fermentation

Review
Production of Oligosaccharides from
Agrofood Wastes
María Emilia Cano 1 , Alberto García-Martin 2 , Pablo Comendador Morales 2 ,
Mateusz Wojtusik 2 , Victoria E. Santos 2 , José Kovensky 1 and Miguel Ladero 2, *
1 Laboratoire de Glycochimie, des Antimicrobiens et des Agroressources CNRS UMR 7378,
Université de Picardie Jules Verne, 80025 Amiens, France; maria.emelia.cano@u-picardie.fr (M.E.C.);
jose.kovensky@u-picardie.fr (J.K.)
2 Chemical Engineering and Materials Department, Chemistry College, Complutense University,
28040 Madrid, Spain; albega13@ucm.es (A.G.-M.); pabcomen@ucm.es (P.C.M.); mwojtusik@ucm.es (M.W.);
vesantos@ucm.es (V.E.S.)
* Correspondence: mladerog@ucm.es; Tel.: +34-91-394-4164




Received: 25 December 2019; Accepted: 5 March 2020; Published: 8 March 2020


Abstract: The development of biorefinery processes to platform chemicals for most lignocellulosic
substrates, results in side processes to intermediates such as oligosaccharides. Agrofood wastes
are most amenable to produce such intermediates, in particular, cellooligo-saccharides (COS),
pectooligosaccharides (POS), xylooligosaccharides (XOS) and other less abundant oligomers
containing mannose, arabinose, galactose and several sugar acids. These compounds show a
remarkable bioactivity as prebiotics, elicitors in plants, food complements, healthy coadyuvants in
certain therapies and more. They are medium to high added-value compounds with an increasing
impact in the pharmaceutical, nutraceutical, cosmetic and food industries. This review is focused on
the main production processes: autohydrolysis, acid and basic catalysis and enzymatic saccharification.
Autohydrolysis of food residues at 160–190 ◦ C leads to oligomer yields in the 0.06–0.3 g/g dry solid
range, while acid hydrolysis of pectin (80–120 ◦ C) or cellulose (45–180 ◦ C) yields up to 0.7 g/g dry
polymer. Enzymatic hydrolysis at 40–50 ◦ C of pure polysaccharides results in 0.06–0.35 g/g dry solid
(DS), with values in the range 0.08–0.2 g/g DS for original food residues.

Keywords: biorefinery; food waste; oligosaccharides; saccharification; (bio)catalysts; prebiotics

1. Introduction
When considering abiotic resources, including all mineral and fossil resources, there is a progressive
perception that, while new extraction technologies and their careful and efficient use will lead to a
long-term availability with an increasing price per ton, their use will be ultimately restricted to the
higher value-added applications as their depletion progresses, according to the Hubbert peak theory [1].
Thus, in terms of sustainability, the need of renewable resources to turn linear feedstock processing
and use to a circular one, seems evident to integrate human activities within natural cycles with the
lowest impact possible [2]. In this aspect, Circular Integration emerges as a mixture between Circular
Economy, Industrial Ecology and Process Integration as a strategy to optimize the use of material
and energy resources and maximize the cyclic nature of resource use [2]. To this end, renewables
resources of solar origin, including water and air convective movements for energy and biomass
for energy, food, feed, chemicals and materials should play a progressively important role in facing
human needs while avoiding resource depletion and irreversible impacts to the Planet [2,3]. Plants
and algae are able to turn solar energy and simple chemical compounds into organic matter by means
of photosynthesis, and their productivity in this sense can be intensified by genetic, chemical, agro and

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Fermentation 2020, 6, 31 2 of 27

forestall engineering approaches, to name a few. Lignocellulosic biomass, of any origin is, therefore,
a most promising raw material for biorefineries, considering such facilities as integrated refineries
turning biomass into fuels, platform chemicals, food, feed and materials using integrated processes
with an optimized used of resources [4]. This vision can be extended to resources of aquatic origin
(seaweed, seagrass and microalgae) as well as residues from livestock [5,6]. In general, apart from
forestall and energy crops biomass, most of it depends on the production of biomass and, in particular,
food wastes [7,8]. While more than 100,000 M tons of biomass wastes are yearly produced [7], wastes
strictly considered as food wastes (foods not consumed from any part of the food supply chain or
any part of the food that is non edible and, therefore, becomes a residue) account for more than
1300 M tons each year [8]. The valorization of biomass wastes into a plethora of useful energy vectors,
chemical compounds and ingredients receives a notable amount of interest from all stakeholders,
including researchers and entrepreneurs. They are a source to several value-added products, such as
monosaccharides (glucose, xylose, mannose, fructose, arabinose and more), oligosaccharides (fructo-
or FOS, xylo- or XOS, galacto- or GOS, galacturonic- or GALOS, lactosucrose, etc.), biofuels (ethanol,
butanol, dimethylether –DME-, biodiesel, hydrogen), bioactive compounds (flavonoids, phenolic acids,
terpenes, terpenoids, carotenoids), nanocellulose (bacterial, wood-related), lignin and its derivatives
(a source of aromatics from biomass and prospective substitute of the aromatic or BTEX fraction
produced in oil refineries) [8]. Oligomers from cellulose, hemicellulose, lignin, pectin and other
biomass-related polymers, as chitin, compose a class of value-added compounds with an enormous
potential. As indicated by Bhatia et al. [9], their bioactivity turn them into useful ingredients for
cosmetics, foods and drugs, and they can be applied, prospectively, to almost countless applications in
health improvement and new therapeutic approaches (gut health, immune system boosting, cancer
treatment, anti-adhesive action, to name some applications in this area). They can be obtained
from several wastes related to food and agriculture, such as, for example, vine shoots [10], banana
peels [11], sugar beet residues [12] and wheat chaff [13]. Agrofood related waste is a rich source of
mannooligosaccharides [14], while oligomers such as those from alginate, agarose and κ-carrageenan,
can be derived from macroalgae [15].
Lignin oligomers are notorious for their rich variability and number of functional groups, rendering
them valuable platform chemicals for their application in commodity and advance materials and
coatings [16]. Nevertheless, lignin depolymerization is nowadays complex to control, while lignin
itself is relatively inert as a material ingredient, an aspect that hinders its inclusion into novel materials.
Effective lysis to polyols, with their importance in polyurethane formulation, seems a promising
application of the abundant lignin (accounting for 15–40% dry weight of lignocellulosic biomass). To
render it more reactive, lignin can be turned into lower molecular weight fractions by an assortment of
catalytic routes (acid, basic, with metal oxides, ionic liquids and enzymes) and in sub- and supercritical
conditions using several solvents. However, up to now, these processes should be enhanced notably both
from the technical perspective, facing catalysts deactivation and lignin repolymerization, and from the
economical viewpoint, as harsh pressure and temperature conditions turn these operations unfeasible [16].
In later years, there is an increasing evidence of cellooligomers (COS) utility in the formulation
of food complements for calves in the preweaning period, when they are developing their ability
to digest cellulose and the intake of cellooligosaccharides can help them to develop a better rumen
environment [17]. COS could be used together with isoflavones as a valuable food complement to
reduce bone fragility when estrogen concentrations are low, i.e., during menopause and afterwards [18].
COS are less studied than other oligosaccharides, due to the refractory nature of cellulose itself, a very
high molecular weight biopolymer. It can present up to 90%–95% crystallinity and is organized into
tightly bonded bundles named microfibrils, which conforms higher-order bundles or macrofibrils. They
are obtained from lignocellulosic sources by depolymerization, either by hydrolysis or by oxidative
routes. Hydrolysis of residual cellulose can be achieved using endo- and exoglucanases with a reduce
activity of β-glucosidases [19] or modified carbon catalysts [20]. Enzyme-driven lytic oxidation is
performed with polysaccharide monooxygenases (LPMOs) [21], enzymes that are present nowadays
Fermentation 2020, 6, 31 3 of 27

