Waste Management 77 (2018) 516–521

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Waste Management
journal homepage: www.elsevier.com/locate/wasman

Effect of total solid content and pretreatment on the production of lactic

acid from mixed culture dark fermentation of food waste
Ahasa Yousuf, Juan-Rodrigo Bastidas-Oyanedel ⇑, Jens Ejbye Schmidt 1
Department of Chemical and Environmental Engineering, Khalifa University of Science and Technology, Masdar Institute, Masdar City, P.O. Box 54224, Abu Dhabi, United
Arab Emirates

a r t i c l e i n f o a b s t r a c t

Article history: Food waste landfilling causes environmental degradation, and this work assesses a sustainable food val-
Received 14 May 2017 orization technique. In this study, food waste is converted into lactic acid in a batch assembly by dark
Revised 23 April 2018 fermentation without pH control and without the addition of external inoculum at 37 °C. The effect of
Accepted 25 April 2018
total solid (TS), enzymatic and aeration pretreatment was investigated on liquid products concentration
Available online 30 April 2018
and product yield. The maximum possible TS content was 34% of enzymatic pretreated waste, and
showed the highest lactic acid concentration of 52 g/L, with a lactic acid selectivity of 0.6 glactic/gtotalacids.
Keywords:
The results indicated that aeration pretreatment does not significantly improve product concentration or
Mixed culture fermentation
Food waste
yield. Non-pretreated waste in a 29% TS system showed a lactic acid concentration of 31 g/L. The results
Carboxylic acid showed that enzymatic pretreated waste at TS of 34% results in the highest production of lactic acid.
Lactic acid Ó 2018 Elsevier Ltd. All rights reserved.
Enzymatic pretreatment
Total solids content

1. Introduction and chemical industries (Agler et al., 2011; Bastidas-Oyanedel

Excessive generation of the waste is currently a major issue
worldwide due to urbanization and human population growth.
The food waste composition of the world municipal solid waste
is on average 40%, with a range from 23% to 67.5% (Hoornweg &
Bhada-Tata, 2012). According to United Nations Food and Agricul-
ture Organization (FAO), 1.3 billion tonnes of food were wasted in
2011 (FAO, 2011). If used in landfill, the high moisture and volatile
solid content of food waste can cause environmental degradation
by greenhouse gases emission, odor and ground water contamina-
tion. This situation calls for efficient resource recovery from the
food waste to both minimize the environmental issues associated,
and also create value from waste.
Dark fermentation (DF), a bioprocess, can convert the food
waste into carboxylic acids, for example lactic, propionic, butyric,
acetic, and valeric acid and solvents in the liquid phase, and bio-
hydrogen and carbon dioxide in the gas phase (Bastidas-
Oyanedel et al., 2015). The acids produced, when separated from
the broth, can be used as platform chemicals for the production
of alcohols, bio-hydrogen and bioplastics and can also be used as
pure acids in various applications including food, pharmaceutical
⇑ Corresponding author.
E-mail addresses: ahasa.yousuf@gmail.com (A. Yousuf), jbastidas@masdar.ac.ae
(J.-R. Bastidas-Oyanedel), jschmidt@masdar.ac.ae (J.E. Schmidt).
1
Post-publication corresponding author.
et al., 2015; Dahiya et al., 2015). Among the biological processes
available, dark fermentation for carboxylic acid production shows
the promise of practical viability due to its high market value in
comparison to methane, animal feed and other products obtained
from different bioprocesses (Bastidas et al., 2016;
Vanwonterghem et al., 2015). Moreover, DF is a mixed culture fer-
mentation (MCF), and therefore does not require sterile operating
conditions and has the potential to consume a wide spectrum of
substrates containing diverse organic compounds (Bastidas-
Oyanedel et al., 2015; Jankowska et al., 2015).
Dark fermentation of food waste to carboxylic acids involves a
series of biological mediated reactions under anaerobic conditions
(Aceves-Lara et al., 2008; Boe et al., 2003; Jankowska et al., 2015).
The mechanisms behind the product spectrum shifts of DF are not
yet clear (Bastidas-Oyanedel et al., 2012; Bastidas-Oyanedel et al.,
2008; Hoelzle et al., 2014; Temudo et al., 2007). A considerable
body of research has already been conducted to control and opti-
mize the product spectrum of MCF with the aid of modeling (Iwa
et al., 2001). However, these models have been made on assump-
tions and require experimental support to be applied on a complex
substrate such as food waste for optimization (Jankowska et al.,
2015). Future interest in research is focused on the maximization
of food waste utilization, without losing the specificity of produced
carboxylic acid. In this regard, Chen et al. (2017a) have maximized
the production of total volatile fatty acids with a maximum con-

