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Accepted Manuscript

Title: Valorization of organic residues for the production of


added value chemicals: A contribution to the bio-based
economy
Author: Daniel Pleissner Qingsheng Qi Cuijuan Gao Cristina
Perez Rivero Colin Webb Carol Sze Ki Lin Joachim Venus
PII:
DOI:
Reference:

S1369-703X(15)30131-5
http://dx.doi.org/doi:10.1016/j.bej.2015.12.016
BEJ 6367

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Biochemical Engineering Journal

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30-7-2015
16-12-2015
20-12-2015

Please cite this article as: Daniel Pleissner, Qingsheng Qi, Cuijuan Gao, Cristina Perez
Rivero, Colin Webb, Carol Sze Ki Lin, Joachim Venus, Valorization of organic residues
for the production of added value chemicals: A contribution to the bio-based economy,
Biochemical Engineering Journal http://dx.doi.org/10.1016/j.bej.2015.12.016
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Valorization of organic residues for the production of added value


chemicals: A contribution to the bio-based economy
Daniel Pleissner1, Qingsheng Qi2, Cuijuan Gao2,3,4, Cristina Perez Rivero5, Colin Webb5,
Carol Sze Ki Lin4, Joachim Venus1*
1

Department of Bioengineering, Leibniz Institute for Agricultural Engineering Potsdam-

Bornim, Potsdam, Germany


2

State Key Laboratory of Microbial Technology, Shandong University, Shanda Nanlu, Jinan

250100, Peoples Republic of China


3

School of Life Science, Linyi University, Linyi, 276005, Peoples Republic of China

School of Energy and Environment, City University of Hong Kong, Tat Chee Avenue,

Kowloon, Hong Kong


5

Satake Centre for Grain Process Engineering, School of Chemical Engineering and

Analytical Science, The University of Manchester, PO Box 88, Manchester M60 1QD,
United Kingdom

*Corresponding author: Joachim Venus, Department of Bioengineering, Leibniz Institute for


Agricultural Engineering Potsdam-Bornim, Potsdam, Germany, Mail: jvenus@atbpotsdam.de, Tel: +49 331 5699 112, Fax: +49 331 5699 849

Abstract
Establishing of a bio-based and green society depends on the availability of inexpensive
organic carbon compounds, which can be converted by microbes into various valuable
products. Around 3.7 109 t of agricultural residues and 1.3 109 t of food residues occur
annually worldwide. This enormous amount of organic material is basically considered as
waste and incinerated, anaerobically digested or composted for the production of heat, power
or fertilizers. However, organic residues can be used as nutrient sources in biotechnological
processes. For example, organic residues can be hydrolyzed to glucose, amino acids and
phosphate by chemical and/or biological methods, which are utilizable as nutrients by many
microbes. This approach paves the way towards the establishment of a bio-based economy
and an effective organic residues valorization for the formation of bio-based chemicals and
materials. In this review, valorization of organic residues in biotechnological processes is
presented. The focus is on the production of three industrially important added value
chemicals, namely succinic acid, lactic acid and fatty acid-based plasticizer, which have been
used for the synthesis of environmentally benign materials and food supplements.
Furthermore, utilization strategies of residues coming from fruit and vegetable processing are
introduced.

Keywords: Succinic acid, Lactic acid, Fatty acids, Bio-plasticizer, Agricultural residues,
Food residues, Vegetable residues

Introduction
Due to the finiteness and environmental impacts of fossil oil, bio-based chemicals have been
considered as sustainable alternatives to petroleum-based chemicals in chemical reactions. It
is particularly the diversity of biochemical pathways of microbes that allows the
biotechnological production of a wide range of industrially relevant bio-based chemicals [1].
The cost-efficient realization of biotechnological processes depends on the presence of
inexpensive nutrients, to be used as carbon, nitrogen and phosphate sources for microbes [2].
Pure nutrients (e. g. glucose, amino acids and phosphate), however, are expensive and make
most of the developed biotechnological processes economically unfeasible.
It was estimated that 3.7 109 t of agricultural residues is produced annually as by-products
by agricultural industries worldwide [3]. Agricultural residues consist of around 40%
cellulose, 30% hemicellulose, 20% lignin, 5% proteins and 5% minerals [4]. In total, it was
estimated that 1,376 106 t cellulose and 848 106 t hemicellulose occur globally every year
[3]. Due to the recalcitrant structure of agricultural residues, tough processes, such as
hydrothermal treatment or chemical hydrolysis in combination with the use of enzymes are
needed for depolymerization and sugar recovery. The released C5- and C6-sugars can then be
used as carbon sources in biotechnological processes [5-9]. Furthermore, it was estimated that
one third of the food produced globally for human consumption is wasted every year. The
overall amount of food wasted corresponds to around 1.3 109 t [10, 11]. A composition of
30-60% starch, 5-10% proteins and 10-40% (w/w) lipids constitutes food residues a
promising feedstock in biotechnological processes [12-14]. Recovery of nutrients from food
residues in the form of carbon, nitrogen and phosphorous compounds can be performed by
chemical and biological/enzymatic methods after solubilization of the waste matter [15-19].
Even though the technologies for organic residues valorization are known, the potential of
organic residues as nutrient sources in biotechnological process for the establishment of a
bio-based economy has not been fully exploited.

The concept of circular economy considers the reuse and recycling of any types of waste. In
this aspect, the utilization of organic residues in biotechnological process for the production
of value added chemicals would enable an application of the circular economy concept on
organic waste management and contribute to the development of a bio-based economy.

Within the circular economy, the cascading use of biomass is particularly important, as it
considers the production of food and feed prior to material and energetic usage [20].

