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Waste Biomass Valor (2014) 5:903917

DOI 10.1007/s12649-014-9311-x


Enzyme Production from Food Wastes Using a Biorefinery

Esra Uckun Kiran Antoine P. Trzcinski

Wun Jern Ng Yu Liu

Received: 13 February 2014 / Accepted: 30 June 2014 / Published online: 9 July 2014
Springer Science+Business Media Dordrecht 2014

Abstract According to Food and Agricultural Organiza- Introduction

tion (FAO), one-third of food produced globally for human
consumption (nearly 1.3 billion tonnes) is lost along the Food waste (FW) is organic waste produced in food pro-
food supply chain. In many countries food waste is cur- cessing plants, domestic and commercial kitchens, cafete-
rently landfilled or incinerated together with other com- rias, and restaurants. It accounts for a considerable
bustible municipal wastes for possible recovery of energy. proportion of municipal solid waste all over the world [1].
However, these two options are facing more and more According to FAO [2], nearly 1.3 billion tonnes of foods
economic and environmental stresses. Due to its organic- including fresh vegetables, fruits, meat, bakery and dairy
and nutrient-rich nature, theoretically food waste can be products are lost along the food supply chain.
converted to valuable products (e.g. bio-products such as The amount of FW is continuing to increase due to the
methane, hydrogen, ethanol, enzymes, organic acids, increase in population and economical growth, particularly
chemicals and fuels) through various fermentation pro- in Asian countries. The annual amount of urban FW in
cesses. Such conversion of food waste is potentially more Asian countries would rise from 278 to 416 million tonnes
profitable than its conversion to animal feed or transpor- from 2005 to 2025 [3]. The highest absolute amount per
tation fuel. Food waste valorisation has therefore gained year was in China (82.8 Million tonnes (MT) followed by
interest, with value added bio-products such as methane, Indonesia (30.9 MT), Japan (16.4 MT), Philippines (12
hydrogen, ethanol, enzymes, organic acids, chemicals, and MT) and Vietnam (11.5 MT). However, the highest amount
fuels. Therefore, the aim of this review is to provide of FW produced per capita was in New Zealand and
information on the food waste situation with emphasis on Australia with 280 kg/year, while it was around
AsiaPacific countries and the state of the art food waste 120130 kg in Southeast Asia other than Cambodia
processing technologies to produce enzymes. (173 kg/year). Although the absolute amount of food waste
in China is the highest, the waste production per capita is
Keywords Food waste  Biorefinery  Amylase  the lowest (61 kg/year), while the waste production per
Protease  Lipase  Lignocellulosic enzymes  Pectinolytic capita is 120 and 168 kg/year in Singapore and Hong
enzymes Kong, respectively [4, 5], showing that food wastage seems
more prevalent in high-income states. Food wastes have
been dumped, landfilled, incinerated, composted, digested
E. Uckun Kiran  A. P. Trzcinski  W. J. Ng  Y. Liu anaerobically and/or used as animal feed. In many Asian
Advanced Environmental Biotechnology Centre, Nanyang
countries FW is still dumped with other household waste in
Environment & Water Research Institute, Nanyang
Technological University (NTU), Singapore 637141, Singapore landfills or dumpsites (Fig. 1). Unfortunately, the capacity
of the landfills is limited and would not be able to handle
W. J. Ng  Y. Liu (&) increasing amount of FW [6].
School of Civil and Environmental Engineering, Nanyang
In order to reduce its volume, FW is traditionally
Technological University, 50 Nanyang Avenue,
Singapore 639798, Singapore incinerated with other combustible municipal solid wastes
e-mail: for generation of heat or energy, particularly in Japan and

904 Waste Biomass Valor (2014) 5:903917

Fig. 1 Waste treatment

methods in Asian countries [6

Singapore. The incineration of FW is a favourable option environmental impact and a high economic efficiency
against landfilling in terms of overall energy recovery, and compared to other treatment methods. However, the high
emissions of greenhouse gases [9]. However, the inciner- moisture content of FW will lead to substantial release of
ation may not be an affordable approach for most low- leachate [12]. Indeed, compost is more expensive than
income countries due to the high capital and operating commercial fertilizers and the current market of compost
costs [6]. It should also be noted that incineration of FW produced from FW is limited [13].
can potentially cause air pollution [10]. Anaerobic digestion is another alternative which yields
Another approach to handle biodegradable FW is com- methane and carbon dioxide as metabolic end products and
posting which results in a valuable soil conditioner and therefore could be feasible from an economic and envi-
fertilizer [11]. Composting has a relatively low ronmental point of view because methane is used as an

Table 1 Characteristics of mixed food waste

Origin pH Moisture Total solid VS/TS Total sugar Starch Cellulose Lipid Protein Ash References