in most up-to-date cellulolytic enzyme industrial preparations. β-glucosidases not only hydrolyze
cellobiose but they can catalyzed the reverse reaction (transglycosilation) to render C2, C3, C4 and C5
COS (cellobiose, cellotriose and higher molecular weight oligosaccharides) in the presence of relatively
low concentrations of water [22].
The hemicellulose fraction in lignocellulosic biomass is a rich source of xylooligosaccharides and
mannooligosaccharides. Hemicellulose can reach up to 35% in corncob and 25% in nutshell, with similar
values for straws, corn stover, sugarcane bagasse and other food-related wastes [9–11,23]. Hemicelluloses
are linear-ramified heteropolysaccharides with a relatively low molecular weight (circa 15 kDa) very rich
in xylose, galactose, fructose, glucose and mannose. One of the main polymer fractions in hemicelluloses
is xylan, a polymer of xylose linked by β-1,4-xylosidic bonds that can be depolymerized by acid,
enzymatic, mechanical and thermal operations (and some of their combinations) to xylooligosaccharides
(xylobiose, xylotriose, up to xylodecaose) or XOS. In particular, acetic acid pretreatment enhances
endoxylosidase action, reducing the associated costs [24]. XOS have a recognized potential as prebiotics,
being a common ingredient of food complements [9,10]. They are also present in cosmetics, used as
gelling agent and for the treatment of diabetes [9,25]. They are also active as immunomodulators
and immunostimulators, and their antioxidant activity can be notable too [9]. However, their
cost is a major concern to exploit all their potential, with prices in the 40–80 USD/kg range [9].
Mannooligosaccharides can be derived from mannans (both α- and β-mannans, from yeasts and plants,
respectively), glucomanans, galactomanans and glucogalactomannans, that can be degraded by an
assortment of enzymes acting on the β-1,4-linkages between the glycosidic moieties: β-mannanases,
β-mannosidases, β-glucosidases and some auxiliary enzymes (α-galactosidases and acetyl mannan
esterases). Antitumor and antimetastatic action of mannans and glucans is well-studied [26]. This
property is also present in their oligomers, which also show a prebiotic activity that controls microbiota
population in the gastrointestinal tract [9,26].
A well-known heteropolysaccharide in vegetable and fruit peels is pectin. Its composition and
structure are notably more complex than the ones of the other polysaccharides typically encountered
in lignocellulosic biomass [27]. Linear regions conformed only by α-1,4 linked galacturonic acid are
known as homogalacturonans, while there are other parts of pectin rich in rhamnose that are branched
or hairy regions. Rhamnogalacturonan I contains a main chain of rhamnose and galacturonic acid
with lateral chains of galactose and arabinose, with several types of bonds. Rhamnogalacturonan
II can contain, apart from all those monomers previously mentioned, other rare ones as apiose and
aceric acid [27]. Though pectin is a typical food ingredient for jellies, marmalades and jams, its slow
degradation in the intestine permits its use with calcium salts to treat diarrhea, it can ameliorate diverse
colon cancer, promoting gut health by controlling microbiota populations (a prebiotic effect) [27,28].
Oligosaccharides derived from pectin potentially maintain and even increased pectin bounties in gut
health, and can be produced from a diversity of peels and pulps from beet, citrus species, apple pomace
and other fruit waste [9,12,28].

2. Autohydrolysis Processes

2.1. Definition and Main Process Variables

Autohydrolysis is a hydrothermal pretreatment based on the use of pressurized water. When water
is above 120 ◦ C, ionization processes are promoted so that the H3 O+ concentration increases. According
to [29], hydronium ions concentration at 250 ◦ C is 23.3 higher than the one at 25 ◦ C. As consequence,
hemicelluloses and pectin (depending on the biomass) are subjected to depolymerization. Once this
happens, acetic acid and uronic acids are released, which enhances the depolymerization process. In
fact, the contribution of these acids to H3 O+ formation is much higher than the water dissociation
contribution [29]. Autohydrolysis can be a process that renders a high yield of oligosaccharides, as
it allows minimizing the monomers and degradation products by adjusting the principal variables
involved: time and temperature [30,31].
Fermentation 2020, 6, 31 4 of 27