The current options for the valorization of waste organic residues are shown in Table 1. The
options range from the production of antioxidants, flavonoids, enzymes and proteins, fatty
acid methyl esters, glycerol and erucic acid from fruits and vegetables, animal waste, meat
and derivatives, waste oil and dairy products [21-23]. Lignocellulosic biomass has also been
used for the production of various compounds, such as phytosterols, polypropylene, acrylic
acid and esters [23]. Furthermore, lignin has been used as substrate for the production of
polyhydroxyalkonates and adipic acid [24, 25]. It should be indicated here that the metabolic
versatility of microbes enables the fermentative production of a wide range of products.
Figure 1 shows relevant industrial metabolites obtainable via fermentative processes [1]. The
products range from amino acids, such as aspartate and lysine, carboxylic and dicarboxylic
acids, such as lactic acid and succinic acid, and polyhydroxyalkanoates. Furthermore,
microorganisms are able to synthesize long carbon chains in form of fatty acids. It should be
admitted that the metabolic versatility of microbes opens not only the door to the
development of biotechnological processes for the production of value-added chemicals, but
also to innovative treatment strategies of organic residues.

The aim of this review is to give an introduction to biotechnological utilization strategies of


organic residues, including biochemical principles and strain development, for the production
of three added value chemicals, namely succinic acid, lactic acid and bio-based plasticizer.
These chemicals are highly wanted feedstocks in chemical reactions by chemical industry for
the synthesis of environmentally benign materials. Similarly, there is great demand of
succinic acid and lactic acid by food industry as food supplements [26-28]. An integrated
bioprocess for the simultaneous production of succinic acid, lactic acid and fatty acid-based
plasticizer from food waste is introduced. The simultaneous production of materials and food
supplements from organic residues contributes to the principle of cascading use of biomass.
Furthermore, valorization strategies of residues from fruit and vegetable processing are
presented.

Succinic acid
Succinic acid, a member of the C4-dicarboxylic acid family, is an important platform
chemical and was identified as one of the top twelve potential chemical building blocks for
4

the future by the US Department of Energy [29]. It can be used to produce various high value
commodity derivatives for industrial applications, such as pharmaceutical, food, antibiotics,
surfactants and detergents [30, 31]. Recent estimates of the market potential of succinic acid
and its immediate derivatives were projected to be as much as 245,000 t per year,
manufactured at industrial scale mainly by catalytic hydrogenation of petrochemically
derived maleic acid or maleic anhydride [32, 33]. In the past decade, an exciting movement
towards bio-based chemicals has been prompted from fossil feedstock to renewable raw
materials due to the declining reserves of fossil feedstock and the environmental impacts of
oil-based industries [34, 35].

Succinic acid is an intermediate of the tricarboxylic acid (TCA) cycle and a fermentation endproduct, which has been found to be produced naturally by a number of microbes including
Actinobacillus

succinogenes,

Anaerobiospirillum

succiniciproducens,

Mannheimia

succiniciproducens and Bacteroides fragilis [36-39]. Most of the succinic acid producing
strains were isolated from rumen, are anaerobic or facultative anaerobic and capnophilic. In
order to create economically feasible bio-based succinic acid production processes, rational
strain development by metabolic engineering is crucial. However, natural succinic acid
producers usually lack of genetic tools. Furthermore, many of them are even conditional
pathogenic bacteria and grow slowly, which make them inappropriate for industrial succinic
acid production [40]. Consequently, there is a demand for a faster and cheaper development
of new production strains, which preferably can utilize renewable resources [1]. In order to
overcome this drawback, researchers focused on genetically modified non-natural producers,
such as Escherichia coli and yeasts. Table 2 presents a summary of fermentative succinic
acid production from conventional media and organic residues using genetically modified
and wild type strains. Some of the renewable feedstocks tested (e.g. bread wastes and other
types of food waste) achieved similar results to those obtained from conventional media, with
a productivity over 1 g L-1 h-1 and a yield of 0.8 g SA g-1 glucose. As shown in Table 2, the
pretreatment of food waste can be carried out by in-situ enzymatic hydrolysis, which is a
relatively simple approach compared to the traditional chemical pretreatments required to
make carbon compounds available from lignocellulosic materials.

Three different biochemical strategies for succinic acid production: the reductive TCA
pathway, the oxidative TCA pathway and the glyoxylate shunt exist (Figure 2). The
maximum theoretical yield of 1.7 mole succinic acid per mole glucose can be obtained from
5

the reductive TCA pathway. However, only 1 mole succinic acid per mole glucose can be
obtained from the oxidative TCA pathway and the glyoxylate shunt [41]. The latter two
strategies can provide more energy, which is vital for cell growth and maintenance. Recently,
Li et al. designed and developed a novel whole-phase succinic acid fermentation strategy in
engineered E. coli that makes all these three pathways work under aerobic, microaerobic and
anaerobic conditions by depressing the inhibition of low dissolved oxygen, eliminating the
NADH competitive pathways, modulating the redistribution of metabolic flux and increasing
the transport rate of the sole carbon source, glucose [42]. By employing this strategy, the
engineered E. coli strain YL106/pSCsfcA was able to produce 85.3 g L-1 succinic acid after
40 hours of cultivation.

The major drawback of using microbes in succinic acid production is the decrease in pH of
fermentation media as a result of succinic acid formation. In order to keep microbes active,
the pH of media needs to be controlled by adding a base. As a consequence, succinate salts
are formed and subsequent separation of salt ions needs to be carried out after fermentation in
order to produce pure succinic acid. This is neither practical nor efficient in large-scale
fermentation processes and leads to increased operating costs. Therefore, yeasts have been
explored recently for succinic acid production, which can operate at low pH. This approach
prevents bacterial contamination and reduces the amount of additives needed for pH
regulation and consequently benefits to downstream processing [40]. By redirecting the
carbon flux towards the glyoxylate cycle, this acid tolerant Saccharomyces cerevisiae strain
produced 3.62 g L-1 succinic acid at a yield of 0.11 mole mole-1 glucose in shake flask
cultures [40]. Furthermore, the reductive pathway was constructed in S. cerevisiae by
overexpression of pyruvate carboxylase PYC2p, cytosolic retargeted MDH3p, FRDS1p and
E. coli FumCp, combined with gene deletion of pdc1, pdc5, pdc6, gpd1and fum1 [43]. The
engineered strain produced 13 g L-1 succinate at a yield of 0.2 mole mole-1 glucose at pH 3.8
in a bioreactor. However, further strain development is needed in order to increase
productivity.