Dining hall NR 79.5 20.5 95.0 NR NR NR NR 21.9 NR Han and Shin [16]
Cafeteria 5.1 84.1 15.9 15.2 NR NR NR NR NR NR Kim et al. [26]
Cafeteria 5.1 80.0 20.0 93.6 NR NR NR NR NR 1.3 Kwon and Lee [27]
MSW NR 85.0 15.0 88.5 NR NR 15.5 8.5 6.9 11.5 Rao and Singh [28]
Cafeteria 4.6-5 79.1 20.9 93.2 NR NR NR NR NR NR Ramos et al. [29]
Cafeteria NR 75.9 24.1 NR 42.3 29.3 NR NR 3.9 1.3 Ohkouchi and Inoue [30]
NR NR 87.6 12.4 89.3 NR NR NR NR NR NR Kim et al. [31]
Residents 4.9 80.8 19.2 92.7 NR 15.6 NR NR NR NR Pan et al. [22]
Dining hall NR 80.3 19.7 95.4 59.8 NR 1.6 15.7 21.8 1.9 Tang et al. [32]
Dining hall NR 82.8 17.2 89.1 62.7 46.1 2.3 18.1 15.6 NR Wang et al. [33]
Restaurant 3.9 80.0 20.0 95.0 70.0 NR NR 10.0 13.0 NR Zhang et al. [34]
Dining hall 5.6 82.8 17.2 85.0 62.7 46.1 2.3 18.1 15.6 NR Ma et al. [35]
Cafeteria NR 61.3 38.7 NR 69.0 NR NR 6.4 4.4 1.2 Uncu and Cekmecelioglu [36]
Food court NR 64.4 35.6 NR NR NR NR 8.8 4.5 1.8 Cekmecelioglu and Uncu [37]
Canteen NR 81.7 18.3 87.5 35.5 NR NR 24.1 14.4 NR He et al. [24]
Restaurant NR 81.5 18.5 94.1 55.0 24.0 16.9 14.0 16.9 5.9 Vavouraki et al. [23]
Restaurant NR 81.9 14.3 98.2 48.3 42.3 NR NR 17.8 NR Zhang and Jahng [38]

Total Solid, Total sugar, Starch, Cellulose, Lipid, Protein and Ash Contents were given in wt% on the basis of dry weight. Volatile solid contents were given as the
%VS ratio on total solid basis. NR: not reported

Waste Biomass Valor (2014) 5:903917 905

energy source [9]. Hirai et al. [14] evaluated the environ- generating electricity ($60150/ton biomass) and animal
mental impacts of FW treatment and found that utilising a feed ($70200/ton biomass) [25].
methane fermentation process prior to incineration reduces During the bioconversion of FW, its saccharification is
approximately 70 kg CO2eq/tonne waste of the global the rate limiting step. For an efficient biomass conversion,
warming potential, due to the substitution effect. Food carbohydrate components of FW should be hydrolyzed to
waste is also used as animal feed. The disadvantages are its yield high concentrations of fermentable oligosaccharides
variable composition and the high moisture content, which and monosaccharides. Hence, there is an increasing interest
favors microbial contamination [15]. To prevent this, ani- in the production of biomass saccharifying enzymes,
mal feed is generally dried but greenhouse gas emission mainly amylases and cellulases [39]. There are remarkable
increases depending on the energy usage during the drying amount of publications on the lab-scale production of
process, which is related to the water content of FW [10]. various industrial enzymes, such as proteases, amylases,
FW is mainly composed of carbohydrate polymers lignocellulosic enzymes and lipases using different types of
(starch, cellulose and hemicelluloses), lignin, proteins, FW. Therefore, this review presents the state of the art of
lipids, organic acids (Table 1). Total sugar and protein production of various industrial enzymes from FW.
contents in FW are in the range of 35.569 and
3.921.9 %, respectively. Due to its inherent chemical
complexity, alternative treatment methods are currently Enzyme Production
explored with emphasis on production of high value-added
products, such as biofuels, biodiesel, platform chemicals Various kinds of enzymes have been commonly used for
and enzymes [1624]. In general, fuel applications (selling many industrial purposes. As such, enzyme production is of
price: $200400/ton biomass) and organic acids, biode- important to sustain various industrial needs. So far, solid
gradable plastics & enzymes applications ($1000/ton bio- state fermentation (SSF) has extensively explored for the
mass) are usually creating more value compared to production of different enzymes with the ultimate aims to

Table 2 Amylase production from food wastes

Residual Microorganism Pretreatment Fermentation mode & Fermentation conditions Duration Achievements References
materials method vessel type (day)

Potato Bacillus subtilis Dried, SSF-250 mL flasks 40 C, pH 7, 65 % MC, 2 a-amylase [43]

peel ground, 10 % (v/w) inoculum (600 U/mL)
Potato Bacillus Dried, SSF-250 mL flasks 40 C, pH 7, 70 % MC, 2 a-amylase [43]
peel licheniformis ground, 10 % (v/w) inoculum (270 U/mL)
Coffee Neurospora Ground, SSF-250 mL flasks 28 C, pH 4.6, 60 % MC, 5 a-amylase [49]
waste crassa CFR steamed 1 mm PS, 107 spores/g ds (6,342 U/g
308 ds)
Potato Bacillus firmus Dried, SmF-250 mL flasks 35 C, pH 7.5, 1 % S 2 a-amylase [48]
peel CAS 7 ground, (676 U/mL)
Tomato Aspergillus Dried, SSF-plate-type SSF 28 C, pH 5 5 a-amylase [50]
pomace awamori milled, bioreactor (10.9 IU/g
sieved ds)
Bread Bacillus NR SmF- 1L flask with 30 C, pH 7 1 a-amylase [51]
waste caldolyticus 100 ml working vol (6.7 U/g ds)
DSM 405
Pea pulp Bacillus None SmF- flasks 70 C, 150 rpm 6 a-amylase [51]
caldolyticus (8.6 U/mL)
DSM 405
Food Aspergillus None SmF-250 mL flasks 30 C, pH 5, 120 rpm, 5 % 4 GA (137 [45]
waste niger UV-60 I/S U/mL)
Bread Aspergillus None SSF-petri plates 30 C, MC:1.8 (w/w, db), 6 GA (114 [52]
waste oryzae PS:20 mm, 106spore/gdS U/gdS)
S substrate, SSF solid state fermentation, SmF submerged fermentation, I/S Inoculum to substrate ratio, ds dry substrate, MC moisture content, PS
particle size, ds dry solid, GA glucoamylase


