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Removal and recovery of inhibitory volatile fatty acids from mixed acid
fermentations by conventional electrodialysis
Rhys Jon Jonesa, Jaime Massanet-Nicolau, Alan Guwy, Giuliano C. Premier, Richard M. Dinsdale, Matthew
Reilly.
a Sustainable Environment Research Centre, Faculty of Computing Engineering and Science,
University of South Wales, Pontypridd CF37 1DL, United Kingdom.
E-mail: [email protected]
Abstract
Hydrogen production during dark fermentation is inhibited by the co-production of
volatile fatty acids (VFAs) such as acetic and n-butyric acid. In this study, the
effectiveness of conventional electrodialysis (CED) in reducing VFA concentrations in
model solutions and hydrogen fermentation broths is evaluated. This is the first time
CED has been reported to remove VFAs from hydrogen fermentation broths. During 60
minutes of operation CED removed up to 99% of VFAs from model solutions, sucrose-
fed and grass-fed hydrogen fermentation broths, containing up to 1,200 mg·l-1 each of
acetic acid, propionic acid, i-butyric acid, n-butyric acid, i-valeric acid, and n-valeric
acid. CED's ability to remove VFAs from hydrogen fermentation broths suggests that
this technology is capable of improving hydrogen yields from dark fermentation.
Keywords
Anaerobic Digestion; Hydrogen; Grass; Electrodialysis; Volatile Fatty Acids;
Fermentation.
1. Introduction
Alternative energy sources to fossil fuels must be made readily available if the problems
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associated with diminishing reserves, environmental damage, security of supply, and
increasing demand are to be overcome (Patterson et al., 2008; Yüksel, 2010).
Converting a biomass energy source to a hydrogen energy vector is attractive due to its
high calorific value of 122 kJ·g-1 (Azbar and Cetinkaya Dokgoz, 2010), and because it
represents a renewable and carbon neutral fuel (Meherkotay and Das, 2008). Fossil fuels
are currently more economically attractive than alternative energy vectors however and
questions regarding the long term availability of biomass in sufficient volumes to
establish a hydrogen economy need to be addressed before its large-scale production is
feasible (Hay et al., 2013).
Dark fermentation, which uses a range of substrates from industrial waste to energy
crops, is a widely researched, renewable, pathway to hydrogen. Theoretically, it is
possible to produce 4 mol H2·mol-1 hexose sugar when acetic acid is the only product
(Guwy et al., 2011), but experimental values tend to be in the range of 2.5 - 3.5 mol H2
mol-1 hexose sugar due to thermodynamic limitations (De Gioannis et al., 2014;
Rosales-Colunga et al., 2010). Hydrogen yields are also limited by the co-production of
volatile fatty acids (VFAs), in particular acetic acid and n-butyric acid, which form
during fermentation. VFA formation eventually prevents hydrogen production due to
end product inhibition (Hawkes et al., 2007; Hirata et al., 2005) and cell lysis of the
hydrogen producing bacteria (Choudhari et al., 2014; Tang et al., 2014)
Studies have demonstrated that reducing the concentrations of acetic acid and n-butyric
acid in hydrogen fermentation broths, via bipolar membrane electrodialysis, increases
hydrogen yields (Redwood et al., 2012a, 2012b; Tang et al., 2014). Bipolar membrane
electrodialysis is one of several electrodeionisation and electrodialysis processes, the
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majority of which were described by Huang et al (Huang et al., 2007). Bipolar
membrane electrodialysis requires expensive, bipolar, water-splitting, membranes in
order to work and reported increases in hydrogen yield using glucose as a substrate are
inconsistent. For example, Tang et al. (Tang et al., 2014) report an increase from 1.7 to
2.2 mol H2·mol-1 glucose, whereas Redwood et al. (Redwood et al., 2012b) claim that
the removal of organic acids via bipolar membrane electrodialysis prolongs
fermentation time from 3 days to 3 weeks, tripling H2 production in doing so from 1 to 3
mol H2·mol-1 glucose. More recent work used activated carbon as a means to extract
inhibitory byproducts from hydrogen reactors fed by water hyacinth, and increased
hydrogen yields from 124.9 ml H2·g-1 total volatile solids to 134.9 ml H2·g-1 total
volatile solids (Cheng et al., 2015). As will be discussed below, VFAs are valuable in a
number of applications and their recovery following activated carbon treatment would
be difficult.