Although this method was firstly developed for the fractionation of lignocellulosic biomass by
dissolving the hemicellulose fraction, it was successfully used for pectin depolymerization [32].
The hydrolysis mechanism includes the following steps [33]: i) migration of the protons to the
solid surface, ii) chemisorption, iii) reaction between the proton and the polysaccharide in the surface,
iv) cleavage and desorption of oligosaccharides and v) diffusion of the oligomers to the bulk liquor.
Usually, the chemical reaction step is the rate-controlling one [33]. The main process variables are:
(1): Particle size: a small particle size increases surface area, porosity and improves flow properties.
A big size leads the surface to overreact whereas the inside part would be incompletely hydrolyzed.
However, it is important to take into account that the energy demand associated to milling is high so a
compromise should be reached [34].
(2): Liquid-solid ratio (LSR): This value can vary from 2 to 40 g water/g dry material but it is
usually between 8–10 g/g [35]. A low LSR increases acetic and uronic acids concentration, improving
autohydrolysis efficiency. Furthermore, energy requirements during the reaction and purification
processes can be reduced, resulting in lower operating costs and wastewater generation [36]. However,
it is important to select a LSR value taking into account that a good impregnation of the material is
necessary. The value also depends on the water retention capacity of the biomass [37].
(3): Temperature/time: these factors affect significantly the process and are usually grouped in
one parameter: the severity factor [37]. It will be described below.
(4): pH: controlling and monitoring the pH during the process improves the selectivity to
oligomers and minimizes a further reaction of this compounds to monomers and degradation products.
Maintaining the pH above 4.0 limits the hydrolysis of polysaccharides and the formation of degradation
products [38,39].
As commented above, in order to compare experiments in different conditions, severity factor
is commonly used. It was firstly proposed by [40] for pulping processes, assuming that the overall
kinetics follow a first-law concentration dependence and the rate constant has an Arrhenius type
dependence on temperature. In addition, there are slight modifications of this general model in order
to include different operational conditions such as non-isothermal temperature profiles [41] or low pH
levels [42,43] in a combined severity factor.
According to the temperature profile, the treatment can be isothermal or non-isothermal. In
the first case, once the target temperature is reached, it is maintained during the reaction time and
then, the reactor is cooled down [44]. In the second case, once the target temperature is reached, the
reactor is cooled down [45]. It is accepted that higher temperatures and shorter reaction times lead to
higher pentoses yield and minor degradation products formation [37]. Furthermore, molecular weight
distribution of oligosaccharides depends on time and temperature [46]. For a given temperature, an
increasing reaction time lead to the accumulation of low molecular weight oligosaccharides.
Regarding to the reaction system, there are several reactor configurations that can be used in
order to carry out the autohydrolysis process: batch reactor, semi-continuous reactor or continuous
reactor [34]. The most commonly used is batch operation [37]. Finally, it has been reported that this
process has several advantages over other treatments [47,48]:
(1): Reduced chemicals consumption. Acetyl groups naturally present in biomass are liberated,
leading to an increase in acetic acid concentration, which catalyzes the process.
(2): Solubilization of hemicelluloses and pectic fractions as oligosaccharides and monosaccharides
with limited generation of degradation products.
(3): Both solid and liquid resulting from the process are valuable products. The liquid is rich
in oligosaccharides and the solid is an adequate substrate for further fractionation (by enzymatic
hydrolysis, for example).
(4): Low capital cost due to low corrosion potential.
Fermentation 2020, 6, 31 5 of 27

2.2. Application to Lignocellulosic Waste Residues

Autohydrolysis, which is a hydrothermal treatment, was at first used for the fractionation of
woody biomass. Between 1970 and 1980, this process was employed in the delignification of different
woods [49]. During the next decade, it was used as a pretreatment in order to maximize the accessibility
to cellulose, which can be hydrolyzed (chemical or enzymatic treatment) to simple sugars and use
them to produce biofuels or other chemicals [50–52].
In the 1990 decade, several studies showed the health properties of xylooligosaccharides [53,54],
so the autohydrolysis started to gain attention not only as a method to enhance cellulose hydrolysis
but a method to produce this kind of oligosaccharides selectively [55]. In 1999, it was the first time the
autohydrolysis was used focusing attention into oligosaccharides production. Degradation kinetics of
this fraction was studied, taking into account the xylan depolymerization into xylooligosaccharides
and xylose. Xylose degradation products were also studied [30]. This study sets the bases for a new
environmentally friendly method for hemicelluloses valorization.
From that moment on, several studies came up trying to apply this technology on different
materials such as woods, agroindustrial and food wastes. Food wastes are especially interesting since
they are produced in huge quantities, as commented in the introduction. They can be grouped in two
categories: those generated within the raw material conditioning (Table 1) and those generated within
the raw material processing or consumption (Table 2).
The food wastes in the first group contain a high xylan content so that the liquors obtained by
autohydrolysis are rich in xylooligosaccharides.
Arabinan, which is usually present in these lignocellulosic residues, is more susceptible to
hydrolysis than xylan, so the optimum conditions for XOS production (Table 1) are not the same as the
ones for AROS production (190 ◦ C, 36 min heating) [45,56,57]. In these studies, a similar conversion
from xylan to XOS in similar conditions has been reported (65.6% for corncob, 64.3% for rice husks and
67% for barley husks). However, the degree of polymerization of these compounds is not mentioned.
When almond shells are treated, an increase in the severity of the process lead to
xylooligosaccharides with a low degree of polymerization (xylobiose and xylotriose) [58]. However,
due to the low concentration of these XOS (3.3 g/100 g dry solid—DS), enzymatic hydrolysis (leading
to a yield of 8.2 g/100 g DS) and purification steps of the liquors were added.
In some cases, in addition to XOS, small amounts of galactooligosaccharides and
glucooligosaccharides are obtained [44]. Maximum concentration of these compounds (10.1 g/L
XOS, 0.7 g/L GAOS, 0.11 g/L GOS) were found at severity factors between 3.7–3.8. Below these
severity factors, polysaccharides solubilization is low and, above these values, concentrations of
monosaccharides and degradation products increase. Additionally, less than 30% of the produced
xylooligosaccharides (0.025 g/g DS) have a degree of polymerization (DP) lower than 6 in the indicated
conditions. However, the percentage can improve up to 37% (0.04 g/g DS) with a severity factor of
4.02. In this case, a lower concentration of total XOS (9 g/L instead of 10 g/L) is obtained. It shows that
temperature and holding time should be adjusted precisely to obtain XOS with the desired DP.
By comparing references [46] and [59], we can appreciate that the optimum severity factor for
the production of XOS from brewer’s spent grains is 3.64 and that arabinan degradation is faster than
xylan degradation, as commented above. The novelties in the last reference mentioned are the previous
extraction of starch from the grains, which affects the prebiotic potential of the mixture obtained, the
study of the main substituents (uronic acids and acetyl groups) in the XOS produced, and the partial
enzymatic hydrolysis step (using endoxylanases) added to reduce the average molecular weight of the
oligosaccharides produced.
Gullón et al. reported that, at relatively low severity factors (2.7), the solubilization of
polysaccharides is higher in chestnut shells (24.5%) [60] than in other residues such as hazelnut
shells (12.3%) [16]. In optimum conditions (180 ◦ C, severity factor = 3.08), 7.1 g/L XOS and 6.8 g/L
GOS were obtained. Arabinooligosaccharides and galacturonicoligosaccharides are more reactive its
concentration was very low. The use of less severe conditions compared to other materials permits to
Fermentation 2020, 6, 31 6 of 27