Table 3 Lignocellulosic enzyme production from food wastes

Residual materials Microorganism Pretreatment Fermentation Fermentation conditions Duration Achievements References
method mode & (day)
vessel type

Banana wastes Bacillus Dried, ground, SSF-250 mL 35 C, pH 7, 400 lm PS, 70 % MC, 3 FPAse (2.8 IU/ds), CMCase (9.6 IU/g [65]
subtilis acid and alkali flasks 15 % (v/w) I/S ratio ds), Cellobiase (4.5 IU/g ds)
(CBTK106) pretreatment
Grape pomace Aspergillus Dried, milled, SSF- petri 30 C, 10 g S, 7 Xylanase (40.4 IU/g ds), Cellulase [69]
awamori sieved dishes 5 9 105 I/S, 60 % MC (9.6 IU/g ds)
Apple pomace Trichoderma Dried, crushed, SSF-250 mL 32 C, 70 % MC, 6 Cellulase (5.8 U/g ds) [66]
sp. sieved flasks 108 spores/flask
Banana peel Trichoderma Dried, crushed, SSF-250 mL 30 C, 65 % MC, 6 FPA(5.6U/g ds), CMCase (10.3 U/g ds), [67]
viride GIM sieved flasks 109 spores/flask b-glucosidase (3U/g ds)
Tomato pomace Aspergillus Dried, milled, SSF-plate- 28 C, pH 5 5 Xylanase (195.9 IU/g ds), CMCase [50]
awamori sieved type SSF (19.7 IU/g ds)
Carrot, orange, Aspergillus Acid/base SSF-250 mL 30 C, pH 7, 1:1.5 to 1:1.75 S/M ratio 4 CMCase (310 U/gds), FPase (17 [62]
pineapple, potato niger NS-2 pretreatment flasks U/gds), b-glucosidase (33 U/gds)
peels, wheat bran using alkaline pretreated wheat bran
Apple pomace Aspergillus Drying, SSF-500 mL 30 C, 1.7-2 mm PS, 75 % MC, 7 FPase (113.7 IU/gds), CMCase [64]
niger crushing, flasks 7 (172.31 IU/gds), b-glucosidase
10 spores/g dS
NRRL-567 sieving (60.1 IU/gds), Xylanase (1412.6 IU/
Grape pomace and Aspergillus Dried, milled SSF-petri 30 C, pH 5, 70 % MC, 4.5 9 108 spores/g S. 15 Exo-PG (3.8 IU/gds), Xylanase [68]
orange peel awamori and sieved dishes (32.7 IU/gds), Cellulase (5.4 IU/gds)
Potato peel Aspergillus Dried, ground SSF 30 C, 107 spores/g dS, 50 % MC 3 FPase (0.015 U/mL), CMCase (0.023 [41]
niger U/mL), Xylanase(0.024 U/mL)
Mango Peel Trichoderma Alkaline SmF-250 mL 30 C, pH 7, 200 rpm 6 Cellulase (7.8 IU/mL) [63]
reesei pretreatment flasks
Passion fruit waste Pleurotus Dried, milled. SSF-250 mL 28 C in complete darkness 14 MnP (0.22 U/mL), b-xylosidase (4.76 [70]
pulmonarius flasks U/mL), b-Glucosidase (2.96 U/mL),
b-galactosidase (6.21 U/mL)
Passion fruit waste Macrocybe Dried, milled. SSF-250 mL 28 C in complete darkness 14 Laccase (10.2 U/mL), Pectinase (1.72 [70]
titans flasks U/mL), Endoxylanase (0.27 U/mL)
S substrate, SSF solid state fermentation, SmF submerged fermentation, I/S Inoculum to substrate ratio, DS dry substrate, S/M substrate to moisture ratio, MC moisture content, PS particle size,
ds dry solid, PG polygalacturonase, CMCase carboxymethylcellulase, MnP Manganese peroxidise, NR Not reported
Waste Biomass Valor (2014) 5:903917
Table 4 Pectinolytic enzyme production from food wastes
Residual materials Microorganism Pretreatment Fermentation mode & Fermentation Duration Achievements References
method vessel type conditions (day)

Apple pomace Aspergillus None SSF- petri dishes 30 C, pH 4, 103 I/S 2 Pectinase (1,300 U/g S) [80]
NRRL 341
Citrus waste Aspergillus None SSF- petri dishes 30 C 2 Pectinase (1,641 U/g S) [77]
NRRL 341
Apple pomace Aspergillus None SSF- 15L horizontal 35 C 3 900 AJDA U/mL [79]
Waste Biomass Valor (2014) 5:903917