The work reported here compares the ability of conventional electrodialysis (CED) to
reduce VFA concentrations in model solutions, and post-fermentation broths that were
obtained following dark fermentation of sucrose and grass pellets. CED is a versatile
technology that can concentrate, dilute, and separate matter whilst producing relatively
low amounts of waste (Bailly et al., 2001; Huang et al., 2007; Lameloise and
Lewandowski, 2012). CED utilises less costly materials than bipolar membrane
electrodialysis, as was used by Redwood et al. (Redwood et al., 2012b) and Tang et al.
(Tang et al., 2014), and so in some applications it could possess an economical
advantage over bipolar membrane electrodialysis. VFAs extracted via CED would not
be contaminated as they might be using Cheng et al’s (Cheng et al., 2015) activated
carbon method, so they can easily be used as substrates in downstream bioenergy
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systems such as photofermentation, microbial electrolysis, and microbial fuel cells,
theoretically producing up to 12 mol H2·mol-1 hexose sugar (Claassen et al., 2010;
Guwy et al., 2011; Redwood et al., 2012a, 2012b; Singhania et al., 2013, 2012).
Acetic acid, one of the VFAs that can be extracted, also has uses beyond conversion to
an energy carrier. It has been called “one of the world’s most important chemicals”
(Ijmker et al., 2014) due to widespread use in manufacturing polymers, polyethylene
terephthalate, and solvents. According to market forecasts, its global demand in 2013
was 10.4 mt, and by 2020 its market revenue is expected to reach $12.2 billion. There is
also demand for butyric acid, which is used in the cosmetic, food, and pharmaceutical
industries and along with other VFAs, it can also be used as a precursor to fuels and
chemicals (Agler et al., 2011; Blahušiak et al., 2013; Choudhari et al., 2014).
The aim of this work is to establish how well conventional electrodialysis can reduce
the VFA concentrations of post-fermentation broths compared to model solutions. It is
important to make this comparison because post-fermentation broths are high in
microbial and particulate matter, both of which are known to contribute to fouling and
thus a gradual reduction of the ion flux within a CED stack (Hongo et al., 1986; Lee et
al., 2003; Singhania et al., 2012; Strathmann, 2010). Fouling is reported to increase
electrical resistance within CED stacks, thereby reducing current efficiency, which is
widely used to quantify the performance of electrodialysis processes (Ferrer et al., 2006;
Huang et al., 2007; Lameloise and Lewandowski, 2012; Wang et al., 2011, 2010). If
CED is found to be capable of removing VFAs from post-fermentation broths in similar
quantities to model solutions, there would be scope for further studies in to the ability of
CED to remove VFAs from working reactors. The possibility exists that CED may also
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be capable of removing VFAs from dilute aqueous solutions, which has hitherto proved
problematic for the production of chemicals and fuels from the otherwise promising
carboxylate platform (Agler et al., 2011), although this application falls outside of the
scope of this study. This is the first time the ability of conventional electrodialysis to
remove VFAs from post-fermentation broths has been reported and quantified. It is also
the first study in which a comparison has been drawn between the ability of
conventional electrodialysis to treat model solutions and post-fermentation broths.
2. Materials and Methods
2.1 Experimental design
Conventional electrodialysis was carried out on controls; model solutions that contained
VFAs and deionised water to establish baseline VFA removal data in the absence of
microbial and particulate matter. CED was then performed on hydrogen fermentation
broths collected following sucrose and grass fermentations within continuously stirred
batch reactors, which contained microbial and particulate matter, and the VFA removal
data were compared to the baseline established by CED of model solutions. CED was
carried out on two batches each of the model solution, sucrose fed reactor broth, and
grass fed reactor broth.
2.2 Apparatus
The apparatus for conventional electrodialysis (Figure 1) is typically referred to as a
CED “stack” and consists of two electrodes (one anode and one cathode) across which
an electrical potential is established by an external power supply, and which are housed
within an anode chamber and a cathode chamber. Between the electrodes are alternating
anion exchange membranes (AEMs) and cation exchange membranes (CEMs), which
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are separated by spacers to create Diluate and Concentrate Chambers, through which
liquids flow. A wider housing encases and supports the aforementioned components. In
this study the CED stack was manufactured by PCCell GmbH (Heusweiler, Germany),
and the model was an ED 64002 with 20 cell pairs (0.128 m2 effective membrane area).
2.3 Preparation of model solutions and stock solutions
Three, distinct, solutions flow through a CED stack; concentrate, dilute, and electrolyte.