obtain substantial quantities of antioxidant compounds. In the work of Rico et al. [61], for example, a
severity factor of 4.09 was needed to obtain 7.6 g/L of XOS, which lead to low concentrations of GOS,
AROS (0.45 and 1 g/L) and antioxidant compounds.
Vine shoots could be an adequate feedstock for XOS and GOS production obtaining 12.2 g/L and
8.64 g/L, respectively, with a severity factor of 4.01 [62]. Other oligosaccharides were observed in
small quantities (AROS, GALOS, MANOS). A further observation showed that the polydispersity of
the hemicellulosic fraction decreased with higher severity, which indicates that the molecular weight
distribution become narrower.

Table 1. Main results in autohydrolysis studies on wastes from raw material conditioning.

Year Residue Treatment Conditions Reactor Product (g/g DS) Ref.

Stainless steel Parr reactor
V= 3.75.
2 Rushton turbines.
202 ◦ C
Autohydrolysis Heating with external XOS (0.20 g/g)
2002 Corncob 39 min (heating) [44]
non-isothermal fabric mantles and cooled AROS (0.016 g/g)
LSR = 8
by internal stainless steel
loops. PID-controlled
Temp.
212 ◦ C
Autohydrolysis XOS (0.10 g/g)
2004 Rice husks 45 min (heating) Parr reactor [56]
non-isothermal GOS (0.027 g/g)
LSR = 8
202 ◦ C
Autohydrolysis
2004 Barley husks 39 min (heating) Stainless steel Parr reactor XOS (0.18 g/g) [57]
non-isothermal
LSR = 8
200 ◦ C 1.5 L stainless steel 5100
Autohydrolysis XOS (0.10 g/g)
2016 Vine shoots LSR = 8 Parr reactor. [62]
non-isothermal GOS (0.069 g/g)
H = 4.01 PID-controlled Temp.
190 ◦ C High-pressure reactor
5 min (heating) (BR-300) 0.6 L stainless
Hazelnut Autohydrolysis 5 min (holding) steel tank with heating
2017 XOS (0.10 g/g) [44]
shells isothermal LSR = 10 block. Paddle agitator.
N = 300 r.p.m. Tap water cooling
H = 3.92 through internal coil.
1.5 L stainless steel
180 ◦ C
Chestnut Autohydrolysis reactor using a Parr PID XOS (0.057 g/g)
2018 LSR = 8 [60]
shells non-isothermal controller to control GOS (0.054 g/g)
H = 3.08
temperature
210 ◦ C
Autohydrolysis 0.6 L stainless steel
2018 Peanut shells LSR = 8 XOS (0.061 g/g) [59]
non-isothermal reactor (Parr 4842)
H = 4.09
200 ◦ C 1 L stainless steel 316
High DP XOS
20 min (heating) pressure reactor with
Almond Autohydrolysis (0.077 g/g)
2019 5 min (holding) provision for water [58]
shells isothermal Low DP XOS
LSR = 10 circulation.
(0.033 g/g)
H = 3.94 PID-controlled Temp.
Note: H is the severity factor (Log (R0)).

The second group of wastes, whose autohydrolysis results are shown in Table 2, is characterized
for being rich in other polysaccharides different from xylan, such as pectin or arabinan, which make
them softer and more susceptible to hydrolysis. Residues with high content in pectin are orange peels,
lemon peels, sugar beet pulp, apple pomace, passion fruit peels and olive by-products. Sugarcane
bagasse and coconut meal are rich in xylan and mannan, respectively.
Optimum conditions for orange peels [63], lemon peels [64] and sugar beet pulp [65] autohydrolysis
are very similar (160 ◦ C, severity factor = 2.5), for the same LSR. Liquors from sugar beet pulp contain
a high concentration of arabinooligosaccharides (13 g/L), whether the ones from orange and lemon
peel are rich in pectooligosaccharides (17 g/L and 21 g/L respectively). The overall amount of
Fermentation 2020, 6, 31 7 of 27