niger solid state stirred

tank reactor
Grape pomace Aspergillus Milled, SSF- petri dishes 30 C, 60 % MC 1 Exo-PG(40U/g S), Xylanase (40 U/g S) [74]
awamori sieved
Orange bagasse Botryosphaeria Dried, SSF-125 mL flask 28 C 6 Pectinase (32 U/mL), [78]
rhodina ground Laccase (46 U/mL)
Orange waste Aspergillus NR SmF-Flask 30 C, pH 6, 3.5 Exo-PG (48.5 U/mL) [82]
giganteus 120 rpm, 1.107
CCT3232 spores/mL
Fruit residues (apple, lemon Aspergillus Dried, SmF-Flask 37 C, pH 3.5-5.5, 3 Endopectinase (6 U/mL), Pectinlyase (5 U/mL), [81]
peel, grape skin & tamarind flavipes FP- milled, 150 rpm, 1.106 Exopectinase (4.8 U/mL), Rhamno-
kernel) 500 sieved spores/mL galacturonase (33 U/mL)
Fruit residues (apple, lemon A. terreus FP- Dried, SmF-Flask 37 C, pH 3.5-5.5, 3 Endopectinase (3 U/mL), Pectinlyase (33 U/mL), [81]
peel, grape skin & tamarind 370 milled, 150 rpm, 1.106 Exopectinase (4.8 U/mL), Rhamno-
kernel) sieved spores/mL galacturonase (4 U/mL)
Tomato pomace Aspergillus Dried, SSF-plate-type SSF 28 C, pH 5 5 Exo-PG (36.2 IU/g ds) [50]
awamori milled, bioreactor
Lemon peel pomace Aspergillus Dried, SSF- column-tray 30 C, 70 % MC, 4 Pectinase (2.18 U/mL) [42]
niger Aa-20 ground bioreactor 194 mL/min AFR,
20.7 mm PS
Passion fruit waste Macrocybe Dried, SSF-250 mL flasks 28 C in complete 14 Pectinase (1.72 U/mL) [70]
titans milled. darkness
Orange peel Aspergillus Dried, Fixed bed bioreactor 25 C, 3.105 spores/ 7 Endo-PG (1.18 U/mL), [83]
niger ground mL Exo-PG (4.11 U/mL)
S substrate, SSF solid state fermentation, SmF submerged fermentation, I/S Inoculum to substrate ratio, AFR air flow rate, DS dry substrate, MC moisture content, PS particle size, ds dry solid,
PG polygalacturonase, CMCase carboxymethylcellulase, NR not reported

908 Waste Biomass Valor (2014) 5:903917

Table 5 Protease production from food wastes

Residual Microorganism Pretreatment method Fermentation Fermentation Duration Achievements References
materials mode & conditions (day)
vessel type

Date Bacillus sp. 2-5 Heat treatment & filtration SmF-125 mL 37 C, pH 10, 2 57,420 APU/ [91]
waste flask 125 rpm mL
Potato Saccharomyces NR SmF- 250 ml 28 C 5 360 U/mg [92]
waste cerevisiae flask
Fish meal Bacillus pumilus None SmF-20L 30 C, pH 7.5 2 7.05 U/mL [88]
MTCC 7514 bioreactor
Waste Aspergillus oryzae None SSF-petri 30 C, MC:1.8 (w/ 6 83.2 U/gdS [52]
bread plates w, db), PS:20 mm,
106 spore/gdS
Cuttlefish Vibrio Heat treatment, pressing, SmF- 250 mL 37 C, pH 8.7, 1 2,487 U/mL [94]
by- parahaemolyticus grinding, drying at 80 C flasks 200 rpm
products o/n, powdering
Shrimp Pseudomonas Heat pretreatment SmF- 250 mL 37 C, 200 rpm \1 15,000 U/mL [93]
waste aeruginosa MN7 (100 C, 20 min), flasks
drying, grinding
SmF submerged fermentation, SSF solid state fermentation, MC moisture content, PS particle size, S substrate, o/n overnight, NR not reported

Table 6 Lipase production from food wastes

Substrate Microorganism Pretreatment method Fermentation Fermentation Duration Achievements References
mode & vessel conditions (day)

Banana waste, melon Bacillus None SSF-Flasks 37 C, pH 7 1 148.9 U/g S [97]

waste, watermelon coagulans from melon
waste waste
Waste cooking oil Y.lipolytica None SmF- 5L 30 C, 6 0.93U/mL [105]
CECT 1240 stirred tank 400 rpm
bioreactor with
3L working
vol, fb
Waste cooking olive oil Aspergillus Filtration SmF-250 mL 28 C, pH 6, 3 645 U/mL [106]
and flasks 200 rpm
Olive oil cake Y.lipolytica Alkaline SSF-150 mL 30 C, pH 7, 4 40 IU/g S [107]
NRLL pretreatment (3 % Erlenmeyer 55 % MC
Y-1095 NaOH) 20 C o/n flasks
Tri-substrate (wheat bran, A.niger None SSF-3*1 kg 30 C, 60 % 4 745.7 IU/gdS [108]
wheat rawa and coconut MTCC2594 tray type MC
oil cake) bioreactor
Seafood processing waste Bacillus Drying (80 C o/n) SSF-Flasks 50 C, pH 8, 3 2U/gdS [109]
altitudinis 80 % MC (Esterase)
Tuna by-products Rhizopus Heat pretreatment SmF- 1L flasks 30 C, pH 6, 3 23.5 IU/mL [110]
oryzae (100 C 20 min) 150 rpm
and filtration
Wheat bran with 2 % Aspergillus None SSF-Flasks 29 C, pH 7, 4 121.4 U/gdS [111]
olive oil flavus 65 % MC
Wheat bran with 2 % Aspergillus None SmF- 500 mL 30 C, pH 6, 8 1.46 U/mL [112]
olive oil niger J1 flasks 100 rpm
Wheat bran with 2 % Aspergillus None SSF- flasks 30 C, pH 6, 7 1.46 U/mL [112]
olive oil niger J1 65 % MC
S substrate, ds dry substrate, SSF solid state fermentation, SmF submerged fermentation, fb fed-batch, Y. lipolytica Yarrowia lipolytica, MC
moisture content, o/n overnight