Reactor design and operation of succinic acid fermentation are likely to become more
important with the prospect of bulk scale production on the horizon. Continuous production
of succinic acid is likely to outperform batch processing, especially when considering the
projections of future processing quantities. To date, the number of studies on continuous
succinic acid producing cultures is limited. On the other hand, a continuously stirred tank
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reactor has the disadvantage of cells washout, which means that the steady-state succinic acid
production is difficult unless the residence time is very long. Urbance et al. [44] reported high
productivities (up to 8.8 g L-1 h-1) by A. succinogenes, where a special polypropylene
composite support was used to enhance cell immobilization. However, the results are
scattered with low succinic acid yields at high productivities. Apart from normal suspended
cell systems, cell recycling systems using membranes were used in an attempt to enhance
productivity [45].

Fibrous bed bioreactor (FBB) with cell immobilization has been reported with the advantages
of achieving high cell density and long term stability in continuous succinic acid fermentation
with high productivity [46, 47]. According to Yan et al. [46, 47] and Li et al. [48], cotton
was used as the packing bed for cell immobilization for continuous succinic acid and butanol
fermentations, respectively. Spirally wound cotton towel has a porosity over 95%, which
enables the formation of an external recycle biofilm. During continuous fermentation, the
bacterial cells attached onto the fibrous matrix are continuously replenished, which results in
constant cell viability and biomass in a FBB. The advantages of using cotton as
immobilization material are: (i) chemically inert and not harmful to cells; (ii) good mass
transfer performance; (iii) higher cell recovery; (iv) low cost; (v) simple operation and
suitable for mass production; (vi) high mechanical strength and long service time. Recent
research conducted by our group focused on evaluation of the feasibility for using
agricultural residues, such as cotton stover, corn bran and wheat straw, as immobilization
materials in a FBB. We aim to obtain a similar or even better FBB operation stability and cell
viability during continuous succinic acid fermentation as compared to the performance in the
typical materials, such as wound cotton towel.

Food waste can be defined as a by-product or residues of food processing by industries and
consumers, which has not been recycled or used for other purposes. Examples of typical
sources of wasted food are households, institutions, schools, restaurants, grocery and bakery
stores, which create complex organic waste streams. More recently, research has appeared
switching to the use of food and agricultural wastes as feedstock for fermentative succinic
acid production. Our group previously demonstrated that succinic acid can be produced using
waste bread as the sole nutrient source [49]. Solid-state fermentation was performed to
produce enzyme mixtures of -amylase and protease for the hydrolysis of bread waste instead
of using commercial available enzymes, which resulted in over 100 g L-1 glucose and 490 mg
7

L-1 free amino nitrogen (FAN). This hydrolysate derived from waste bread was used in A.
succinogenes fermentations, which led to the production of 47.3 g L-1 succinic acid with a
yield of 1.16 g succinic acid per g glucose and productivity of 1.12 g L-1 h-1. This corresponds
to an overall yield of 0.55 g succinic acid per g bread, which is the highest succinic acid yield
compared to other food waste-derived media. Yu et al. [50] examined the feasibility of using
corncob as feedstock in succinic acid fermentation by A. succinogenes. By adding yeast
extract as nitrogen source and MgCO3 for pH control, a total of 23.6 g L-1 of succinic acid
was produced with a yield of 0.58 g g-1 sugar without any detoxification of corncob
hydrolysate. Meanwhile, lignocellulosic biomass derived from corn stover and pinewood was
adopted for succinate production using A. succinogenes 130Z and E. coli MG1655. In order
to produce utilizable carbon sources from lignocellulosic biomass, a pretreatment step is
required which converts the cellulose and hemicellulose fractions into C5 and C6 sugars, and
avoids the formation of inhibitory compounds such as aldehydes. After pretreatment of the
lignocellulosic biomass with 1-allyl-3-methylimidazolium chloride ionic liquid (AmimCl)
and enzymatic hydrolysis, succinic acid production reached 20.7 g L-1, with an average yield
of 0.37 g per g of biomass [51].

Stringent waste regulations worldwide are pushing local companies and sectors towards
higher sustainability standards. The development of novel strategies for food waste utilization
is economically and environmentally sound. Food waste utilization contributes to a solution
of the waste issue, at the same time it represents an inexpensive nutrient source for
biotechnological processes and contributes to the bio-based economy [52]. For instance, Y.
lipolytica can utilize hydrophobic substrates such as fatty acids, lipids and alkanes and simple
carbon sources, such as glucose and glycerol, which can all be found in food waste. This
broad range of substrate makes Y. lipolytica a promising candidate for the degradation and
valorization of food waste, and for the production of organic acids, such as citric and ketoglutaric acids.

Recently, Y. lipolytica was shown to be able to produce succinic acid [53]. Using a
recombinant strain of Y. lipolytica, 25 g L1 succinic acid and a volumetric productivity of
0.15 g L1 h1 under oxygen limitation were obtained [54]. Another approach in order to
produce succinic acid using Y. lipolytica was presented and based on the deletion of gene
encoding subunit of the succinate dehydrogenase [55]. The created strain named Y-3314
produced 45 g L-1 succinic acid in shake flasks containing CaCO3 as buffer and 126 g L-1
8

glycerol as carbon source. The outcomes indicate that the application of genetically modified
Y. lipolytica has promising potential for succinic acid production. However, further strain
development is needed in order to increase volumetric productivity and yield.

Only few studies have been reported for fermentative succinic acid production from wastes
[56, 57]. Therefore, in order to develop innovative food waste utilization strategies, our
current research supported by the General Research Fund from the Hong Kong Research
Grants Council, focuses on the construction of an engineered Y. lipolytica strain to degrade
mixed restaurant food waste and to produce succinic acid and polyhydroxyalkanoates
simultaneously at high productivities and yields.