In this study, the concentrate (250 ml phosphate buffer solution: 8,000 mg·l-1 NaCl;
1,440 mg·l-1 Na2HPO4; 240 mg·l-1 KH2PO4; and 200 mg·l-1 KCl) and electrolyte (1,000
ml of Na2SO4 at 35,510 mg·l-1) remained the same throughout all experiments. The
dilute varied between experiments and consisted either of 250 ml model VFA solutions
(1,000 mg·l-1 each of acetic, propionic, i-butyric, n- butyric, i-valeric and n-valeric acid,
and 8,000 mg·l-1 NaCl; 1,440 mg·l-1 Na2HPO4; 240 mg·l-1 KH2PO4; and 200 mg·l-1 KCl),
or hydrogen fermentation broths, the compositions and preparations of which are
outlined below. VFA concentrations in model solutions where chosen to approximate
VFA levels obtained from fermentative hydrogen production using a variety of
substrates such as sewage biosolids, grass and wheat co-product (Massanet-Nicolau et
al., 2013, 2010; Yu et al., 2014).
2.4 Preparation of hydrogen fermentation broths
Two dark hydrogen fermentation reactors, one sucrose-fed, and one grass pellet fed
continually stirred batch reactors were adapted from Reilly et al’s (Reilly et al., 2014)
method as follows. The sucrose-fed continuously stirred batch reactors contained 100
ml of 15 g·l-1 sucrose solution, 120 ml of inoculum (sewage sludge from a sewage
treatment works serving a large metropolitan area), and 280 ml of water. The grass
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pellet fed continuously stirred batch reactors were identical except 100 ml of 80 g·l-1
grass pellet suspension was added instead of sucrose solution. To inactivate
methanogenic organisms and to prevent their eventual consumption of hydrogen, the
inoculum was heated to 120°C for 40 minutes and once cooled to room temperature,
120 ml of inoculum was added to each continuously stirred batch reactor. To establish
anaerobic conditions for dark fermentation, each continuously stirred batch reactor was
sparged with carbon dioxide until its pH level reached 6.25. The headspace of each
continuously stirred batch reactor was then flushed with CO2 in order to ensure
anaerobic conditions. The four continuously stirred batch reactors were then incubated
at 35°C for 40 hours. Hydrogen yields from the sucrose and grass fermentation broths
were 240.4 ml g-1 VS and 28.2 ml g-1 VS respectively.
Following incubation, the contents of each of the four continuously stirred batch
reactors were separately centrifuged at 3,500 x g for 40 minutes, and then the clarified
liquor was aspirated off and filtered to 2.5 μm. The four resulting effluents then had
8,000 mg·l-1 NaCl; 1,440 mg·l-1 Na2HPO4; 240 mg·l-1 KH2PO4; and 200 mg·l-1 KCl
added to them to minimise the conductivity gradient between the diluate and
concentrate streams ensuring the majority of ion flux was as a result of electrodialysis.
2.5 Operation of conventional electrodialysis stack
The CED stack (Figure 2) was connected to three, separate, circuits; one fed by the
electrode rinse reservoir, another by the concentrate (phosphate buffer solution)
reservoir, and another by the diluate reservoir, which contained either model solutions
or treated hydrogen fermentation broths depending on the experiment. Each circuit was
pumped through the CED stack with peristaltic pumps at a rate of 2.0 l·hr-1. Each
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reservoir was stirred with magnetic stirrers for the duration of the CED experiment.
Once the CED stack was filled with liquid, 18 V of electrical potential was applied
across the stack using an Array (Nanjing, China) 3644A programmable DC power
supply.
2.6 Sampling technique and analysis
Samples (1 ml) were taken from the concentrate and diluate reservoirs as soon as the
power supply was activated, and at ten minute intervals for 60 minutes thereafter. The
VFA content of the samples taken from the concentrate and diluate reservoirs were
measured using a headspace gas chromatograph, equipped with a flame ionization
detector and a free fatty acid phase column (Nukol), which operated at 190°C and at 14
psi with a nitrogen carrier gas according to the method of Cruwys et al. (2002). At the
same time as samples were taken from the concentrate and diluate circuits, the current
(A) flowing through the CED stack was recorded.