oligosaccharides obtained is higher for sugar beet pulp (31.2 g/100 g oven-dry biomass). Furthermore,
evidence in all experiments indicates that acetyl substituents in oligosaccharides decrease drastically
at temperatures higher than 160 ◦ C, resulting in high monosaccharides and degradation products
concentration. The conditions of sugar beet pulp autohydrolysis were optimized for the production of
feruloylated arabinooligosaccharides [65]. The operation in a continuous flow reactor is also studied for
scaling-up, which leads to similar results in terms of AROS production, but achieving a considerable
reduction in the residence time.
Pectin extraction from apple pomace and citrus wastes has also been studied [66]. Although
the aim of this study is to assess the properties of the pectin extracted, it can be extrapolated that
autohydrolysis is suitable for pectin extraction and further depolymerization (as seen in [63] and [64]
for orange and lemon peels). For apple pomace, the highest yield of pectin (40.13% w/w) was obtained
at 150 ◦ C, maintaining this temperature during 5 minutes. The pectin extracted had lower molecular
weight than the one extracted by conventional methods, establishing the suitability of autohydrolysis
for pectin depolymerization. This apple pomace pectin has more galactose and less arabinose than
citrus pectin. This study set a basis for further investigations in pectic oligosaccharides production
from apple pomace.
Another common peel residue, fruit peel passion peels, which are composed mainly of pectin
and cellulose, were subjected to autohydrolysis. The results obtained were similar to those for orange
peels [67]. The best conditions for oligosaccharides production were achieved at a similar severity
factor (2.21), being the yield to total oligosaccharides 0.21 g/g DS, from which 0.14 g corresponded to
POS and 0.05 g to GOS. Therefore, most glucan may come from the hydrolysis of starch and not from
cellulose. In addition, hemicelluloses were more difficult to hydrolyze than pectin.
As a very common agricultural subproduct, with more than 46 Mtons/year production, sugarcane
bagasse autohydrolysis was also studied aiming to higher yields of low DP XOS, which were maximized
at 200 ◦ C with a reaction time of 10 min [68]. Then, 11.63 g/L of xylooligosaccharides were produced, of
which 98% had a degree of polymerization between 2 and 5. The effect of acetyl groups in the biomass
was also studied by adding a 35% of white birch (similar composition to sugarcane bagasse but higher
content in acetyl groups) to the mixture. The total amount of XOS obtained at 160 ◦ C and a reaction
time of 100 min was almost the same as that produced at 200 ◦ C and 10 min without white birch, which
indicates that the addition of acetyl groups increases the total amount of XOS and reduces the average DP.
A common residue from olive oil production, alperujo, has also been treated by autohydrolysis
under a special configuration based on steam processing [69]. It was possible to obtain different fractions
of oligosaccharides (POS, XOS and GOS) with specific range of molecular weight by fractionation
through chemical hydrolysis (HCl, 70 ◦ C, 2h), ultrafiltration and enzymatic hydrolysis (endo- and
exo-polygalacturonases, pectinesterases and pectinliases, 40 ◦ C, 72h) after the mild steam processing.
As seen in other studies, a mild autohydrolysis process makes it possible to obtain high molecular
weight oligosaccharides.
Autohydrolysis of coconut meal is interesting due to its high content in mannan polymers [70].
Under the optimum conditions (severity factor of 4.5), 0.23 grams total oligosaccharides per gram
dry coconut meal were obtained, from which 90.5% had a DP between 2 and 6. The type of
oligosaccharides was not studied but, according to coconut meal composition, the majority should
be mannooligosaccharides. Liquid solid ratio was also studied (5–100), concluding that if the target
products are monosaccharides, a low liquid solid ratio should be used, whereas if oligosaccharides are
the target product, a high liquid solid ratio could give a better yield.
It should be noted that in the majority of the studies mentioned, the autohydrolysis liquors are
subjected to purification and concentration and the spent solid can be used for further fractionation
of cellulose and lignin. As seen, there are two approaches: try to optimize operational conditions to
maximize oligosaccharides production with the desired DP in one step or carry out a fractionation
process, extracting high DP oligosaccharides and processing them selectively through chemical or
enzymatic methods. In both cases, a purification step (usually based on membranes) is needed.
Fermentation 2020, 6, 31 8 of 27

Table 2. Main results in autohydrolysis studies on wastes from processing or consumption stages.

Year Residue Treatment Conditions Reactor Product (g/g DS) Ref.

2 L stainless steel Parr
190 ◦ C
reactor 4532 M. 2 Rushton
44 min (heating)
Brewery’s Autohydrolysis turbines. Electric heating.
2004 5 min (holding) XOS (0.13 g/g) [46]
spent grains isothermal Cooling by water through
LSR = 8
coil.
N = 150 r.p.m.
PID-controlled Temp.
160 ◦ C AROS (0.17 g/g)
Sugar beet Autohydrolysis 3.75 L stainless steel Parr
2009 LSR = 12 POS (0.15 g/g) [65]
pulp non-isothermal reactor
H = 2.46 GALOS (0.036 g/g)
3.75 stainless steel Parr
reactor fitted with two
160 ◦ C
four-blade turbine POS (0.20 g/g)
Autohydrolysisnon LSR = 12
2010 Orange peel impellers. Electric AROS (0.076 g/g) [63]
-isothermal H = 2.46
heating. GALOS (0.066 g/g)
N = 150 r.p.m.
Cooling through internal
loop.
170 ◦ C
POS, XOS, GOS
Steam processing, 15 min, saturated 100 L stainless steel
2012 Alperujo (no quantitative [69]
isothermal steam reactor
info on yield)

160 ◦ C
POS (0.25 g/g)
Autohydrolysisnon- LSR = 12 3.75 L stainless steel Parr
2013 Lemon peel AROS (0.068 g/g) [64]
isothermal H = 2.51 reactor
GALOS (0.026 g/g)
N = 150 r.p.m.
0.05 L reactor vessel made
160 ◦ C
of SUS316. Reactor
5 min (heating)
Beet fiber Autohydrolysis heated in a molten salt
2013 2 min (holding) AROS (0.15 g/g) [71]
(beet pulp) isothermal bath. Reactor cooled in a
3 min (cooling)
water batch to 50 ◦ C in
LSR = 8
less than 3 min.
Autoclave 0.5 L working
150 ◦ C, 5 min volume. Thermocouple
Citrus peel,
Autohydrolysis (holding) and pressure gauge to
2014 Apple POS (0.17 g/g) [66]
isothermal LSR = 30 assay temperature and
pomace
pressure inside the
reactor.
0.12 L stainless steel
275 ◦ C, 14.5 min vessel. Heated by an
Coconut Autohydrolysisnon- (heating + cooling) aluminum block heater
2014 MANOS (0.23 g/g) [70]
meal isothermal LSR = 10 controlled by a PID.
H = 4.52 Vessel cooled with
running tap water
195 ◦ C XOS (0.12 g/g)
Brewery’s Autohydrolysisnon-
2015 LSR = 8 Stainless steel Parr reactor GOS (0.040 g/g) [59]
spent grains isothermal
H = 3.65 AROS (0.032 g/g)
0.125 L stainless steel
175 ◦ C
vessel heated by
Fruit passion Autohydrolysisnon- 5,5 min (heating) POS (0.14 g/g)
2017 aluminum block heater [67]
peel isothermal LSR = 16 GOS (0.051 g/g)
and cooled by running
H = 2.21
tap water
0.6 L stainless steel
reactor. Stirring with two
200 ◦ C four-blade turbine
Sugarcane Autohydrolysis Low DP-XOS
2018 10 min (holding) impellers. Electric [68]
bagasse isothermal (0.12 g/g)
LSR = 10 heating.
Water cooling by internal
loop.
Note: H is the severity factor (Log (R0)).
Fermentation 2020, 6, 31 9 of 27

Regarding to polymers susceptibility to autohydrolysis, it seems that the following order applies
(from higher to lower susceptibility): POS < GALOS, AROS < XOS < MANNOS.
In the commented studies, some operational variables, such as particle size or agitation speed,
have not been examined. These variables that are critical to understand the effect mass transfer in
dynamic processes. The predominant type of operation is batch: in general, all the experiments were
carried out on batch reactors optimizing the time and temperature.
Moreover, it is worthy to mention that autohydrolysis is not only suitable for the production of
oligosaccharides but it is also useful for the production of a solid feedstock appropriate for further
fractionation. It makes cellulose more accessible to enzymes and the sugars obtained by enzymatic
hydrolysis can be upgraded to valuable products by catalysis and bioprocessing [41,47].