Lactic acid
Lactic acid (2-hydroxypropionic acid) is one of the most promising platform chemicals,
which can be produced biotechnologically. The food, cosmetic, pharmaceutical and chemical
industries have been using lactic acid in many applications, such as pH regulation,
antimicrobial agent, green solvent and cleaning agent [58]. Furthermore, lactic acid gained
significant attention as a monomer to be used in the production of the biodegradable plastic,
poly(lactic acid), which has the potential to substitute considerable amounts of petroleumbased plastics in the future [26, 59, 60]. Thus, lactic acid is not only an industrially relevant
platform chemical, but also an important product for the bio-based economy. In 2013, the
demand of lactic acid was estimated at 714,000 t. It is expected that the demand further
increases at an annual rate of 15.5% between 2014 and 2020, which is mainly based on the
demand of bio-plastic [61-63].

Lactic acid is produced biotechnologically using several microbes, including bacteria, fungi,
yeast, cyanobacteria and algae [61]. The fermentative lactic acid production has a long
history and was first carried out at industrial scale in 1881 [64]. Nowadays, bacteria
belonging to the groups of Lactobacillus, Bacillus, Lactococcus, Streptococcus, Pediococcus
and Enterococcus, and filamentous fungi, such as Rhizopus oryzae are used as production
strains, which are able to efficiently convert hexoses, but also pentoses into lactic acid [9, 6577]. A comparison of lactic acid production from conventional media and low-cost
feedstocks is shown in Table 3. Yields obtained using lignocellulosic materials vary from
0.5-0.9 g g-1. Food waste is an advantageous substrate for lactic acid production as the supply
of additional nutrients, such as carbon and nitrogen compounds, in order to stimulate cell
9

growth and metabolic activity is unnecessary. Lactic acid fermentation is carried under
anaerobic or microaerobic conditions. Under these conditions, biomass formation is restricted
and most of the carbon consumed is used in lactic acid formation. Thus, the yield of lactic
acid is generally high and up to 0.9 g lactic acid per g glucose can be obtained in practice [73,
78, 79]. The simplicity of the biochemical pathway from glucose to lactic acid additionally
favors high yields (Figure 2). Basically, two moles of lactic acid can be produced from 1
mole of glucose. However, despite high yields, the costs of carbon (e. g. glucose) and
nitrogen (e. g. yeast extract) compounds, to be used as nutrient sources in fermentations, are
high and challenge the economic feasibility of the industrial production of the rather
inexpensive product lactic acid [79, 80]. Therefore, the recent research focus is on making
organic residues available as inexpensive nutrient sources, with the goal to develop costefficient fermentation processes.

Several organic residues were successfully investigated as nutrient sources, such as starchy
and lignocellulosic materials from agricultural industry, nitrogen-rich grass press juice and
food waste [78, 81-83]. It should be admitted here, that the yields of lactic acid in these
studies were similar to the yields obtained when defined media were used in fermentations.

Recently, the possibility of fermentative lactic acid production using barley hydrolysates,
green press juice from alfalfa and salts in batch cultures and continuous cultivation with
biomass retention of Lactobacillus paracasei was investigated [84]. Batch and continuous
cultivations were carried out at 40.5 C and pH 6.0. Both values were found to be appropriate
in order to achieve high volumetric lactic acid productivities and yields. L. paracasei
converted 90% of the supplied glucose into lactic acid and more than 100 g L-1 lactic acid
was produced in a batch culture within 30 hours. The process was thereafter performed as a
continuous culture with cell retention for more than 120 hours (Figure 3). Cell retention was
carried out with hollow fibre membranes. The lactic acid concentration during continuous
cultivation was constant at around 50 to 60 g L-1. The retention and recycling of cells
continuously increased the biomass concentration in the fermenter. The increase in biomass
concentration eventually caused an increase in volumetric productivity, which rose to 25 g
lactic acid per litre per hour. This productivity was up to four times higher than the
productivity found in comparable continuous cultures without cell recycling. Due to the
increase in volumetric productivity, the dilution rate was continuously increased from 0.05 h-1
at the beginning to 0.35 h-1 after 110 hours. This approach revealed the opportunity to design
10

effective and efficient lactic acid fermentation processes based on organic residues as nutrient
sources [84].

Bio-plasticizer
Bio-plasticizers are used to improve the flexibility and stability of polymers, such as
polyvinyl chloride [85]. Compared to petroleum-based plasticizer, plasticizers from
biological sources are biodegradable and do not accumulate in the environment. Therefore,
bio-plasticizers are considered as environmentally benign compounds and are produced at
around 200,000 t annually [85, 86]. The formation is based on simple and conventional
reactions, including methylation of fatty acids and epoxidation of unsaturated fatty acid
methyl ester using hydrogen peroxide in presence of toluene and formic acid (Figure 4). The
advantage of this approach is the simultaneous formation of two wanted products from fatty
acids, bio-plasticizer and biodiesel.

The bottle neck of bio-plasticizer production is the availability of unsaturated fatty acids,
which, due to differences in biochemical pathways, are not present in all biological materials
[87]. The biosynthesis of unsaturated and polyunsaturated fatty acids basically includes two
reactions: elongation and desaturation. During elongation, the carbon chain is extended by
two carbon atoms supplied by malonyl-CoA (Figure 5, vertical arrows). Desaturation,
includes the formation of double bonds by dehydrogenation of carbon atoms catalyzed by
desaturases (Figure 5, horizontal arrows). Synthesis of polyunsaturated fatty acids starts with
the introduction of a second double bond in the carbon chain of a monounsaturated fatty acid
like palmitoleic or oleic acid, the precursors of all n-3 and n-6 polyunsaturated fatty acids
(Figure 4). The introduction of further double bonds between the first existing double bond
and the terminal methyl group is essential for the synthesis of polyunsaturated fatty acids.
This particular reaction is carried out by plants, microalgae and yeasts, but not by mammals.

