC particles. The effect of PAC dosage on the composition of fermentation broth is presented in Table 4. Concentration of succinic acid after the PAC treatment was determined to ensure minimum loss of succinic acid during the treatment process. Encouragingly, no discernible reduction in the succinic acid concentration was observed despite the increase of PAC loading. Formic acid was not detected at PAC dosages of 3% (w/w) and above. This can be attributed to its low initial concentration and relatively smaller molecular size compared to other organic acids, which is preferential for adsorption. It has been reported that smallersized molecules could reach the surface of adsorbent faster than larger molecules during activated carbon adsorption [43]. Equally noteworthy is that the residual glucose in the broth could be completely removed with PAC dosage as low as of 2% (w/w). This is likely due to the high adsorption affinity of glucose to the PAC [44]. The color intensity analysis indicated significant improvement of decolorization for an increasing amount of PAC dosages from 2 to 4% (w/w) while no further improvement was observed at dosages above 4% (w/w). From all of the results, it can be inferred that the PAC treatment is appropriate to treat succinic acid broth and that an adequate PAC dosage of 4% (w/w) was chosen for the clarification of fermentation broth for protocol B. The impact of pretreated broth on fouling propensity in the subsequent FO concentration step is presented in the next section.

(7) (8)

where CSA is the succinic acid concentration in crystals recovered, WC is the dry weight of crystals recovered, and V is the UP water volume used in dissolving the crystals recovered, WSA is the dry weight of succinic acid in crystals recovered, and W0 is the initial dry weight of succinic acid in fermentation broth. 2.5. Analytical methods The concentrations of succinic acid, acetic acid, formic acid, and glucose were quantified using HPLC. The HPLC system (Dionex UltiMate 3000, Thermo Scientific, USA) equipped with a solvent rack (SR-3000), HPLC pumps (UltiMate 3000 Series), autosamplers (WPS3000), column compartment (TCC-3000), and a RI detector (RefractoMax521) was operated through Chromeleon Console software. Rezex ROA column (300 × 7.8 mm; Phenomenex, USA) with a guard column (50 × 7.8 mm) was operated at 60 °C. The sulfuric acid mobile phase (0.005 N) was maintained at the flow rate of 0.6 mL/min. Sample injection volume was 20 μL. All samples were filtered through 0.22 μm membrane syringe filter prior to HPLC analysis. 3. Results and discussion 3.1. Clarification of fermentation broth The first step of succinic acid recovery process was to separate cell debris/biomass from fermentation broth via centrifugation [9,42]. The filtrated broth was then treated with PAC overnight to remove impurities and colors. Broth decolorization is required to ensure high purity of final product and reduce the tendency of contamination of succinic acid crystals [16,18]. Fig. 3 presents the decolorization ratio of 143

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Fig. 4. SEM micrographs of PAC: (a) & (b) virgin PAC and (c), (d), (e) & (f) after broth adsorption by 4% (w/w) PAC.

3.2. FO concentration of fermentation broth

because the cellulose-based membrane contains hydrophilic hydroxyl groups. Contact angle of the membrane support layer was also measured for comparison. Both the active and support layers demonstrated similar hydrophilicity due to the same polymer material throughout the membrane [45]. The hydrophilic nature of CTA membrane can favor water transport during FO process. Zeta potential measurements showed that the surface charges of both sides of the membrane were

3.2.1. Membrane characterization Membrane hydrophobicity and surface charge were characterized by measuring the contact angles and zeta potentials of both sides of the CTA membrane, respectively. According to Table 3, the contact angle of the active layer was 57.6°, which is moderately hydrophilic. This is Table 4 Concentration of each component in the broth after activated carbon treatment. PAC dosage (g activated carbon/g broth)

Component (g/L) Succinic acid Acetic acid Formic acid Glucose Color intensity OD420 nm Platinum-Cobalt (PtCo)