Waste Biomass Valor (2014) 5:903917 909

obtain high activity enzymes at lower cost, while using low enzymes production [44]. However, there are only a few
cost substrates as feed. reports on SSF bioreactor design in the literature. The large
The So far, various kinds of FWs have been used to scale production of enzymes using SSF is challenging
produce different enzymes including proteases, cellulases, because of difficulties in control of pH, temperature, aer-
amylases, lipases and pectinases particularly through solid ation, oxygen transfer and moisture content [40, 45].
state fermentation (SSF) (Tables 2, 3, 4, 5, 6). SSF has
several advantages over submerged fermentation (SmF): Amylases
(i); cost and energy-effective; (ii) a simple fermentation
medium; (iii) superior productivity and (iv) less wastewater The amylase family has two major classes, namely a-
generated [40]. Moreover, an easy control of bacterial amylase (EC and glucoamylase (GA) (EC
contamination and lower costs of downstream processing a-amylase can hydrolyse starch into maltose, glucose and
make it more attractive. Dos Santos et al. [41] have eval- maltotriose by cleaving the 1,4-a-D-glucosidic linkages
uated SSFs efficiency for producing enzymes. It is appro- between adjacent glucose units in the linear amylose chain
priate for the production of enzymes, especially because of [46], while glucoamylase hydrolyses the non-reducing ends
the higher enzyme yields that can be obtained compared to of amylose and amylopectin to glucose [47]. Amylases
submerged fermentation [4244]. SSF provides a similar have been widely used in the food, fermentation, textiles
environment to the microorganisms natural environment and paper industries [46], and they are also employed for
which provides better conditions for its growth and the pre-treatment of agroindustrial and organic by-products

Fig. 2 Simplified process flow

diagram for FW based
biorefinery concept

910 Waste Biomass Valor (2014) 5:903917

to improve the bioproduct yield in subsequent processes. cocktail rich in amylolytic and proteolytic enzymes to
High activity amylases can be produced from various kinds hydrolyze waste bread in SSF. The resulting fermented
of FWs, such as kitchen refuse [45], potato peel [43, 48], solids were added directly to a bread suspension to gen-
coffee waste [49] and tomato pomace [50] via the opti- erate a hydrolysate rich in glucose and free amino nitrogen.
mization of fermentation using different microbial strains. The bread hydrolyzate was then used as the sole feedstock
However, it is difficult to compare the efficiency of various for A. succinogenes fermentations, which led to the pro-
processes as the produced enzymes activities are defined duction of 47.3 g/L SA with 1.16 g/g glucose, which is the
in different ways (Table 2). The main advantage of enzyme highest SA yield compared with other FW-derived media
production from FW is that fermentation of FW would not reported to date. This consolidated process has potential to
require harsh pre-treatments and extra nutrient transform FW into SA.
Wang et al. [45] investigated the production of gluco- Lignocellulolytic Enzymes
amylase from FW by Aspergillus niger UV-60 using SmF,
and found that nutrient supplementation had no significant Lignocellulolytic enzymes composed of cellulases, xylan-
influence on the glucoamylase production. Maximum glu- ases and ligninases are mainly produced by several fungi.
coamylase activity of 137 U/mL was obtained using They can degrade the lignocellulosic materials. For
3.75 % FW and 5 % (v/w, 106 spores/mL) inoculum at example, cellulases have many applications in various
30 C, 120 rpm for 96 h. A reducing sugar concentration industries including food, animal feed, brewing and wine
of 60.1 g/L could be produced from 10 % FW (w/v) within making, agriculture, biomass refining, pulp and paper,
125 min using the produced crude glucoamylase. Shukla textile, and laundry [56]. The bioconversion of cellulose to
and Kar [43] also reported production of high activity a- fermentable sugars requires the synergistic action of com-
amylase from potato peels by SSF. Under optimal condi- plete cellulase system comprising of three enzyme classes:
tions (40 C, pH 7, particle size of 1 mm with 6570 % endoglucanases (EC which act randomly on solu-
moisture content), alpha-amylase activities obtained using ble and insoluble cellulose chains, exoglucanases (cello-
B. licheniformis and B. subtilis were 270 and 600 U/mL, biohydrolases; EC which liberate cellobiose from
respectively. In another study, a-amylase was produced the reducing and non-reducing ends of cellulose chains,
from potato peels by SmF with thermophilic isolate of and b-glucosidases (EC which liberate glucose
alkaline tolerant Bacillus firmus CAS7 strain [48]. Under from cellobiose [57]. Xylanases have many applications in
optimal conditions (at 35 C, pH 7.5 using 1 % of substrate food, feed, pulp and paper, brewing, wine making and
concentration), 676 U/mL of a-amylase was obtained. In textile industries with or without concomitant use of cel-
addition, Murthy et al. [49] used coffee wastes as sole lulases [58]. The hydrolysis of xylans mainly requires the
carbon source to produce a-amylase using SSF with a action of endo-b-1,4-xylanase and b-xylosidase. However,
fungal strain of Neurospora crassa CFR 308. a-amylase the presence of other accessory enzymes is needed to
activity of 4324 U/g dry substrate was obtained using 107 hydrolyse substituted xylans [59]. Lignin is an undesirable
spores/g dry substrate, 60 % moisture content at 28 C, pH polymer for biofuel production as it prevents the accessi-
4.6. It was also found that pre-treatment by steam improved bility of plant derived polysaccharides. However, lignin
the accessibility of coffee waste and the a-amylase activity derived materials can be used to develop valuable products
of 6,342 U/g dry substrate was obtained. such as dispersants, detergents, drilling mud thinner, sur-
FW can be used to produce high activity amylases using factants, coagulants and flocculants (for sewage and waste
suitable microbial strains. In studies of the lactic acid water treatment), adhesives, graft polymers including
production from FW, a saccharification step using com- polyurethanes, polyesters, polyamines and epoxies and
mercial amylases was included prior to the fermentation to rubbers [60, 61]. In order to degrade lignin polymers lig-
improve and ease the fermentation process [53, 54]. If the ninolytic enzyme mixtures consisting of laccases, lignin
enzyme production step can be integrated to the fermen- peroxidases and Mn-peroxidase are utilized.
tation system, the process costs could be lowered. The Lignocellulolytic enzymes are also used for the pre-
consolidated biorefinery concept using enzyme production treatment of the agroindustrial and organic by-products to
process from FW is shown in Fig. 2. FW can either be used improve the bioproduct yields in subsequent processes [62,
to produce enzymes only (pathway B) or the enzymes 63]. Table 3 summarizes recent studies on lignocellulolytic
production is integrated into a bioprocess for producing enzyme production using different FWs. Because the
biofuels or chemicals through fermentation (pathway A). enzyme activity can be defined in different ways, it is not an
Leung et al. [55] produced succinic acid (SA) from waste easy task to compare the achievements and identify the best
bread through pathway A presented in Fig. 2. Aspergillus method. However, fungal SSF is the most preferable method
awamori and Aspergillus oryzae produced an enzyme generally [6267]. Krishna [65] reported that the total