In order to make unsaturated fatty acids for the production of bio-plasticizer available, much
efforts have been put on the investigation of vegetable oils from various sources, such as
soybean, linseed, canola, sunflower and rubber seed [88, 89]. In addition to vegetable oils,
microalgae are known as a source of fatty acid containing lipids. Oleaginous microalgae are
able to accumulate more than 20% of their biomass as lipids, containing saturated and
unsaturated fatty acids, under stress conditions, such as nitrogen limitation [13, 78, 90, 91].
Some microalgae are even able to accumulate more than 50% of their biomass as lipids [92].
11

However, even when microalgae can be cultivated in bioreactors, the realization at larger
scale is challenging. Phototrophic algal strains have the advantage of converting carbon
dioxide into biomass and thus, fatty acids. Nevertheless, the cultivation is restricted by fairly
low biomass productivities and high demand of nutrients [93]. The biomass productivity of
heterotrophic algal strains is high, however, the need of expensive nutrients (e. g. glucose)
makes cultivations at larger scale economically unfeasible. Therefore, in order to develop
feasible cultivation processes, recent research has been focused on the use of organic residues
as nutrient sources [94].

Table 4 lists different microalgal and yeast strains that have been investigated for the
production of fatty acids, and in particular unsaturated fatty acids. Cultivations of the listed
microbes were carried out in presence of hydrolyzed organic residues as carbon and/or
nitrogen sources. The tested microalgae and yeasts grew well on organic residues derived
nutrients and all microbes accumulated lipids including unsaturated fatty acids. The
volumetric lipid and unsaturated fatty acid productivities were dependent on the type of
strains, their abilities to utilize organic residue derived nutrients and the mode of cultivation.
For instance, Chlorella vulgaris was cultivated under mixotrophic conditions on soy whey
and thin stillage, and an unsaturated fatty acid productivity of 0.1 and 0.9 g L-1 d-1 was
obtained, respectively [95]. Using the alga Schizochytrium mangrovei and food waste
hydrolysate, the volumetric lipid and fatty acid productivities were 2.2 and 0.9 g L-1 d-1,
respectively [13]. Due to a higher biomass concentration in fed-batch cultures, considerably
higher volumetric lipid (1.8 g L-1 d-1) and fatty acid (1.2 g L-1 d-1) productivities of
C. pyrenoidosa were found (Table 4) as compared to batch cultures in presence of food
waste hydrolysate [78]. Fed-batch processes are particularly an attractive option when the
microbes are sensitive to high substrate concentrations. For example, the growth of C.
pyrenoidosa was inhibited when more than 30 g L-1 glucose was supplied. Thus, fed-batch
cultures performed at a glucose concentration below 30 g L-1 is an appropriate fermentation
strategy.

The accumulation of lipids and unsaturated fatty acids depends on the carbon-to-nitrogen
(C/N) ratio. It is well known that the limitation in nitrogen favors the accumulation of both,
lipids and fatty acids, in oleaginous microbes [13, 78, 90, 91]. However, an adjustment is
difficult when complex organic substrates are used. Therefore, Ryu et al. [96] supplemented
spent yeast lysate with glycerol in order to increase the C/N ratio from 20 to 35. With this
12

approach, the volumetric lipid productivity of the yeast Crytococcus curvatus was doubled
(Table 4). In order to obtain an appropriate C/N ratio for increased productivities of fatty
acids, one might consider mixing carbon-rich hydrolysates, such as lignocellulosic
hydrolysates, with nitrogen-rich streams, such as green press juice and food waste
hydrolysate. Wiebe et al. [97] carried out fed-batch cultures of Rhodosporidium toruloides
with different C/N ratios in the feed. They found highest lipid content of biomass (75%)
when only glucose was supplied during fed-batch phase. However, not all substrate was
consumed. Decreased lipid contents of 50% and 61% were obtained when the C/N ratios in
the feed were 65 and 80, respectively. The fact that lipid accumulation as a secondary product
is triggered when cultivation is carried out under conditions of restricted growth particularly
favors the application of fed-batch over batch processes.

Valorization of residues from fruit and vegetable processing


Residues coming from fruit and vegetable processing industry have attracted much attention
in recent years as they represent up to 60% of its total production. In this way, the wine and
olive oil industries leave behind a large amount of wastes throughout the production chain,
which could be drawn upon for a more sustainable performance of the plant: from tree
cultivation to wastewater streams or solid residues generated after filtration [98, 99].
Valuable phytochemical compounds for the pharmaceutical, cosmetic or food industry in
form of additives, enzymes or ingredients are extracted (Table 5), and also biofuels and
chemicals can be produced when using those wastes as culture media in fermentations [100].
More recently, research is focusing in obtaining innovative products from those wastes, such
as reinforcement materials in polypropylene composites [101] or novel pectin materials with
good surfactant and biological properties [102].

After citrus juice extraction, 50% of the fresh fruit becomes citrus wastes; these are organic
solids with high content in sugars but low amount of protein, to be used as feeding material in
fermentative processes. Citrus wastes can be utilized for producing enzymes (especially
pectinase) citric acid, succinic acid, dietary fibers production, prebiotic oligosaccharides and
natural antioxidants, and thus improve the profitability of the process [103]. Similarly, potato
residues combined with potato starch have been directly fermented into lactic acid in septic
systems [104]. For the valorization of other agricultural residues, mixed substrates, microbial
consortia or solid state fermentation are some of the most employed techniques [105].

13

Although it is not discussed in this review, the most extended form of organic residues
valorization is in the form of bioenergy. The by-products of a biorefinery facility are also
subject of valorization to achieve a real integrated facility as promoted by the cascade
approach [1]. In this context, lactic acid and poly-3-(hydroxybutyrate-co-hydroxyvalerate)
have been produced from stillage [106, 107]. Obruca et al. [108] presented another scenario
of integrated valorization of organic residues in the coffee industry, in which oil extracted
from spent grounds serves as polyhydroxyalkanoate (PHA) precursor and the remaining
solids after extraction are hydrolyzed in order to generate new feedstocks for either further
PHA or carotenoids production by different microorganisms.