3. Acid Hydrolysis
Partial acid hydrolysis of polysaccharides is the oldest and was the most common technique to
obtain different kinds of oligosaccharides. In this review, we focus on those oligosaccharides that can
be obtained from food and agro-waste and the most important polysaccharides in this field are pectin
and cellulose/hemicellulose. The acid treatments used for these polymers are very varied because of
their completely different structure [72]. Diluted acids and high temperatures are standard conditions
for pectin degradation. In contrast, cellulose can be very hard to hydrolyze due to its rigid crystalline
structure that difficult the acid to penetrate the dense network [73]. In this case, hydrolysis is driven by
concentrated or supported acids.

3.1. Pectin
Acid treatments to perform pectin depolymerization are scarce because of the advantages of
autohydrolysis and enzymatic hydrolysis. Depending of the nature and concentration of the acid
used, a variety of POS can be obtained, as pectin is composed by neutral and acidic sugars that are
linked in different ways. In 1993, Thibault et al. used 0.1M HCl at 80 ◦ C to depolymerized beet, apple
and citrus pectin and they found that the linkage between GalA-GalA is more stable than GalA-Rha,
and much more stable than neutral sugar-neutral sugar linkage. Therefore, they obtained mostly
homogalacturonans (HG) and rhamnogalacturonans (RG) while the arabinans and arabinogalactans
(AG) were hydrolyzed to low molecular weight oligomers [74].
HCl is the most common acid used for this purpose. In a recent publication, La Cava et al. treated
the peels of four cultivars of pink/red and white grapefruits with 2M HCl at 110 ◦ C for only 2 h to
obtain a hydrolysate and use it as culture and encapsulating medium for Lactobacillus plantarum [75].
Pectin polymers and complexes from the pericarp of unripe tomato were hydrolyzed with 0.1M HCl at
80 ◦ C for different reaction times to visualize and characterize the poly- and oligosaccharides by atomic
force microscopy (AFM). They found that, when using these mild acid conditions, changes in intrinsic
viscosity of the sample were observed due to the different rates of depolymerization of RGI and HG [76].
Coenen et al. also used 0.1M HCl at 80 ◦ C but followed by a second hydrolysis with trifluoroacetic
acid (TFA). The hydrolysate contained HG, xylogalacturonan XGA and RGI oligosaccharides. They
applied the reaction to apple pectin modified hairy region to investigate the inter linkages between the
different pectin structural elements. They demonstrated at oligomer level the position of the covalent
linkage between HG or XGA to RGI by MS and MS/MS [77].
TFA is also frequently used as hydrolytic agent in pectins. Recently, Zhang et al. treated citrus
pectin with 1.2 and 2M TFA at 85 ◦ C to obtain fractions of POS and evaluated them as prebiotics. They
also degraded this pectin with H2 O2 in alkaline conditions and the POS fraction obtained with this
method was the most promising prebiotic candidate for Bafidobactorium bifidum [78]. Manderson et al.
obtained other POS but using the peel by-product of orange juice manufacturing. They produced
prebiotic pectic oligosaccharides directly from orange peel albedo in large scale performing a pasteurizer
extraction with HNO3 at pH 1.5. The fraction obtained was treated by nanofiltration to remove excess
of nitrates, and it contained not fully characterized POS and monosaccharides [79].
Fermentation 2020, 6, 31 10 of 27

A different technique was used by Burana-osot et al. [80]. They performed a photochemical
reaction to partially depolymerized citrus pectin using ultraviolet light in the presence of titanium
dioxide catalyst at pH 4 (HCl) and pH 7 (NH4 OH). Using this technique, they can control the molecular
size of the oligomers obtained by the exposure time to the UV light. To obtain good fractionated
POS, 6 h of UV light exposure and pH 7 were the optimal conditions. They obtained POS of DP 2–18
and they also confirmed the presence of methyl ester groups of galacturonic acid after the photolytic
reaction [80]. The main conditions and products can be found in Table 3.

3.2. Cellulose
Acid hydrolysis has been mainly used as a pre-treatment of lignocellulose before enzymatic
degradation to monosaccharides and related derivatives. Exclusively chemical degradation in acidic
conditions has been, in general, conducted in order to obtain, among others, glucose, xylose, furan
derivatives or levulinic acid. Only in the few following examples, the objective was to perform the (in
general acid) hydrolysis in a controlled process leading to oligosaccharides, collected in Table 4.
Bouchard et al. [81] studied the conditions allowing to improve the surface properties of cellulose
nanocrystals (CNC) preparation from bleached kraft pulp. When performed at 45 ◦ C for 25 min, the
hydrolysis in 64% sulfuric acid led to oligosaccharides of degree of polymerization (DP) between 7
and 20. The precipitation of these soluble oligosaccharides onto CNC was achieved by dilution of the
acid. At higher temperatures, the DP of the oligosaccharide decreased, and they remain very soluble at
65 ◦ C. Reference compounds were prepared by 85% phosphoric acid hydrolysis of microcrystalline
cellulose, followed by filtration and precipitation of the oligosaccharide mixtures.

Table 3. Acid hydrolysis of different kinds of pectins.