Waste Biomass Valor (2014) 5:903917 911

cellulase production from banana waste was 12-fold higher laccases, pectinases, and aryl-b-D-glycosidases (b-glucosi-
in SSF than that in SmF. However, Daz et al. [68] found that dases, b-xylosidases, and b-galactosidases).
SmF had higher xylanase production in comparison to SSF Biorefineries need to develop their indigenous enzyme
because of better aeration in SmF. In fact, Umsza-Guez et al. production processes along with their existing processes
[50] showed a clear positive effect of aeration on xylanase (Fig. 2, pathway A), as commercial enzyme production
and carboxymethyl cellulase (CMCase) production using systems are still expensive to incorporate in biorefineries
SSF in a plate-type bioreactor. [72]. As can be seen from the studies above, some strains
In general, the optimum conditions for SSF depend not are producing different lignocellulosic enzymes from food
only on the microorganism employed, but also on the type wastes simultaneously. These enzyme cocktails can be
of substrate. The incubation time, pH, temperature, particle used to hydrolyse biomass effectively at low cost for their
sizes and water content of the medium should be optimized conversion to biofuels or platform chemicals. To further
for given substrate and microorganism. Dhillon et al. [64] improve the hydrolysis, different strains can be co-cultured
investigated the effects of different inducers on cellulase to produce enzyme solutions with synergistic hydrolytic
and hemicellulase production by Aspergillus niger NRRL- effects. Furthermore, some engineered strains can be used
567 using apple pomace as a substrate. The highest filter to improve the saccharification yield.
paper cellulase (FPA) and b-glucosidase activities of
133.68 5.44 IU/gram dry substrate (gds) and Pectinolytic Enzymes
60.09 3.43 IU/gds, respectively were observed using
CuSO4 and veratryl alcohol. Similarly, the highest xylanase Pectinolytic enzymes, i.e. pectinases, degrade pectin
activity of 1,412.58 27.9 IU/gds was obtained with ve- polymers in a sequential and synergistic way, by depo-
ratryl alcohol after 72 h of fermentation, while the highest lymerisation and de-esterification reactions. Complete
CMCase activity of 172.31 14.21 IU/g ds was achieved degradation of pectin requires endo- and exo-acting po-
with lactose after 48 h of incubation. It has also been lygalacturonases and pectin- and pectate lyases as well as
reported that cellulase production using SSF was markedly enzymes rhamnogalacturonases that cleave the rhamno-
improved when lactose and corn-steep liquor was supple- galacturonan chain [73]. Pectinases are widely used in
mented to apple pomace [66]. food industry particularly for juice and wine production as
The cellulase production was found to be inhibited at well as many other industrial processes, such as textile,
high concentration of reducing sugars when grape pomace plant fiber processing, tea, coffee, oil extraction, industrial
was used as substrate [68]. To mitigate such inhibition, the wastewater treatment [42, 74, 75]. The pectinases can be
nutrients composition of grape pomace was adjusted by produced via fungal SSF particularly by using Aspergillus
supplementing orange peel which induced cellulase pro- strains [73]. Industrially, pectinases can be produced from
duction. Moreover, Umsza-Guez et al. [50] also reported pectin-containing wastes, such as citrus and orange wastes
that xylanase production from tomato wastes using SSF [7678], apple pomace [79, 80], grape pomace [69] or
was activated by Mg2?, but strongly inhibited by Hg2? and other fruit residues [81] without any harsh pre-treatment
Cu2?. owing to the nature of these substrates and the low
The substrate pre-treatments may affect the production moisture content [74, 81]. Hours et al. [80] investigated
of cellulase and xylanase. For instance, Krishna [65] the pectinase production from apple pomace by SSF using
investigated the effects of acid, alkaline and heat pre- Aspergillus foetidus. After 36 h culture at 30 C with
treatment on cellulase production from banana waste using nitrogen supplementation, an enzyme activity of 1,300
Bacillus subtilis. Although cellulase production was not U/g was obtained (Table 4).
affected by alkali or acid treatment, it increased 6.84-fold Pectinolytic enzyme was also produced from citrus
after pretreatment of FW by pressure-cooking at controlled waste using Aspergillus foetidus in SSF [77]. It was found
pH. This greatly improved substrate accessibility for that addition of yeast extract and minerals improved the
microbial growth, without the formation of monosaccha- activity significantly after 36 h of culture. Berovic and
ride degradation products, such as furfural and hydroxy- Ostroversnik [79] reported that the pectolytic enzyme
methyl furfural, which otherwise inhibit the cellulases [71]. production from apple pomace was induced and/or
Besides cellulases and xylanases, ligninases were also improved by cheap nutrients such as soya flour, wheat
produced from FWs by white rot fungi. Zilly et al. [70] bran, wheat corn and whey. They also mentioned that
studied the oxidative and hydrolytic enzymes production moisture content was very important in enzyme production
by SSF of yellow passion fruit waste using white-rot fungi and the highest activity was obtained at 38 % initial
Pleurotus ostreatus, Pleurotus pulmonarius, Macrocybe moisture content. However, Ruiz et al. [42] reported that
titans, Ganoderma lucidum, and Grifola frondosa. Under 70 % moisture content gave the highest pectinase activity
the conditions used, the main enzymes produced were using lemon peel pomace.