Integrated biorefinery concept for the production of succinic acid, lactic acid and bioplasticizer
Integrated biorefinery concepts have been presented for the simultaneous production of
various products, such as ethanol and succinic acid from industrial hemp [109], -carotene,
biodiesel, glycerol, omega-3 fatty acids, glycerol, bioethanol and bioenergy from algal
biomass [110, 111] and polyhydroxybutyrate and bioenergy from banana residues [112]. In
the previous sections, opportunities were introduced to valorize organic residues for the
production of added value chemicals. Based on the facts provided above an integrated
biorefinery concept was developed for the simultaneous production of succinic acid, lactic
acid and bio-plasticizer (Figure 6). The concept for the production of lactic acid and bioplasticizer was tested in our earlier studies [78, 113]. Similarly, fermentative production of
succinic acid using hydrolysate derived from mixed food waste was demonstrated by our
groups [56]. From 1,000 kg mixed restaurant food waste, 270 kg glucose, 4.7 kg FAN and 1.9
kg phosphate can be recovered. Furthermore, 478.5 kg lipid-rich solids remain. Nutrients
recovered from food waste are sufficient to produce 213.3 kg algal biomass. Extraction of
lipids from algal biomass and remaining solids gives 111.4 kg unsaturated fatty acids, which
produce 78 kg bio-plasticizer [113]. Alternatively, nutrients recovered from food waste can
be used for the fermentative production of succinic acid. Applying all nutrients recovered
from 1,000 kg food waste would result in the production of 251.1 kg succinic acid [56].

Furthermore, the nitrogen-rich residues obtained after lipid extraction from algal biomass and
remaining solids are sufficient for the production of 1,673 kg lactic acid. However, an
external carbon source is required as the residues do not contain sufficient carbon
compounds. For the process shown in Figure 6, 1,917.5 kg glucose is required, which can be
14

supplied in form of hydrolysate from cellulose and hemicellulose-rich agricultural residues


[114, 115].

Conclusions and future perspectives


Recovered nutrients from organic residues in the form of sugars and amino acids, but also
phosphate can be used as feed for many microbes in biotechnological processes. The
metabolic versatility of microbes enables the fermentative production of a wide range of
products. Valorization of organic residues opens the door to the development of innovative
waste treatment strategies and biotechnological processes, which contribute to the bio-based
economy. As mentioned previously, recent research conducted in our group focuses on the
use of FBB technology and hydrolysate of agricultural residues or food waste as feedstock.
Various agricultural residues such as cotton stover, corn bran and wheat straw are currently
tested as cell immobilization materials in FBB. Such immobilization offers several potential
advantages of a process engineering nature to the continuous fermentation system. These
include ease of handling and of cell separation, and lowering of bulk viscosity, as well as the
obvious potential benefits of increased cell concentration. This approach does not only
contribute to the reduction of the amount of organic waste that needs to be treated, but also to
the production of environmentally benign and added value chemicals with great industrial
potential. Succinic acid, lactic acid and bio-based plasticizer are potential precursors in
chemical reactions. Furthermore, succinic acid and lactic acid can be used as food
supplements. This aspect particularly contributes to the principle of cascading use of biomass.
While lactic acid and fatty acid productions are possible with native microbial strains, the
successful and efficient conversion of organic residues into succinic acid likely depends on
the use of engineered microbial strains. A strictly aerobic yeast Y. lipolytica is currently being
developed in our laboratory as a cell factory for biological production of succinic acid by
metabolic pathway engineering, whole cell bioconversion and upgrading of industrial wastes.
This oleaginous yeast has been demonstrated as a promising host for succinic acid production
using crude glycerol as carbon source. Using fed-batch fermentation strategy, the final
succinic acid concentration, productivity and yield resulted were 160.2 g L-1, 0.40 g L-1 h-1
and 0.40 g g-1 glycerol (unpublished result). More research is needed in order to realize and
implement innovative and effective waste valorization strategies. In this aspect, it is of
particular interest to develop processes that can be operated in a decentralized modus and
contribute to the regional utilization of organic residues.

15

Furthermore, nutrients recovery from food supply chain waste such as expired food and
beverage waste from grocery store would be an innovative waste-based biorefinery strategy.
Therefore, the development of bioconversion process to convert the nutrients in expired food
and beverage wastes (e.g. carbohydrates, proteins, lipid, minor constituents with high market
values) for the production of chemicals, materials and fuels would be the future trend for
waste valorization.

Acknowledgements
The work presented by Q. Qi, C. Gao and C.S.K. Lin on metabolic engineering of Yarrowia
lipolytica for the simultaneous production of succinic acid (SA) and polyhydroxyalkanoates
(PHAs) is part of the research projects supported by grants from the Research Grants Council
of the Hong Kong Special Administrative Region, China [Project No. CityU189713] and the
State Key Lab of Microbial Technology in Shandong University, China [M2014-03].
D. Pleissner and C.S.K. Lin gratefully acknowledge the Innovation and Technology Funding
from the Innovation and Technology Commission [ITS/353/12] in Hong Kong for their
support in research project Sustainable Biorefinery Concept Based on Microalgal Biomass
Produced from Mixed Food Waste.
The Authors want to acknowledge the contribution of the COST Action TD1203 EUBis.

16

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29

Figure 1. Industrially relevant metabolites obtainable via fermentative processes [1].

30

Figure 2. Pathways involved in succinic acid production, including the glyoxylate shunt, the
oxidative pathway and the reductive pathway of the tricarboxylic acid (TCA) cycle.

31

Figure 3. Continuous cultivation of Lactobacillus paracasei with biomass ( ) retention for


lactic acid ( ) production at increasing dilution rate ( ). Glucose ( ) and nitrogen source
were obtained from barley hydrolysate and green press juice, respectively.