0.02

0.03

0.04

0.05

0.06

27.78 ± 1.06 3.67 ± 0.43 0.27 ± 0.08 0

27.79 ± 0.37 4.12 ± 0.10 0 0

28.88 ± 1.47 3.97 ± 0.24 0 0

29.39 ± 1.29 3.68 ± 0.35 0 0

29.50 ± 2.09 3.88 ± 0.40 0 0

0.114 ± 0.019 93 ± 13

0.057 ± 0.007 50 ± 6

0.037 ± 0.003 26 ± 4

0.037 ± 0.001 28 ± 4

0.036 ± 0.001 28 ± 1

144

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Fig. 5. SEM micrographs of the virgin CTA membrane: (a) active layer (top surface), (b) support layer (bottom surface), (c) cross-section (magnification 500×) and (d) cross-section on the active layer side (magnification 2000×).

since the osmotic pressure driving force can be constantly maintained. The osmotic pressure and viscosity of 5 M NaCl were 356 atm and 1.650 cP, respectively. High NaCl concentrations ranged from 4 M to 6 M have been used in previous studies [21,50]. Baseline experiment was conducted to which experimental results can be compared. Fig. 6 (a) presents the experimental water flux profiles as a function of permeation time at initial flux phase (3 h). The baseline flux was significantly higher than the others due to the greater osmotic pressure gradient across the membrane caused by the negligible osmotic pressure of UP water feed. With fermentation broth as the feed solutions, the initial water flux decreased to 9.09 L/m2.h (protocol A) and 10.14 L/m2.h (protocol B), respectively, from an initial baseline value of 13.03 L/m2.h. The adsorption of organic materials (e.g. coloring impurities) to the membrane during the early stage of flux stabilization has resulted in lower initial flux for protocol A [51]. The baseline flux showed slight decline over time, mainly due to the dilution of bulk NaCl DS concentration. Similar flux decline trends were also obtained for broth feed solutions. This observation can be attributed to several factors, including the dilution effect of NaCl DS, concentration effect of fermentation broth, and fouling of membrane [52]. In general, the degree of fouling is reflected by the comparison of flux decline curves. Fig. 6(b) presents the water flux profiles for the concentration of fermentation broths, which is an extension in time of Fig. 6(a). It can be seen that the water flux declined drastically with time for the entire concentration process for both testing protocols, albeit the clarified fermentation broth (protocol B) had apparently contributed to less fouling propensity. Comparison of water flux loss indicated a 35.8% decline in flux for the clarified fermentation broth (12 h) whereas a higher flux loss of 55.1% was observed for untreated fermentation broth (protocol A). The concentration process for protocol A was terminated after 12 h of experimental duration considering the significant reduction of water flux. The flux decline trend of untreated fermentation broth was ascribed to the reduction of osmotic pressure driving force and the adverse effect of cake layer formation on

negative at pH of 7. The membrane support layer exhibited relatively less negative surface potential than the active layer. These results are in agreement with the zeta potential value as reported by Xue et al. [46]. The negative charge is likely related to the adsorption of anions such as hydroxide ions on the membrane surfaces [47]. Fig. 5 shows high quality SEM micrographs of the unique structure of the virgin CTA membrane. These images indicate an asymmetric membrane structure that is made of a dense cellulose triacetate selective layer on top of a porous support layer. Fig. 5(a), (b) and (c) show the presence of embedded polyester mesh on the backside of the membrane. Such structure is designed to provide mechanical strength to the membrane, thus eliminating the need for a thick support layer. According to Fig. 5(c), the cross-section of the membrane has an overall thickness of not greater than 95 μm, depending on the position of the polyester mesh. The support layer is composed of many macrovoids spanning almost the entire layer. It is apparent that the reduced thickness of FO membrane and the porous support structure can mitigate the adverse effect of internal concentration polarization (ICP) and improve the water permeability of the membrane [46,48]. A dense active layer of approximately 1.6 μm is clearly visible in the magnified microscopic image (magnification 2000×), as illustrated in Fig. 5(d). 3.2.2. FO performance for concentrating succinic acid To evaluate the impact of pretreated fermentation broth on FO performances, two testing protocols (with and without activated carbon treatment) were investigated (see Fig. 2). The selection of suitable draw solute with appropriate solution concentration can ensure the spontaneous migration of water molecules from feed to DS compartment. NaCl as a draw solute is well known for its properties such as highly soluble and non-toxic, inexpensive, high osmotic pressure, low viscosity, and easily regenerated. Thus NaCl has been selected as draw solute in this study [49]. Since our work utilized a batch process, the use of 5 M NaCl DS could ensure sufficient effective driving force. It must be noted that a full-scale continuous process would require lower DS concentration 145