912 Waste Biomass Valor (2014) 5:903917

Botella et al. [74] evaluated the feasibility of grape important essential oil for cosmetics, foods and pharma-
pomace for the production of exo-polygalacturonase by ceutical industries. D-limonene can be extracted using
Aspergillus awamori in SSF. The particle size of the sub- suitable solvents. The residue after limonene extraction,
strate did not influence the enzyme production as it was consisting mainly of pectin and lignocellulose, is an
reported by Hours et al. [80], while the addition of carbon excellent source for pectinolytic and lignocelluloytic
sources and the initial moisture content of grape pomace enzyme production and for the growth of microorganisms
were found to have a marked influence on enzymes yields. to generate high value products such as industrial enzymes,
In another study, Giese et al. [78] carried out the produc- ethanol, methane and single cell proteins. Moreover, the
tion of pectinases from orange waste by Botryosphaeria residual biomass i.e. lignin can be used as an energy
rhodina MAMB-05 in SSF and SmF with and without source.
adding nutrients. A better microbial growth was observed
and the highest pectinase titre (32 U/mL) was obtained in Proteases
SSF of orange bagasse without adding nutrients.
Aeration is another important parameter affecting the Proteases are one of the most important commercial
pectinase production. Umsza-Guez et al. [50] reported that enzymes because of their wide range of applications in
the forced aeration had a negative effect on exo-PG syn- food, pharmaceutical, detergent, dairy and leather indus-
thesis, reducing its activity to half in a multi-layer packed tries [8790]. Some fungal strains such as Aspergillus,
bed reactor. MacIel et al. [83] obtained the maximum endo- Penicillium and Rhizopus and bacteria of genus Bacillus
and exo-PG activities of 1.18 U/mL and 4.11 U/mL, have been reported as the most active producers of prote-
respectively, using the reactor without aeration. Obviously, ases [51, 87, 91]. Although protease production from agro-
a system without aeration is preferable because of opera- industrial wastes has been well studied in detail using both
tional and economic considerations. SSF and SmF, the utilization of FWs for protease pro-
The pH value of the medium can also affect the pec- duction is not well documented (Table 5). Khosravi-Darani
tinase production. Martnez Sabajanes et al. [81] investi- et al. [91] used a newly isolated alkalophilic Bacillus sp. in
gated the effect of different substrates (apple, lemon peel, SmF of date wastes. High activity protease (57,420 APU/
grape skin & tamarind kernel) and fungi (Aspergillus mL) was obtained at pH 10, 37 C and the enzyme was
flavipes FP-500 and Aspergillus terreus FP-370) on the reported to be thermostable, indicating its possible utili-
production of pectinases. The highest activities were zation in industrial applications. Afify et al. [92] investi-
obtained using lemon peel. In both strains, acidic pH values gated the production of proteases from potato waste in a
and high carbon source concentration favoured exopectin- submerged system using S. cerevisiae and studied the uti-
ase and endopectinase production, while higher pH values lization of remaining solid waste as a biofertilizer for plant
and low carbon source concentration promoted pectin lyase growth. The highest enzyme activity (360 U/mg) was
and rhamnogalacturonase production. obtained using a fermentation medium containing 15 g
In summary, fruit wastes are preferable substrates for potato waste, at an initial pH of 6.0, at 20 C for 72 h. In a
producing high titers of pectinolytic enzymes using either study of Gupta et al. [88], fishmeal from sardine and pink
SSF or SmF. Process parameters including medium pH, perch were evaluated as a sole carbon and nitrogen sources
temperature, composition, inoculum size, moisture content using Bacillus pumilus MTCC 7514. The protease obtained
and particle size of the substrate and aeration highly in medium containing only fish meal (4,914 U/mL) was
depend on the substrate and microbial strain. Statistical nearly two times higher than that using basal medium
experimental designs can be employed to optimize the (2,646 U/mL). The protease production was enhanced to
fermentation conditions by evaluating the effects and 6,966 and 7,047 U/mL when scaled up from flask to 3.7
interactions of the different parameters that rule a bio- and 20 L fermenters, respectively. The crude protease was
chemical system. found to have dehairing properties in leather processing. In
There is no industrial scale FW biorefinery facility another study [93], P. aeruginosa MN7 was found to grow
currently in operation. However, there are some studies and over-produce proteolytic enzymes (15,000 U/mL) in
reporting the technical advances and engineering chal- media containing only shrimp wastes as sole substrate.
lenges of orange and lemon waste biorefineries [84, 85]. Although there are a few reports on protease production
Direct utilization of citrus peel as animal feed is the sim- from FW, the appreciable protease activities obtained on
plest option, requiring little infrastructure or investment, different FW residues highlighted the potential of these
while increasing the value of the waste material signifi- wastes.
cantly [85]. However, citrus peel contains high value Besides its potential utilization in many industrial
compounds such as pectin and D-limonene [86]. Pectin is applications, proteases produced from FW can also be used
frequently used in food processing, while D-limonene is an for biorefining different biomasses. Koutinas et al. [95]