32

Figure 4. Chemical conversion of saturated and unsaturated fatty acids into biodiesel and
bio-plasticizer, respectively [113].

33

Figure 5. Major pathways of polyunsaturated fatty acid biosynthesis starting from acetylCoA [87].

34

Figure 6. Integrated biorefinery concept for the production of succinic acid, lactic acid and
bio-plasticizer from food waste. Figures are based on dry weights. The remaining nitrogenrich compounds from algal biomass production and lipid extraction would be sufficient to
convert 1,917.5 kg glucose (*obtainable from cellulose and hemicellulose-rich agricultural
residues), into lactic acid.

35

Table 1. Organic residues and their applications.


Organic residues

Application

Ref.

Fruits and vegetables

Antioxidants, flavonoids, phenols, carotenoids, lipids, phytochemicals, carbon source

[22]

Animal waste, meat and derivatives

Proteins, enzymes, collagen, gelatine, nitrogen source, trace minerals

[21, 22]

Dairy products

Carbon and nitrogen sources

[22]

Waste oil

Fatty acid methyl esters, glycerol, erucic acid

[23]

Cellulosic biomass

Phytosterols, polypropylene, acrylic acid, isobutanol, thioester, esters

[23]

Lignin

Polyhydroxyalkanoates, adipic acid

[24, 25]

36

Table 2. Comparison of succinic acid production from conventional media and organic residues.
Feedstock

Pretreatment

Microorganisms

Glucose

NA

Rec. E. coli

Fructose

NA

Rec. E. coli

Xylose

NA

Rec. E. coli

NA

Rec. E. coli

NA

Rec. E. coli

NA

A. succiniciproducens

Glucose,
Fructose
Glucose,
Xylose
Raw whey
(lactose)

A. awamori and A.
oryzae
A. awamori and A.
oryzae
A. awamori and A.
oryzae
A. awamori and A.
oryzae
A. awamori and A.
oryzae

A. succinogenes

Cheese whey

NA

A. succinicproducens

Cheese whey

NA

A. succinicproducens

Cheese whey

NA

A. succinicproducens

Cheese whey

NA

A. succinogenes

Food waste
Wheat-based
feedstock
Waste bread
Cakes
Pastries

Rec. E. coli
A.succinogenes

A. succinogenes
A. succinogenes

Configuration
Batch/bench top
bioreactor
Batch/bench top
bioreactor
Batch/bench top
bioreactor
Batch/bench top
bioreactor
Batch/bench top
bioreactor
Fed-batch
Batch/bench top
bioreactor
Batch/bench top
bioreactor
Batch/bench top
bioreactor
Batch/bench top
bioreactor
Batch/Bench top
bioreactor
Batch/bench top
bioreactor
Fed-batch/bench
top bioreactor
Continuous, bench
top bioreactor
Batch/bench top
bioreactor
37

Final conc.
[g L-1]

Productivity
[g L-1 h-1]

Yield
[g g-1 sugar]

Yield
[g g-1 waste]

Ref.

1.27

0.83

NA

[116]

1.01

0.66

NA

[116]

0.78

0.50

NA

[116]

0.79

0.58

NA

[116]

0.86

0.60

NA

[116]

34.7

1.02

[117]

29.9

0.48

0.56

0.22

[56]

64.2

1.19

0.81

[118]

47.3

1.12

1.16

0.55

[49]

24.8

0.79

0.80

0.28

[14]

31.7

0.87

0.67

0.35

[14]

34.3

0.80

[117]

34.7

0.91

[117]

19.8

0.60

[117]

27.9

0.44

0.57

[119]

Corn stover

Corn stover

Corn straw

Corn straw

Alkaline +
enzymatic
hydrolysis
Alkaline, Acid,
Alkaline peroxide,
Aqueous ammonia
soaking
Alkaline +
enzymatic
hydrolysis
Alkaline +
enzymatic
hydrolysis

A. succinogenes

Batch/bench top
bioreactor

56.4

0.73

[120]

A. succinogenes

SSF

47.4

0.72

[121]

A.succinogenes

Batch/bench top
bioreactor

45.5

0.95

0.81

[122]

A.succinogenes

Fed-batch/bench
top bioreactor

53.2

0.83

1.21

[122]

A.succinogenes

Anaerobic bottle

32.1

0.89

[122]

A.succinogenes

Anaerobic bottle

17.6

0.63

[122]

A.succinogenes

Anaerobic bottle

19.0

0.74

[122]

A.succinogenes

SSF

15.5

0.12

[123]

A.succinogenes

Batch/bench top
bioreactor

61.6

1.21

0.59

[124]

Rec. E coli

Fed-batch/bench
top bioreactor

39.3

0.33

0.97

[125]

Acid + enzymatic
hydrolysis

A.succinogenes

Batch/bench top
bioreactor

20

0.61

0.65

[126]

Acid, potassium
ferrocyanide, resin

A. succinogenes

Batch/bench top
bioreactor

46.4

0.97

0.79

[127]

Corn core
hydrolysate
Rice straw
hydrolysate
Wheat straw
hydrolysate
Rapeseed meal
Sake lees
Sugar cane
bagasse
hydrolysates
Cellobiose &
sugars from
sugarcane
bagasse
cellulose
hydrolysates
Sugar cane
molasses

Acid + enzymatic
hydrolysis
Acid + enzymatic
hydrolysis

38

Soybean meal
Soy solubles

and activated carbon


Acid, potassium
ferrocyanide, resin
and activated carbon
Acid hydrolysis
Acid hydrolysis

Wheat straw

NA

Orange peel

Steam distillation +
acid hydrolysis

Rec. E. coli
Rec. E. coli
Fibrobacter
succinogenes
Fibrobacter
succinogenes

Carob pod
water extracts

A. succinogenes

Sugar cane
molasses

Wood
hydrolysate
Wood
hydrolysate
Wood
hydrolysate
Plant
hydrolysates
(industrial
grade
hydrolysates)