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continuous process. In that regard, the osmotic pressure driving force can be constantly maintained by periodic membrane back-flushing and chemical cleaning, and DS regeneration. Concentration factor (CF) is an important index parameter used to reflect the concentration degree of the feed solution. According to Table 5, a substantial increase in succinic acid concentration was obtained for both experimental protocols. With untreated broth as the feed solution, succinic acid, acetic acid, and formic acid were concentrated by 2.1-fold, 1.9-fold, and 1.6-fold, respectively. Succinic acid was concentrated to 60.53 g/L from an initial feed value of 29.16 g/L. In the case of the clarified fermentation broth, succinic acid was concentrated to a greater extent and a higher flux throughout the process. After 12 h of FO process, the concentration of succinic acid was increased by approximately 3.1-fold to 89.41 g/L. Further extension of FO duration (14 h) demonstrated a remarkable enhancement of CF by 3.9fold and thus resulting in a final succinic acid concentration of 111.26 g/L. Similar CF was obtained for acetic acid. It must be noted that the increase of CF was associated with the significant decline of water flux as a result of decreased effective driving force as described above. This observation is in good agreement with the previous study [54]. In contrast with those that have been observed, glucose exhibited much lower CF than expected. There are several possible reasons for this observation including low rejection efficiency or adsorption and deposition of the solute to the membrane, which will be discussed later. The rejection of feed solute by FO membrane is presented in Table 6. Results revealed that strong succinate rejections of higher than 99% were obtained for both experimental protocols indicating insignificant succinate leakage to the DS. Such observation also explained the high CF obtained in this work. Our previous study demonstrated that the pH-dependent speciation of succinic acid could affect the succinate rejection considerably [55]. At broth pH of 6.8 which is higher than its pKa2 value (see Table 1), succinic acid existed predominantly in the broth as divalent anions (C2H4C2O42−) [14]. Consequently, strong rejection of succinate was promoted by the largersized hydrated succinate anions through molecular size exclusion as well as electrostatic repulsion between the divalent succinate anions and the negatively charged CTA membrane [55,56]. Likewise, acetic acid and formic acid appeared in their ionic forms as monovalent anions. In both cases, the rejection of acetate was slightly lower than succinate. This can be ascribed to the sieving exclusion of relatively smaller-sized acetate anions. Similar rejection performance can be anticipated from formate anions. According to Table 5, the final formic acid concentration obtained from protocol A was very low (0.41 g/L). In that regard, the formate rejection was unquantifiable in this work due to its negligible amount in the DS. For protocol B, formic acid and glucose have been completely removed from fermentation broth during PAC treatment (see Table 4). Hence, the formic acid and glucose rejections were not presented in Table 6. Along with the feed solute rejection, the feed solute flux indicating the forward transport of feed solute was also provided. The findings are useful for process design and optimization in FO. Overall, the results implied that FO is feasible in treating actual fermentation broth and that the water permeating through the dense active layer of the membrane showed almost complete rejection of feed solutes. The superior rejection performance suggests that FO should be performed prior to acidification step (pH

Fig. 6. (a) Water flux profiles as a function of time at initial flux phase (3 h). (b) Water flux profiles for the concentration of fermentation broths (12 or 14 h).

membrane surface, the latter of which was playing a much major role in impacting the flux loss performance. This explanation was supported by the subsequent SEM analysis (section 3.2.3). On the contrary, the flux decline shown by protocol B was largely due to the higher initial flux level and thus leading to more significant broth concentration (see Table 5) and DS dilution [53]. It must be pointed out that a full-scale process for industrial application would almost certainly be a

Table 5 Concentration factor (CF) and final concentration of each component in fermentation broth for two testing protocols. Component

Succinic acid Acetic acid Formic acid Glucose

Protocol A

Protocol B

Cinitial (g/L)

Cfinal,

(g/L)