https://doi.org/10.1016/j.wasman.2018.04.035
0956-053X/Ó 2018 Elsevier Ltd. All rights reserved.
 A. Yousuf et al. / Waste Management 77 (2018) 516–521
centration of acetic acid of 2.7 g/L, at 55 °C mixed culture fermen-
tation, when stepwise increasing the reaction pH from 7 to 9, using
sewage sludge as feedstock with a concentration of 2.7 g/l of total
suspended solids (approximately 0.3% TS). Chen et al. (2017b) have
also obtained high purity propionic acid (16 g/L, with 90% purity)
in a mixed culture fermentation of glucose using different levels
of ammonium.
Another important topic to investigate is the purification and
esterification of produced carboxylic acids, in order to produce
alcohols. Esterification of carboxylic acids has been studied in
organic solution using diverse catalysts then (Kaur & Ali, 2015;
Liu & Wu, 2016; Park et al., 2010; Rezende & Pinto, 2016). The main
challenge is that carboxylic acids produced by fermentation are in
aqueous solution. These aqueous solutions then need to be purified
and concentrated in an organic solvent, in order to be used in the
available esterification technologies.
Total solid (TS) content is one of the parameters that can affect
the MCF process. Several studies have been performed to evaluate
the effect of TS content on the production of methane, yet to date,
there have been no studies conducted for carboxylic acids. The
other obstacle of this promising MCF technology is low product
yield. Pre-treatment methods have been found to have a positive
influence on the yield of carboxylic acid and thus, have become a
point of interest for various researchers (Breton-Toral et al.,
2016; Liu et al., 2016; Liang et al., 2014, 2015; Yin et al., 2014;
Yu et al., 2014).
The objective of the study was to investigate the effect of TS
content on the carboxylic acids spectrum, focusing on lactic acid
from food waste. The study utilized industrial enzymes for waste
degradation and investigated its effect on the product yield. It also
investigated the effect of aerobic pretreatment, which involves the
supply of air into the waste and is aimed at increasing the growth
of microorganisms naturally present in the waste. Thus, in conclu-
sion, the study investigated the effect of TS content, and enzymatic,
and aerobic pretreatment on the product yield and product spec-
trum of the mixed culture fermentation of food waste. The exper-
iments were performed in triplicate in a batch operation in a pH
uncontrolled environment. pH uncontrolled fermentation was con-
ducted as it results in an acidic environment at the end of fermen-
tation, and makes the recovery of carboxylic acids feasible (Tang
et al., 2016; Yousuf et al., 2016).
2. Materials and methods
2.1. Food waste
Synthetic food waste was used in order to reproduce experi-
mental results. The synthetic food waste was prepared mimicking
real food waste, based on the work of Nwobi et al. (2015). It con-
tained 11% rice, 5% pasta, 7% potatoes, 2% corn, 4% bread, 1%
pineapple, 1% apple, 1% carrot, 2% cucumber, 3% lemon, 1% paw-
paw, 6% tomatoes, 3% pickles, 6% meat, 14% fish, 6% dairy, 2% cab-
bage, 2% lettuce, 2% okra, 2% eggplant, 2% cauliflower, 2% broccoli,
13% vegetable oil, 1% newspaper, 0.6% cardboard, and 0.4% A4
paper in terms of weight. The food was cut into small pieces,
cooked, and then mixed thoroughly in the weight ratio mentioned
above. Its composition, in g/100g_TS has carbohydrates, 22.93;
protein, 1.99; fats, 18.01; fibers, 2.49; ash, 4.03, as calculated by
Nwobi et al. (2015). A large quantity of food was prepared and then
stored at 4 °C, to prevent spoilage.
2.2. Batch fermentation
Batch fermentation experiments were performed in triplicate
and were carried in 500 mL glass bottles. After adding the corre-
517
sponding food waste, the bottles were flushed with nitrogen gas
to obtain anaerobic conditions. Bottles were capped with rubber
stoppers and brewing airlocks. The initial pH for the food waste
was found to be 4.4 ± 0.1. The bottles were kept at 37 °C, in an orbi-
tal shaker at a stirring speed of 120 rpm, without pH control, for 7
days. No external inoculum and nutrients were added.
2.3. Effect of total solid content on food waste fermentation
The experiments were performed in semi-dry and dry condi-
tions. In general, wet reactors have <10% TS, semi-dry with (10–
20% TS) and dry with (>20% TS) (Pognani et al., 2009). The experi-
mental conditions to investigate the effect of percentage of total
solid were categorized into three sets: (1) Semi-dry fermentation
with the total solids of 19.0 ± 1%; (2) Dry fermentation with the