Waste Biomass Valor (2014) 5:903917 913

evaluated an oat-based biorefinery for the production of [105] the biodegradation of waste cooking oil and its
lactic acid as well as other value-added by-products, such application as an inducer in lipase production by Yarrowia
as b-glucan and antioxidant-rich oils using Rhizopus ory- lipolytica CECT 1,240 were investigated. The addition of
zae. Rhizopus oryzae produced a range of enzymes (glu- waste cooking oil to the medium led to a significant
coamylase, protease, phosphatase) during the hydrolysis of increase in extracellular lipase production by the yeast,
complex macromolecules in oat. The utilization of waste compared to oil-free cultures. Papanikolaou et al. [106]
biomass and in situ produced enzyme cocktails in such a explored the effects of different Aspergillus and Penicil-
biorefining strategy could lead to significant operating cost lium strains using waste cooking oil as substrate. In car-
reduction as compared to current industrial practices for bon-limited medium, the highest amount of biomass (18 g/L)
lactic acid production from pure glucose achieved by with a lipid content of 64 % was obtained using Asper-
bacterial fermentations. gillus sp. ATHUM 3482, while the highest extracellular
lipase activity (645 U/mL) was obtained by Aspergillus
Lipases niger NRRL 363. The studies above indicated the great
potential of FW either as substrates or inducers for lipase
After proteases and carbohydrases, lipases (EC are production. Lipase production can be further improved
considered as the third largest group based on total sales using mutant or engineered strains.
volumes [96]. They are widely used for several applica- Lipases are also used for biodiesel production from
tions in food, detergent, cosmetics, organic synthesis and crude oil and fats [113] either in free or immobilized form.
pharmaceutical industries. They are catalysing the hydro- Lipase production processes from FW can be integrated in
lysis of triacylglycerols to di- and mono- acylglycerols, a biodiesel biorefining process to decrease the transesteri-
fatty acids and glycerol [9799]. They are also able to fication cost. Phospholipases are used for oil degumming
catalyze alcoholysis, acidolysis, aminolysis, esterification and for increasing fatty acid yields [114]. Further research
and transesterification under certain conditions [100]. should be carried out on phospholipase production using
Phospholipases are a sub-class of lipases that catalyse the FW (Fig. 2, Pathway B).
hydrolysis of one or more ester and phosphodiester bonds
of glycerophospholipids. They vary in site of action on
phospholipid which can be used for the modification/pro- Conclusions
duction of new phospholipids for some applications in oil
refinery, health, food manufacturing, dairy and cosmetics The management of FWs has posed a serious economic and
industries [101]. environmental concern. This review highlighted the
Most of the research has focused on high activity potential of food waste to obtain high titres of industrial
extracellular lipase production using both SmF and SSF enzymes such as amylases, cellulose, pectinases, proteases,
via a wide variety of microorganisms including bacteria, and lipases. The produced enzymes could be used in some
fungi, yeast and Actinomyces [98, 99, 102, 103]. Several industrial applications depending on FW transportation
strains of commercial lipase producing fungi are quite costs and purity requirements. Moreover, these enzymes
dominant, including Rhizopus, Rhizomucor, Aspergillus, can be integrated in other bioprocesses in biorefineries to
Geotrichum, Yarrowia and Penicillium species [104]. produce biofuels and platform chemicals.
Recently, the production of lipase was investigated by So far, biorefinery processes for the conversion of FW
several researchers using different FW as substrates [97] or into ethanol and other value-added products have only
by supplementing FW as inducer [105, 106]. Alkan et al. been achieved at bench-top and pilot levels. There is no
[97] investigated the production of lipase from melon industrial scale FW biorefinery facility currently in
waste by SSF using Bacillus coagulans. The highest lipase operation. Therefore, it is not possible to conduct an
production (78.1 U/g) was achieved after 24 h of cultiva- economical analysis for the proposed biorefinery systems.
tion with 1 % olive oil enrichment at 37 C and pH 7 by However, considering the cost of defined medium prep-
supplementing sodium dodecyl sulphate (Table 6). The aration in current commercial enzyme processes, the uti-
best results were obtained by supplementing starch and lization of low or no cost waste biomass could lead to
maltose (148.9 and 141.6 U/g, respectively), whereas a significant reductions in operating costs. However, diffi-
rather low enzyme activity was found in cultures grown on culties and costs associated with the collection/transpor-
glucose and galactose (approximately 118.8 and 123.6 U/g, tation of FW should also be taken into account.
respectively). Enzymes were inhibited by Mn2? and Ni2? Optimization and scale up studies need to be carried out
by 68 and 74 %, respectively. By contrast, Ca2? enhanced in order to exploit FW for enzymes applications at larger
enzyme production by 5 %. In a study of Dominguez et al. scale.

914 Waste Biomass Valor (2014) 5:903917

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