CF

Cinitial (g/L)

Cfinal,12h (g/L)

CF

Cfinal,

(g/L)

CF

29.16 ± 0.90 3.74 ± 0.37 0.25 ± 0.04 3.35 ± 0.30

60.53 ± 2.68 6.93 ± 0.37 0.41 ± 0.07 3.02 ± 0.19

2.1 1.9 1.6 0.9

28.88 ± 1.47 3.97 ± 0.24 0 0

89.41 ± 1.81 12.83 ± 0.12 0 0

3.1 3.2 – –

111.26 ± 4.23 15.38 ± 0.74 0 0

3.9 3.9 – –

12h

146

14h

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Table 6 Feed solute rejection (RFO) and feed solute flux (Jfs) of each component in fermentation broth for two testing protocols. Component

Protocol A RFO,

Succinic acid Acetic acid Formic acid Glucose

12h

(%)

99.91 ± 0.01 98.05 ± 0.21 – 95.27 ± 0.17

Protocol B Jfs,

12h

2

(g/m .h)

0.364 ± 0.042 0.856 ± 0.093 – 0.907 ± 0.033

RFO,

12h

(%)

99.87 ± 0.01 99.32 ± 0.16 – –

2.0) in the downstream processing of succinic acid (see Fig. 1) due to the speciation behavior of organic acid. One interesting feature observed for protocol A is the decrease of glucose concentration (see Table 5), which is in contradiction with other solutes in the broth. Based on the high rejection efficiency (95.27%), the decrease of glucose concentration was mainly caused by the adsorption of glucose to the membrane [53]. Since glucose molecules were undissociated and uncharged in solution, they became easily attached and accumulated on the membrane surface, and subsequently combined with other coloring impurities and led to the formation of cake layer [52]. Further evidence of this is shown in the results from the SEM and EDX spectroscopy analysis in the later segment. Reverse solute permeation is an inevitable phenomenon and affect the purity of feed solution in FO process. Based on our previous study [55], the reverse chloride fluxes of 5 M NaCl DS were between 6.5 and 7.2 g/m2.h for synthetic succinic acid feed solution. Selection of an ideal draw solute and regeneration process is beyond the scope of the current study. Various studies have explored novel draw solutes that can be easily regenerated via suitable recovery technologies [35].

Jfs,

12h

(g/m2.h)

0.918 ± 0.057 0.707 ± 0.168 – –

RFO,

14h

(%)

99.90 ± 0.01 99.11 ± 0.06 – –

Jfs,

14h

(g/m2.h)

0.892 ± 0.050 1.059 ± 0.068 – –

attributed to the absence of externally applied pressure [23]. It is noteworthy that the formation of a cake layer was absent in the clarified fermentation broth (Fig. 7(f)) albeit with higher CF achievement. The overall findings confirmed that activated carbon treatment as a pretreatment step of fermentation broth could significantly ameliorate membrane fouling for the FO system. Most studies concerning the fouling in FO process have been focusing on the active layer of the membrane. In FO mode operation, the membrane support layer is placed against the DS. Hence, foulant deposition and accumulation is affected by the DS containing ionic salt on the support layer. Fig. 8(a) shows a micrograph of used membrane which is comparable to the support layer of virgin CTA membrane (see Fig. 5(b)). As Fig. 8(b) shows (magnification 2000×), mild foulant deposition was observed after 14 h operation. Evidently, the fouling condition of the membrane support layer was not significant albeit with high concentration of NaCl DS. In general, FO membrane fouling is mainly governed by the chemical and hydrodynamic interactions. Hydrodynamic interactions including permeation drag and shear force, resulting from the convective permeate flow and bulk cross-flow, respectively, affect the foulant formation on the membrane surface [58]. Since the support layer was the back layer of the membrane, it is likely that hydrodynamic interactions and water permeation from the feed towards the DS compartment drove foulant away from the support layer surface. Furthermore, electrostatic repulsion between the chloride anions and the negatively charged support layer may also contribute to less foulant formation [53].