total solids in a range of 29.0 ± 1%; and (3) Extreme dry fermenta-
tion with the total solids of 34% ± 1%. This was the maximum pos-
sible TS content, as the food waste prepared had an approximate TS
content of 34% and the remaining 64% was water present naturally
in the waste. The extreme dry fermentation was only investigated
for enzymatic pre-treated waste. The extreme dry fermentation
condition was not possible to be tested for any other condition
due to extreme dry environment, sampling was difficult because
of absence of free fluids. A fixed amount of food waste, 100 g,
was added in all the bottles, and then diluted with variable amount
of water to achieve TS content of 19 ± 1%, 29 ± 1% and 34 ± 1%. The
total solid concentration of the different TS fermentation was, in g
TS/L: 180.0, 243.7 and 284.34 for 19.0 ± 1%, 29.0 ± 1% and 34.0 ± 1%
of TS, respectively. The batch fermentation was performed as
described in Section 2.2.
2.4. Effect of enzymatic pretreatment
The enzymes were obtained from Novozymes A/S Bagsværd,
Denmark. The mixture of enzymes contained in weight basis,
34.0% cellulase, 37.0% amalyse, 6.8% hemicellulose, 7.1% pectate
lyase, 7.3% lipase and 7.4% protease. The enzymes codes as pro-
vided by the manufacturer are cellulase NS81210, amalyse
NS81217, hemicellulase NS81233, pectate lyase NS81215, lipase
NS81022 and protease NS81220 (Kolbl & Stres, 2016). For all the
experiments performed, 1.631 g enzymes mixture/100 g of food
waste was used, as suggested by (Nwobi et al., 2015). This ratio
was selected based on the manufacturer’s (Novozymes A/S, Den-
mark) recommended loading range.
The enzymatic hydrolysis was carried out in dry conditions
with a TS content of 29% and extremely dry conditions with a TS
content of 34%. Enzymatic hydrolysis was carried out at 50 °C, as
per manufacturer’s recommendation, for 24 h in an orbital shaker
at 120 rpm. After enzymatic hydrolysis, batch fermentation was
conducted as described in Section 2.2. The total process time was
seven days, with enzymatic hydrolysis conditions for one day
and batch fermentation for six days.
2.5. Effect of aeration pretreatment
The effect of aeration pretreatment was performed using an air
pump with a constant flow rate of 1.5 L/min. Air was sparged at the
bottom of the glass bottles (as in Section 2.2) containing food
waste for 24 h. During the aeration, the glass bottles were placed
in a water bath at 37 °C. Aeration was performed without any addi-
tion of specific inoculum. Aerobic conditions would activate the
growth of aerobic and/or facultative microorganisms present natu-
rally in the food waste. Batch fermentation, as described in Sec-
tion 2.2, was performed after the aeration pretreatment. The
total process time was seven days, with aeration pretreatment con-
518 A. Yousuf et al. / Waste Management 77 (2018) 516–521
ditions for one day and batch fermentation for six days. Aeration
pretreatment was performed on a total solid content of 19%.
2.6. Analytical methods
The TS was determined according to standard methods (APHA,
1995). Liquid samples from the different batch fermentation were
first centrifuged for 5 min at a speed of 20,238 rcf, and filtered
through 0.45 mm pore size. The filtered samples were then used
for HPLC and Total Soluble Chemical Oxygen Demand analysis.
The concentrations of lactic acid, acetic acid, propionic acid,
butyric acid, iso-butyric acid, valeric acid, iso-valeric acid, ethanol,
and glucose, were measured by 1260 HPLC (Agilent Technologies,
USA) using an Agilent Hi-Plex H column (65 °C), UV detector at
210 nm for organic acids and RID detector at 35 °C for ethanol
and glucose. The mobile phase was 5 mM H2SO4 with a flow rate
of 0.6 mL/min, and external standards were used for calibration.
The HPLC equivalent COD results were calculated using their
respective COD conversion factors, in g COD/g compound: lactic
acid 1.08, acetic acid 1.08, propionic acid 1.53, butyric and iso-
butyric acid 1.84, valeric and iso-valeric acid 2.06, ethanol 2.02,
and glucose 1.067 (Bonk et al., 2015).
Filtered samples were also used to measure the total soluble
chemical oxygen demand (SCOD), using LCK 014 (range 1000–
10000 mg/L O2) cuvettes by Hach Lange GmbH. After incubation
in a Hach Lange HT 200S digestor, the soluble chemical oxygen
demand (SCOD) was measured using a Hach Lange DR 2800
spectrophotometer.
The HPLC equivalent COD results and the total SCOD results
were compared. It is expected that the HPLC equivalent COD is
equal or lower than the total SCOD value. When the value is lower,