Yield (g/g
Pectin Conditions Product Ref.
Dry Solid)
Beet, Apple and 0.1 M HCl
HG, RG, arabinans and AG Not given [74]
Citrus 80 ◦ C, 72 h
POS and monosaccharides
2 M HCl
Grapefruits from hemicellulose and Not given [75]
110 ◦ C, 2 h
cellulose
0.1 M HCl
Green tomato Polysaccharides, HG, RG 0.13–0.61 [76]
80 ◦ C, 1, 8, 24 and 72 h
0.1M HCl, 80 ◦ C, 48 h
Apple MHR followed by 0.05 M TFA HG, XGA, RGI Not given [77]
100 ◦ C, 6 h
POS 3628 and 2673 KDa
1.2–2 M TFA, 85 ◦ C, 2.5 h
(TFA)
Citrus peel 88.24 mM-66.18 mM H2 O2 Not given [78]
POS 3543, 2661 and 1283
pH 10 90 ◦ C, 4 h
KDa (H2 O2 )
HNO3 , pH 1.5,
Orange albedo POS and monosaccharides 0.16 [79]
120 ◦ C, 30 min
POS and pectic
1 g/L anatase TiO2 , pH = 7,
Citrus polysaccharides of lower 0.88 [80]
UV λ = 220–340 nm, 6h
Mw

Oligosaccharides with DP 3–11 in gram quantities were obtained by treating microcrystalline

cellulose at room temperature (22 ◦ C) using a 4:1 mixture of concentrated hydrochloric acid and
concentrated sulfuric acid for 4–6 h [82]. The soluble oligosaccharides were precipitated with acetone,
and purified by ion exchange column chromatography.
Cellulose of different sources (cotton linters, fibrous microcrystalline cellulose and their derivatives
after alkaline treatment) were heated in 1 M HCl t 105 ◦ C for 3 h [83]. The DPs of the resulting
Fermentation 2020, 6, 31 11 of 27

oligosaccharides were estimated by size exclusion chromatography combined with a multiangle light
scattering detector (SEC-MALS). The samples showed a bimodal elution pattern consisting of a major
high molecular component of DP 35–101, and a minor low molecular component of DP 18–24.
A solid catalyst carrying acidic sulfonic groups was synthesized by carbonization of cellulose and
sulfonation [84]. The prepared catalyst was shown to contain sulfonic, carboxylate and phenolic groups
on a graphene matrix, and was used for the hydrolysis of crystalline cellulose. After 6 h at 100 ◦ C, all the
polysaccharide gave water soluble oligosaccharides, and the catalyst could be recovered by decantation.
The soluble oligosaccharides mixture was analyzed after 3 h of reaction by matrix-assisted laser
desorption ionization time-of-flight mass spectrometry (MALDI-TOF-MS), showing an oligosaccharide
mixture of DP 2 to 10.
Recently, another solid catalyst was recently prepared by oxidation of activated carbon under
air at high temperature (425 ◦ C) for 10 h [20]. Cellulose was hydrolyzed in the presence of this
microporous catalyst in a semi-flow reactor by mix-milling for 1 h at 180 ◦ C at a space velocity of 70 h−1 .
These semi-flow conditions afforded oligosaccharides in 71% yield. By MALDI-TOF MS analysis,
oligosaccharides of DP 2 to 13 were observed. The authors suggested that the adsorption of cellulose
on the catalyst’s surface prevents further degradation.

Table 4. Acid hydrolysis of cellulose.

Yield (g/g
Residue Conditions OGs Ref.
Dry Solid)
64% H2 SO4 , 45 ◦ C,
Bleached kraft pulp DP 7–20 Not given [81]
25 min
HCl(c)/H2 SO4 (c) 4:1,
Cellulose DP 3–11 0.02 [82]
22 ◦ C, 4–6h
cotton linters, fibrous
DP 35–101
microcrystalline 1 M HCl, 105 ◦ C, 3 h 0.5–0.8 [83]
DP 18–24
cellulose
Sulfonated carbon solid catalyst,
Crystalline cellulose DP 2–10 0.68 [84]
water, 100 ◦ C, 6 h
Oxidized microporous carbon, 180 ◦ C,
Cellulose 1 h, DP 2–13 0.70 [20]
mix-milling
Sulfonated hydrothermal treated
Cellulose DP 1–9 0.22–0.47 [85]
carbon, 165 ◦ C, 6.5 h, ball-milling

A recyclable acid solid catalyst was recently prepared by sulfonation of carbonized cellulose
followed by hydrothermal treatment and it was used for the hydrolysis of cellulose by ball-milling [85].
The authors suggested a crucial role of strong Brønsted acid sites of the catalyst in the mechanocatalytic
depolymerization process, though some contribution of auto-hydrolysis and homogeneous catalysis
due to leaching of acidic groups cannot be excluded. The soluble fraction was analyzed by liquid
chromatography coupled to a mass spectrometer (LC-MS) showing the presence of oligosaccharides
with a DP of up to 9. The formation of larger oligosaccharides is also possible during ball-milling, but
they were difficult to detect because of their lower solubility.

4. Enzymatic Processes
The enzymatic breakdown of the food waste biomass matrix consists of the depolymerization of
its structural more relevant polysaccharides: cellulose, hemicellulose and pectin. These processes take
place due to the simultaneous work of different enzymes, mainly catalyzed by hydrolases and to a
lesser extent by lyases. These enzymes cleave ether and ester bonds, releasing oligosaccharides and
monosaccharides. It is essential to take into account that the conditions employed in these processes
Fermentation 2020, 6, 31 12 of 27

are gentler than those used in autohydrolysis and acid hydrolysis operations. However, there are some
shared parameters in all the processes with a very similar influence in the results. We will comment on
these parameters in the following subsections.

4.1. Process Variables

4.1.1. Pretreatment of Biomass

The food waste biomass is very recalcitrant, mainly because of the structure of its principal
component, cellulose. This polymer presents different degrees of crystallinity polymorphisms [86]
and take part of a complex network constituted by cellulose- hemicellulose-pectin, which causes
an important problem of accessibility of the different enzymes employed. A simple mechanical
pretreatment, milling, can increase the specific area of the substrate and reduce the length of cellulose
fibers [87]. More complex physicochemical, hydrothermal and chemical pretreatments, such as acid [88],
alkaline [89] and/or oxidative pretreatments [90], are also employed in order to favor the accessibility
to the most recalcitrant structural polysaccharides and their reactivity. They can remove hemicellulose,
pectin, proteins and extracts, on one side, reduce the length of cellulose fibers and its crystallinity, and
increase the specific area, the porosity.