3.2.3. Microscopic examinations of fouled membranes Microscopic examinations were conducted on the used membranes at the end of the FO operations to facilitate the understanding of the fouling behaviors involving real fermentation broth. Fig. 7(a) presents the SEM micrograph of the active layer surface from the experiment conducted using protocol A. When compared to the virgin CTA membrane (see Fig. 5(a)), the surface of the active layer was densely covered by a smooth cake layer. By contrast, Fig. 7(c) shows a micrograph of used membrane which is comparable to the virgin CTA membrane indicating a mild fouling condition for experiment conducted using protocol B. This is further verified by a magnified view of the active layer surface (magnification 2000×), as shown in Fig. 7(d). These observations are congruent with the foregoing discussion on water flux performance, and substantiates that the membrane was more prone to fouling when untreated fermentation broth was fed as the feed solution. EDX spectroscopy analysis (Fig. 7(b)) showed that the cake layer foulant consisted predominantly of carbon and oxygen elements. It is apparent that the membrane fouling was mainly caused by the organic impurities that contributed to the brown color of the broth [42]. The presence of sodium, chloride and potassium elements was due to the salt impurities that present in the broth and the reverse diffusion of NaCl draw solute. These elements appeared in much lower level compared to carbon and oxygen elements, where no crystalline salt particles were observed on the membrane surface layer. The cross-section of the membrane (Fig. 7(e)) validated the formation of a thick fouling cake layer for untreated broth. Estimates from the micrograph indicated a cake layer thickness of as high as 29.5 μm. No severe internal clogging was observed for the porous support layer. This interesting observation was consistent with the results previously reported by Tang et al. [57] who examined the effect of membrane orientation on FO fouling. They postulated that the membrane fouling in the AL-FS orientation was mainly dominated by cake layer formation on the active layer surface whereas severe internal clogging of the support layer happened in the AL-DS orientation. It has been demonstrated that a thick but relatively soft and fluffy loose structure of fouling layer was formed which was

3.3. Crystallization for succinic acid recovery Being one of the conventional but effective processes for the recovery of succinic acid, direct crystallization was applied as the final purification step. After FO process, the concentrated broths obtained from both the testing protocols were acidified to pH 2.0. Under such acidic condition (pH ≪ pKa1), succinic acid molecules were mainly found in the undissociated free acid form and thus exhibiting low solubility [14]. The low solubility in conjunction with appropriate cooling temperature leads to supersaturation of succinic acid solution, which is vital for the occurrence of crystallization [18]. Table 7 shows the purity and yield of the recovered succinic acid crystals. Synthetic pure acid solutions (assumption of 100% purity) were also tested for comparison. The purity and yield of succinic acid crystals recovered from clarified fermentation broth were 90.52% and 67.09%, respectively, consistent with the results previously reported by Li et al. [14]. In comparison, relatively higher yield (72.42%) was obtained with pure succinic acid solution (Synthetic B). This is due to the fact that high purity singlesolute solution tends to have lower solubility than the impure broth [59]. Additionally, small amounts of succinic acid were lost during the wash off of the crystal surfaces [18]. The yield of the crystals was substantially increased at higher initial succinic acid concentration, as shown by the synthetic solutions. The scope of this study does not cover the optimization of the crystallization process. One notable finding is that the crystallization of untreated fermentation broth was unsuccessful and that the succinic acid product remained miscible in the broth. Apparently, the presence of impurities (i.e. glucose, coloring impurities) in the untreated broth has been a major hindrance to the 147

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Fig. 7. SEM micrographs of the active layer (top surface) and cross-section of fouled membranes from experiments conducted by protocol A and protocol B; EDX spectra of the cake layer on the active layer surface.

Fig. 8. SEM micrographs of the support layer (bottom surface) of fouled membrane: (a) magnification 100× and (b) magnification 2000×.

148

149

Current work

[14]

[8]

- Operation at ambient temperature and pressure (FO) - Prevent product degradation 67.09 90.52

1.25 MPa (NF), 80 °C (evaporation) 25 °C (FO) MF-NF-evaporation- crystallization

FO-crystallization

75 °C (vacuum distillation) – Reactive extraction-vacuum distillation- crystallization One-step crystallization

99.18

86.53

One-step recovery process (still require pretreatment of fermentation broth) High succinic acid crystals purity and yield

60 °C (vacuum distillation)

70

Yield (%) Purity (%)

Vacuum distillation- crystallization

The authors wish to gratefully acknowledge the financial support

Operating conditions

Acknowledgements

Downstream process

Table 8 Summary of downstream processing of succinic acid recovery integrating direct crystallization.