it indicates the presence of undetectable HPLC components.
3. Results and discussion
3.1. Effect of TS content
Fig. 1 presents the dark fermentation liquid product concentra-
tion for the 19%TS and 29%TS conditions. For 19%TS condition,
products corresponded to approximately 61% lactic acid (19.56 g/
L), 8.3% to acetic acid (2.65 g/L), 6.2% to propionic acid (2.0 g/L),
4.9% iso-butyric acid (1.57 g/L), 1.8% of butyric acid (0.59 g/L),
3.1% of valeric acid (1.01 g/L), 7% of iso-valeric acid (2.25 g/L),
and ethanol (2.19 g/L). This makes a total liquid product concentra-
tion of 31.86 g/L for semi dry fermentation.
For the dry environment, i.e. 29%TS, the total concentration of
liquid products was around 43.32 g/L. Lactic acid accounted for
72% (31.2 g/L) of the total metabolites. Acetic acid is the second
dominant metabolite with 2.9 g/L, the concentration of propionate
did not change, 2 g/L, when increasing the TS content. The concen-
tration of butyrate increased from 2.1 to 2.6 g/L as TS content
increased, again, the concentration of valerate (both valeric and
iso valeric acid) increased from 3.27 g/L to 4.0 g/L as TS content
of the system increases. The total product yield of liquid products
from food waste in the semi dry, 19%TS, and dry condition, 29%TS,
was 0.18 gprod/gTS and 0.17 gprod/gTS, respectively.
The impact of increasing TS from 19% to 29% resulted in around
a 36% increase in the concentration the total liquid fermentation
products, however, the product spectrum and the total liquid pro-
duct yield was similar. Therefore, decreasing water input in the
beginning could make downstream processing simple and
efficient.
An increase of TS from 19% to 29% has positive effects on the
concentration and yields of the total liquid dark fermentation
products. However, this fact does not seem to agree with previous
50
45
40
35
Concentration (g/L)
19% Total solids
30
25
29% Total Solids
20
15
10
5
0
Acetic acid
products
Propionic
Ethanol
Valeric acid
Butyric acid
Lactic acid
Total
acid
Fig. 1. Fermentative Product Distribution after 7 days of fermentation at different
TS condition, at temperature 37 °C, without pH control, without inoculum, without
pretreatment.
literature, where it is believed that increasing water content, i.e.
decreasing TS, provides a homogeneous environment and
improves the accessibility of microorganisms to substrates, result-
ing in a higher conversion. Staley et al. (2011) suggested that
higher solid content creates a depletion zone at the microscopic
level, having no microbial activity. These depletion zones result
in lower degradation of the substrate and thus lower conversion
rate.
At 19%TS the HPLC equivalent COD was 41.6 g-COD/L, while the
measured total SCOD was 42.8 g-COD/L, corresponding to a COD
balance of 97.3%, and an HPLC equivalent COD over measured total
SCOD. At 29%TS, the HPLC equivalent COD was 53.2 g-COD/L, and
the measured total SCOD was 54.4 g-COD/L, with a COD balance
of 97.8%. The results were similar confirming the accuracy of the
results.
3.2. Effect of enzymatic pretreatment
Hydrolysis is the rate-limiting step in dark fermentation, and
thus an efficient pretreatment method can help to improve food
digestibility and the product yield (Aceves-Lara et al., 2008).
Fig. 2 presents the product spectrum obtained from the enzymati-
cally pretreated food waste at different TS content. For dry condi-
tions, for example, at TS of 29%, there was 31% increment in the
total concentration of carboxylic acids in comparison to the non-
enzymatically-pretreated waste. The total liquid product was
43.3 g/L of non-pretreated food waste. and 63 g/L from pretreated
waste. The product yield improved from 0.18 gprod/gTS to 0.259
gprod/gTS. The concentration of lactic acid was 44.2 g/L (41% higher)
and propionic acid was 9.3 g/L.
The extreme dry fermentation condition, specifically at 34%TS,
resulted in a product yield of 0.28 gprod/gTS, the highest observed
so far. The total liquid product concentration was found to be
82.1 g/L, with a lactic acid concentration of 52.5 g/L, followed by
propionic acid, 17.7 g/L, acetic acid, 2.8 g/L. The HPLC equivalent
COD and total SCOD, for 29%TS, were 89.6 g-COD/L and 113 g-
COD/L, respectively, representing a COD balance of 79%. At 34%TS
the results were 121 g-COD/L and 167 g-COD/L, respectively, with
a COD balance of 72%.
The COD of enzymes was unknown and thus, this COD was not
included in the calculation of theoretical COD. The difference in
theoretical and measured COD with 29% TS is smaller and could
 A. Yousuf et al. / Waste Management 77 (2018) 516–521 519