3. Results and discussion
3.1 CED of model solutions
In the first experiment, CED was used to reduce the concentration of acetic, propionic,
i- butyric, n-butyric, i-valeric, and n-valeric acids from model solutions. The initial
concentrations of all acids were in the range of 800 and 1,000 mg·l-1, and were reduced
consistently by up to two orders of magnitude following 60 minutes of CED, and in the
second run, acetic acid was reduced to below detectable levels for gas chromatography
(less than 10 mg·l-1) (Figure 3). The concurrent increases in the VFA concentrations of
the concentrate circuit were expected and demonstrated that ion flux progressed as
expected.
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3.2 CED of hydrogen fermentation broths from sucrose-fed continuously stirred batch
reactors
Figure 4 shows that during the CED of hydrogen fermentation broths from sucrose fed
continuously stirred batch reactors, the concentrations of acetic and n-butyric acid were
successfully reduced by at least 92%, and the majority of removal occurred during the
first 30 minutes. In both instances, acetic acid was removed entirely.
3.3 CED of hydrogen fermentation broths from grass pellet fed continuously stirred
batch reactors During the CED of grass reactor hydrogen fermentation broths the acetic
and n-butyric acid concentrations were successfully reduced by up to 96%, with the
fastest rate of reduction occurring in the initial 30 minutes (Figure 5). The removal of
other VFAs is not presented as they were not present in concentrations greater than 40
mg·l-1 following dark hydrogen fermentation.
As demonstrated by the conventional electrodialysis of model solutions (Figure 3), it is
possible to reduce an initial acetic acid concentration by around 1,000 mg·l-1, and
although the n-butyric acid concentration of the diluate circuit (hydrogen fermentation
broths from grass fed continuously stirred batch reactors) is initially lower than in the
model solutions, it was still possible to reduce the concentration from 642 mg·l-1 to 18
mg·l-1. Concurrently, the concentrate circuit becomes more concentrated with acetic and
n-butyric acid, illustrating the ion flux from the diluate circuit to the concentrate circuit.
3.4 Comparing percentage reduction in VFA concentrations
Table 1 shows that in terms of percentage reduction, there is little difference between
the ability of conventional electrodialysis to treat model solutions and hydrogen
fermentation broths. Mean acetic acid concentration reduction is 98% in model
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solutions (from 1,031 mg·l-1 to 20 mg·l-1), more than 99% in sucrose fed reactor broths
(753 mg·l-1 to less than 10 mg·l-1), and 94% in grass fed reactor broths (1,189 mg·l-1 to
71 mg·l-1). It also shows that acetic acid is typically the most readily removed of the two
VFA species, except when comparing reduction data from the grass reactor
experiments, in which n-butyric acid concentration is reduced by 96% (642 mg·l-1 to 25
mg·l-1) as opposed to 94% for acetic acid (1189 mg·l-1 to 71 mg·l-1). There is a
correlation between the molarity of the different VFA species and their rates of
transport (Figure 3) suggesting that initial concentration gradient of the acid influences
the rate at which it is removed from the concentrate stream.
After 50 minutes into the CED of grass fed reactor broths, acetic acid levels in the
diluate stream increase (Figure 5). This increase was found to be statistically significant
(P=0.0406 using a Student’s T-Test). Back diffusion, a phenomenon whereby a
concentration gradient overcomes the electrical gradient and ions move against
conventional current would explain this observation (Bailly et al., 2001).
Numerous investigations into the removal of VFAs from solutions exist, however they
employ methods other than CED and there is little uniformity between the variables
tested so comparisons between methodologies are therefore difficult. For example,
Choudari et al. (Choudhari et al., 2014) use pervaporation with polyether block amide
based composite membranes to remove butyric acid of concentration 5,950 mg·l-1 from
2 l of anaerobic digestion broths. In that study, a total membrane area of 0.01591 m2
was reported to be able to remove up to 120 g·m-2·hr-1 of butyric acid, which equates to
a 23% reduction in butyric acid concentration in 60 minutes as compared to a maximum
of over 99% in this work, which represents a fourfold increase in performance. An
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advantage of polyether block amide based membranes is that less costly materials than
polymer-based membranes such as graphene can be used, but this appears to be at the
expense of removing larger amounts of VFAs, which, as discussed are extremely
valuable.
Tang et al. (Tang et al., 2014), used bipolar membrane electrodialysis to remove acetic
acid from ethanol type fermentation broths and report a reduction in acetic acid
concentration from 1,600 mg·l-1 to 110 mg·l-1 following 39 minutes of bipolar
membrane electrodialysis. Figures 3, 4, and 5 demonstrate that CED is capable of
similar rates of reduction, with the advantage that anion exchange membranes and
cation exchange membranes are less costly than bipolar membranes.