This research developed an integrated downstream process involving three main steps: removal of broth impurities by using activated carbon, concentration of the fermentation broth by FO process followed by purification of succinic acid by crystallization. Activated carbon treatment could effectively clarify the fermentation broth, with low PAC dosage of 4% (w/w). The pretreated broth has notable impact on fouling amelioration in the subsequent FO process. Osmotically driven FO is an exciting method of concentrating succinic acid broth at ambient conditions. With clarified broth as the FO feed, succinic acid concentration was increased by approximately 3.9-fold to 111.26 g/L, from an initial feed value of 28.88 g/L. The increase of CF was associated with significant water flux loss as a result of decreased effective driving force. No discernible foulant layer was formed in the clarified broth experimental protocol, which is noteworthy. The CTA membrane consisting of a dense active layer satisfied high succinate rejection (> 99%) requirement in FO mode operation. The overall findings showcased the remarkable ability of FO to increase the concentration of succinic acid in complex fermentation broth, which is a vital part of FO feasibility study. The fermentation end product was successfully obtained in succinic acid crystal form via direct crystallization. This work provides practical insight into the FO-crystallization downstream process for succinic acid recovery from real fermentation broth. However, a number of technical obstacles and challenges must be overcome including the development of ideal draw solutes that can be cost effectively regenerated and the fabrication of FO membranes that can mitigate ICP and tailoring them for bioprocess industries. Further work on optimization of process performances (concentration, yield, purity) of the multi-stage downstream system would be desired.

Advantages

4. Conclusions

90

Disadvantages

crystallization process which could be attributed to the increase of succinic acid solubility [59]. Table 8 summarizes the recent research efforts in the downstream processing of succinic acid recovery integrating direct crystallization. Each of the methods has its own advantages and disadvantages depending on the need of the process. This work demonstrated the development of a FO-crystallization process that is currently missing within the scientific literature. In the food and beverage industry, succinic acid is used as flavoring enhancer, sequestrant, neutralizing agent, and anti-microbial agent [60,61]. Conventional thermal-driven evaporation can cause quality degradation problems in addition to being uneconomical due to high energy consumption [16,20,21]. With ambient operating conditions as well as acceptable separation performance, FO can act as a bridge between the upstream and downstream processes, thus replacing the energy intensive thermal-driven processes. In the absence of externally applied pressure, it is expected that the lifespan of FO membrane is longer compared to the RO membrane that utilizes high hydraulic pressure as driving force. Further assessment on the economic viability and apparent benefits of each method for full-scale production of bio-based succinic acid would be desired.

- Require highly selective extractant - Replenishment or regeneration of extractant The elimination of concentration step was due to high succinic acid concentration in the fermentation broth - High water consumption during diananofiltration mode - High energy consumption during evaporation Replenishment or regeneration of DS

72.42 ± 2.24 67.09 ± 2.94 48.52 ± 1.98 –

66.44–67.05

100.00 90.52 ± 0.41 100.00 –

98.17–99.55

110.00 111.26 ± 4.23 60.00 60.53 ± 2.68

[7]

Synthetic B Broth (protocol B) Synthetic A Broth (protocol A)

Low succinic acid crystals purity and yield

Yield (%)

Simultaneous removal of volatile byproducts and concentration of fermentation broth by vacuum distillation High succinic acid crystals purity

Purity (%)

28

Succinic acid concentration (g/L)

45

Solution

Ref.

Table 7 Summary of succinic acid crystals recovered from fermentation broths and synthetic succinic acid solutions (A and B).

[16]

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for this work provided by the LRGS/2013/UKM-UKM/PT/03 grant from the Ministry of Education Malaysia.

[24]

Appendix A. Supplementary data

[25]

Supplementary data to this article can be found online at https:// doi.org/10.1016/j.memsci.2019.04.036.

[26]

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