90 and 0.7 glactic/gtotalacid, lower than the optimum desirable value of

0.9 glactic/gtotalacid. Further investigation of the effect of different
80 29% Untreated Total Solids
parameters and their control could help to achieve high selectivity
70
of single acid in a mixed culture environment.
29% Total Solids Enzymatically
Table 1 compares the maximum lactic acid concentration
pretreated
60 obtained in this study with similar studies using mainly food
34% Total Solids Enzymatically
Concentration (g/L)

waste. As a summary, the maximum lactic acid concentration in

50
pretreated
this study, 52 g/l, was obtained using a non-externally inoculated
mixed culture fermentation, i.e. using the indigenous microbiota
40
present in the non-sterile feedstock (food waste), where the feed-
30 stock was treated by enzymatic hydrolysis, and the fermentation
was performed in a batch uncontrolled pH mode, in the pursue
20 of developing a process with a level of sophistication according
to the feedstock used, food waste, and the product sought, an
10
organic acid with a market price of 1000–2100 USD/tonne
0
(Bastidas-Oyanedel et al., 2016). Liang et al. (2014) has obtained
a maximum concentration of 15 g/l of lactic acid, with a selectivity
Propionic
products

Valeric acid

Ethanol
Acetic acid

Butyric acid
Lactic acid
Total

acid

of 0.66 glacticacid/gtotalproducts, using a very similar approach, i.e.