CED is a technology capable of reducing the acetic and n-butyric acid concentrations of
hydrogen fermentation broths provided that the pre-CED filtration steps outlined in this
work are taken. In moving towards an automated process, in which VFAs are removed
continuously with a view to improving hydrogen yields, it is important to establish how
effective CED is at treating hydrogen fermentation broths with fewer pretreatment steps
and if successful, to use CED to remove VFAs from hydrogen reactors as they evolve.
If this can be achieved, conventional electrodialysis represents a way in which to
increase hydrogen yields from a given dark fermentation reactor at potentially low cost.
3.5 pH levels
In this study, the aim of CED was to remove VFAs from model solutions and post-
fermentation broths, and in doing so pH levels were affected. Following CED and the
associated removal of VFAs, the model solution's pH rose from 3.03 to 3.89, the
sucrose fermentation broth's pH rose from 6.74 to 8.72, and the grass fermentation
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broth's pH rose from 6.31 to 6.48. It is known that the pH level of a hydrogen reactor
has an effect on gas yields but in these instances CED was used to treat fermentation
broths that were obtained once fermentation had been completed. Further studies will
examine the effect of VFA removal together with changes in pH on ongoing
fermentative hydrogen production.
3.6 Electrical current data
The electrical current data shown in Figure 6 follow a trend consistent with their
respective acetic and n-butyric acid reduction rates shown in Figures 3, 4 and 5. For the
grass fed and sucrose fed fermentations (Figures 4 and 5) the majority of acetic and n-
butyric acid flux had occurred by 30 minutes, and this is reflected by the sharp decrease
in current from greater than 1.5 A to roughly 0.35 A (Figure 6) during the first 20
minutes of those experiments.
The diluate circuit (Figure 2) in these experiments became gradually depleted of ions,
and this is reflected by the current data (Figure 6). As ions become retained within the
concentrate circuit, overall stack resistance increases because ions were not replaced in
the diluate circuit. If CED is used to treat hydrogen fermentation broths during
continuous dark fermentation, the likelihood is that the diluate circuit will be
replenished with acetic acid and n-butyric acid and their associated ions continuously,
resulting in a consistent electrical current during CED.
4. Conclusions
CED can reduce the acetic and butyric acid concentrations of a 250 ml diluate circuit by
over 92% from an initial concentration of up to 1,200 mg·l-1 for both acids without
bipolar membranes. VFA removal rates from CED of sucrose and grass fermentation
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broths as were similar to those from model solutions. Decreases in electrical current
within the CED stack were observed as VFAs were removed from the diluate circuit.
The ability of CED to successfully remove VFAs from fermentation broths indicates it
could be used to increase hydrogen and VFA yields during anaerobic processes and
facilitate their recovery.
Acknowledgements
The authors would like to acknowledge the support of the EPSRC Hydrogen and Fuel
Cell Consortium Funding (EP/J016454/1), University of South Wales Centenary
Scholarship Fund and the European Regional Development Fund for the
CymruH2Wales project.
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Figure 1: Configuration of CED stack used in this study. Movement of acetate and
butyrate species are shown.
Figure 2: Schematic diagram of the CED stack used in this study showing electrolyte,
concentrate and diluate circuits and reservoirs.
Figure 3: Concentration flux of individual acids in concentrate and diluate circuits
during CED of model solutions.
Figure 4: Acetic acid and n-butyric acid concentration flux in concentrate and diluate
circuits during CED of fermentation broths from sucrose fed hydrogen fermentations.
Figure 5: Acetic acid and n-butyric acid concentration flux in concentrate and diluate
circuits during the CED of fermentation broths from grass fed hydrogen fermentations.
Figure 6: The decrease in electrical current observed as the CED of model solutions,
sucrose fed continuously stirred batch reactors, and grass fed continuously stirred batch
reactors progressed.
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Table 1: Mean concentration reductions in acetic acid and n-butyric acid in diluate
circuits composed of model solutions and hydrogen fermentation broths
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Diluate circuitStandard deviation
Standard deviation
(mg·l-1) (%) (mg·l-1) (mg·l-1) (%) (mg·l-1)
Model solution 1,031 98% 33 919 95% 35Sucrose broth 753 >99% 97 722 97% 18Grass broth 1,118 94% 14 617 96% 7
Mean acetic acid concentration reduction (n=2)
Mean n-butyric acid concentration reduction (n=2)
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