A. succinogenes

Fed-batch/bench
top bioreactor
Batch/flask
Batch/flask
Batch/serum
bottles
Batch/serum
bottles
Batch/bench top
bioreactor

55.2

1.15

[127]

11.2
36.8

0.64
0.64

[128]
[128]

2.0

[129]

1.9

0.03

0.05

[129]

1.61

0.54

[130]

Steam explosion +
enzymatic
hydrolysis
Steam explosion +
enzymatic
hydrolysis
Steam explosion +
enzymatic
hydrolysis

A. succinogenes

Batch /bench top


bioreactor

24.0

0.88

[131]

M. succiniciproducens

Batch/bench top
bioreactor

11.7

1.17

0.56

[132]

M. succiniciproducens

Continuous, bench
top bioreactor

8.0

3.19

0.55

[132]

Rec. E. coli

72.0

1.00

1.00

[133]

39

Table 3. Comparison of lactic acid production from conventional media and organic residues.
Feedstock

Pretreatment

Sucrose/Yeast
NA
Bacillus coagulans
extract
Defatted algal
Fungal enzymes in
biomass and defatted
submerged
B. coagulans
food waste
fermentation
Defatted algal
Proteolytically
biomass and defatted pretreated defatted food
B. coagulans
food waste
waste derived solids
Lactobacillus
Ragi and wheat bran Enzymatic hydrolysis
plantarum
Wheat bran
L. biferementans
hydrolysate
Wheat bran
hydrolysate
Cane
molasses/glucose
Barley hydrolysate
and green juice from
alfalfa
Barley hydrolysate
and green juice from
alfalfa

Configuration

Final conc.
[g L-1]

Productivity
[g L-1 h-1]

Yield
[g g-1 sugar]

Batch/bench top
bioreactor

55.0

0.92

[73]

Batch/bench top
bioreactor

32.0

0.84

[78]

Batch/bench top
bioreactor

37.0

0.84

[78]

Batch/conical flasks

0.94

[81]

Batch/test tubes

41.3

0.47

[134]

62.8

0.83

[134]

168.3

2.1

0.88

[79]

Microorganisms

Batch/cell
immobilization by
calcium alginate beads
Fed-batch/bench top
bioreactor

Ref.

L. biferementans

B. coagulans

L. paracasei

Batch

100.0

3.3

[83]

L. paracasei

Continuous/ hollow fibre


membrane reactor

60.0

25.0

[83]

40

Sugarcane bagasse
Cassava bagasse
Corncob
hydrolysates

Steam + alkali +
enzymatic hydrolysis
Enzymatic hydrolysis
Acid + enzymatic
hydrolysis
NaCl scalding +
milling and sieving

L. delbrueckii

SSF

67.0

0.93

0.83

[135]

L. delbrueckii

SSF

1.4

[136]

Rhizopus oryzae

Batch/flask

97.5

0.81

[137]

Batch/flask

2.2

[138]

Batch/flask

2.4

[138]

Batch/flask

2.4

[138]

Grapefruit peel

Milling and sieving

Pineapple peel
Opuntia ficus fruit
peel

Milling and sieving

Aerococcus
viridans
Pediococcus
pentosaceus
A. viridans

Milling and sieving

A. viridans

Batch/flask

2.1

[138]

Soft wood

Acid hydrolysis

L. casei susp.
rhamnosus

Batch/bottle

0.38

0.80

[139]

Wood hydrolysate

Acid hydrolysis, Steam


explosion, Commercial
enzymes

Enterococcus
faecalis

Batch/bench top reactor

24-93

1.7-3.2

[140]

Blending

L. acidophilus

Fed-batch

0.79

[141]

48.7

1.11

[142]

27-45

[143]

Grapefruit albedo

Municipal solid
wastes
Kitchen waste

Homogenizing

Kitchen waste

Batch
L. manihotivorans
L. phantarnm, L.
Batch, pH intermittently
brevis
neutralized
predominantly

41

Table 4. Lipid concentration and productivities of lipids and unsaturated fatty acids (UFAs) of various microalgal strains cultivated in presence
of organic residues as carbon and/or nitrogen sources.
Microbes

Carbon source

Nitrogen source

Lipid concentration

Lipid productivity

UFA productivity

[g L-1]

[g L-1 d-1]

[g L-1 d-1]

Ref.

Algae
C. vulgarisa,c

Food waste

Food waste

1.1

0.3

0.2

[144]

C. vulgarisa,d

Soy whey

Soy whey

0.6

0.2

0.1

[95]

C. vulgarisa,d

Thin stillage

Thin stillage

4.2

1.1

0.9

[95]

C. pyrenoidosaa,c

Food waste

Food waste

0.6

0.2

0.1

[13]

C. pyrenoidosab,c

Food waste

Food waste

9.0

1.8

1.2

[78]

S. mangroveia,c

Food waste

Food waste

2.2

2.2

0.9

[13]

8.8*

1.6*

[96]

19.1*

3.6*

[96]

Yeasts
C. curvatusa,e
C. curvatus a,e,f

Spent yeast lysate /

Spent yeast

glycerol

lysate

Spent yeast lysate /

Spent yeast

glycerol

lysate

*Based on quantified fatty acid methyl esters; aBatch culture; bFed-batch culture; cGrown under heterotophic conditions;
d

Grown under mixotrophic conditions; eCultivation carried out at a C/N ratio of 20; fCultivation carried out at a C/N ratio of 35

42

Table 5. Phytochemicals in fruit and vegetable residues.


Phytochemical compound

Fruit and vegetable residues

Ref.

Phenolic acids

Apple pomace, carrot pomace, onion wastes

[145]

Flavonoids

Apple pomace, grape pomace, mango peel, lemon pomace, onion waste

[145-148]

Carotenoids

Peach peel, carrot pomace, tomato pomace, lemon pomace

[149-152]

Anthocyanins

Apple pomace, grape pomace, mango peel, carrot pomace, onion waste

[153-156]

Hydroxycinnamic acids

Orange pomace, cauliflower by-products

[148, 157]

43