mixed culture fermentation, in batch uncontrolled pH mode. The
most significant difference is that their feedstock has been steril-
Fig. 2. Effect of Enzymatic Hydrolysis on the production of carboxylic acids from ized. Better results, i.e. 39 g/l of lactic acid where obtained by
food waste at TS of 29% and 34% after 7 days of fermentation, temperature 37 °C, pH Tang et al. (2016) and Tashiro et al. (2016). In both approaches
un-control, without inoculum.
the feedstock was not sterilized, as in the present study, but the
fermentation pH was controlled in the range of 6–7. When com-
be because of enzymes. However, the difference at a higher TS was paring these mixed culture approaches with pure culture fermen-
slightly higher, and this could be because of the presence of tation, the maximum lactic acid concentration achieved by Kwan
polysaccharides along with the enzymes. While this may be the et al. (2016) was 94 g/l, using a Lactobacillus casei Shirota, filter
reason, as yet, experiments have not been conducted to confirm sterilized food waste, and pH controlled at 6. Nguyen et al.
this correlation. (2013) obtained a maximum of 186 g/l of lactic acid using a Lacto-
The enzymatic pretreatment of food waste improved the total bacillus coryniformis with non-sterile hydrolyzed fresh sweet
liquid product concentration and yield, in comparison to the sys- potato, and pH controlled at 6. This encourage the study of mixed
tem without enzymatic pretreatment. The system which had the culture fermentation to achieve similar results obtained with pure
TS of 34% was able to produce a higher concentration of acids, in culture fermentation.
comparison to all the previous experiments. Secondly, the product
yield was also improved. For this system, along with lactic acid, 3.3. Effect of aeration pretreatment
propionic acid was the second dominant component. The impor-
tant thing that should be noted here is the selectivity of lactic acid. Fig. 3 presents the liquid product concentration obtained from
Though the experiments were targeted to produce a mixture of aerobically pretreated food waste. The product spectrum is similar
carboxylic acids, the downstream processing of these mixed acids to the experiment without aeration pretreatment and concentra-
could be costly. The selectivity of lactic acid ranges between 0.4 tion is higher, around 18% increment is observed with aerated food

Table 1
Maximum lactic acid concentration produced using food waste as feedstock.

Lactic acid
Feedstock System Max. conc. Yield Selectivity Reference
(g/L) (gLactic/gTS) (gLactic/gtotalprod)
Food waste hydrolysed by Mixed culture fermentation using feedstock indigenous 52 0.18 0.64 This study
an enzymatic cocktail microbiota (non sterilized feedstock). Uncontrolled pH
mode. Temperature controlled at 37 °C
Potato peel waste Mixed culture fermentation using activated sludge from 15 0.22 0.66 Liang et al. (2014)
a municipal wastewater treatment plant. Batch mode.
Sterile-gelatinized feedstock. Uncontrolled pH mode.
Temperature controlled at 35 °C
Food waste Mixed culture fermentation using feedstock indigenous 39 0.85 Tang et al. (2016)
microbiota (non sterilized feedstock). Continuous mode,
OLR 18, using pH and temperature controlled at 6.0 and
37 °C, respectively
Food waste Mixed culture fermentation using compost as 39 1.38 Tashiro et al. (2016)
fermentation seed. Batch mode. Non sterilized feedstock,
pH and temperature controlled at 7.0 and 50 °C,
respectively
Food waste hydrolysed by Lactobacillus casei Shirota. Batch mode. Filter sterilized 94 0.94 Kwan et al. (2016)
A. awamori and A. oryzae food waste hydrolysate, pH and temperature controlled
at 6.0 and 37 °C, respectively
Fresh sweet potato hydrolysed Lactobacillus coryniformis. Batch mode. pH and 186 0.85 Nguyen et al. (2013)
by an enzymatic cocktail temperature controlled at 6.0 and 37 °C, respectively
520 A. Yousuf et al. / Waste Management 77 (2018) 516–521

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