4.1.2. Temperature and pH

When enzymes are employed, the temperature is a very important parameter because proteins
can suffer structural disorders and subsequent inactivation, while, with temperatures below optimal
conditions, reaction rates can be too low. Therefore, an agreed temperature around 45 and 50 ◦ C is
recommended on average for the different enzymes mixtures. It is essential to consider that every
single enzyme has its own optimal temperature, which usually tends to be superior to their maximum
stability temperature. Thus, it is necessary to find a consensus between both values [91,92]. Another
important aspect of this enzymatic reaction is the pH, whose operational value ranges from 3 to 5 [93].
The requirement of maintaining an adequate pH value needs pH control or buffer usage. Most common
buffers are acetate [94] and citrate [95].

4.1.3. Particle Size and Solid Loading

The pretreatment of food waste biomass generally produces a size distribution that should be
considered as an influential factor over enzymatic hydrolysis. Substrate particle size affects the overall
rate of the hydrolysis process [96], given that this size impacts upon the efficiency of the substrate
access of the enzymatic mixture, introducing mass transfer limitations in bigger particles. In addition,
high solid presence in the reaction medium, an industrial tendency, increases viscosity and also affects
the external and the internal mass transfer rate [97,98].

4.1.4. Side Products Formation

The use of mild temperatures and pH around neutrality reduce the degradation of biomass and
side compound formation such as furfural and 5-hydroxymethylfurfural (HMF) (by dehydration of
glucose and other hexoses) and corrosion problems. The reduction of aldehyde compounds formation
is positive to avoid the inhibition of enzymes and of microorganisms in subsequent bioprocesses, apart
from reducing cost in purification operations downstream the reaction section [99].

4.1.5. Source of Enzymes

Main natural source of cell wall degrading enzymes are members of phylo Ascomycota [100] and
Basidiomycota [101]. Within Ascomycota phylum, Aspergillus, Trichoderma and Neurospora have important
industrial applications as enzyme producers. However, in Basidiomycota, there are two of the most
efficient lignocellulose biomass degraders: white and brown rot fungus.
Fermentation 2020, 6, 31 13 of 27

4.2. Oligosaccharides from Agricultural Wastes Production by Enzymatic Hydrolysis

Oligosaccharides are intermediates of depolymerization reaction of lignocellulosic materials. In
the 50s decade of twentieth century, the enzymatic hydrolysis of different substrates from lignocellulose
was studied. Hydrolysis of isolated cellulose [102], xylan [103] (main component of hemicellulose)
and pectin [104], generated some products of glucidic nature with a higher molecular weight than
the one of monosaccharides (150–180 Da). This observation led to the verification of oligosaccharides
formation during enzyme hydrolysis of biomass.

4.2.1. Cellulose
In the decade of the 70s, new studies about the use of enzyme for the production of single sugars
for use as microorganism carbon source appeared. Wilke and Miltra studied enzymatic saccharification
for process development of a specific source of cellulose that participate before in research for the
production of cellulolytic enzymes: newsprint paper [105,106]. The knowledge about the huge amounts
of lignocellulosic materials produced as residues in agriculture, opened a new variety of raw material
that could be subjected to enzyme saccharification [107]. Cellulases is a group of enzymes that effect its
lytic activity over cellulose, having a synergistic effect amidst all different enzymes activities. These
enzymes and their main activities are collected in Table 5.
Production of β-glucans or gluco-oligosaccharides is a less studied subject in comparison to
the production of glucose because of its importance as carbon source for bioprocesses and, lately,
as promising C6 platform chemical within the biorefinery concept. It should be taken into account
that β-glucosidase is an impediment of cellooligosaccharides (COS) accumulation, since this kind
of enzymes hydrolyses glycosidic bond within cellobiose, yielding high amounts of β-D-glucose.
Cellobiose is the product released by exo-glucanases that can be considered as a DP2 oligosaccharide.

Table 5. Principal enzymatic activities involved in cellulose degradation.

Enzyme Commission
Enzyme Name Activity Product
Number
Endohydrolysis of
Endo-cellulase
3.2.1.4 (1→4)-β-D-glycosidic linkages in Cellodextrins
(endoglucanase)
cellulose
Cellulose Hydrolysis of
1,4-β-cellobiohydrolase 3.2.1.176 (1→4)-β-D-glycosidic linkages of Cellobiose
(reducing end) reducing end of polymer
Cellulose 1,4-β- Hydrolysis of
cellobiohydrolase 3.2.1.91 (1→4)-β-D-glycosidic linkages Cellobiose
(non-reducing end) from non-reducing end of polymer
Hydrolysis of (1→ >
β-glucosidase 3.2.1.21 4)-β-D-glycosidic linkages in β-D-glucose
cellobiose

Removing one or some enzymes, or reducing their activities in the enzyme cocktail, allows
obtaining oligosaccharides with a higher DP degree. That is the reason why some procedures are
focused on the adsorption of these enzymes on its natural substrate. When the cellulase mixture
gets in contact with cellulose, endo-cellulases and exo-cellulases bind specifically to it, due to the
presence of a cellulose-binding domain (CBD) in their structure. Cellulolytic enzymes have specific
domains that allows them to interact with cellulose [108]. Chu et al. demonstrated that the selective
removing of β-glucosidase activity in a corncob residue manages to double cellooligosaccharide
production in a subsequent enzymatic hydrolysis, leading to an increase in COS yield (from 0.15 g/g
to 0.25 g/g, corresponding at final concentration of 7.6 g/L and 12.6 g/L, respectively) and selectivity
(from 30 to 60%) [109]. Birhade et al., on the other side, discovered that these differential adsorption
Fermentation 2020, 6, 31 14 of 27

processes are deeply influenced by the accessibility of cellulose. When phosphoric acid-swollen
cellulose (PASC), ammonia-treated wheat straw (AWS), sodium hydroxide-treated wheat straw (NWS)
and nitric acid-treated maize bran (NMB) were used as substrates in pre-enzymatic adsorption step
with the following conditions: 20 FPU/g cellulose, pH 4.8, 20 min and 4 ◦ C, 34% (PASC), 27.97% (NWS),
25.11% (NMB) and 8.11% (AWS) of endo-glucanase activity was retained. AWS waste showed a low
interaction with β-glucosidase (next to 0.1%), and low endoglucanase retention, which makes this
material the best option to selectively remove exo-glucanase activity. Adsorption with AWS followed
by separation step and hydrolysis leaded to a different result. If the cellulose and exo-cellulose mixture
was employed, cellobiose was the main product. However, if the supernatant of the adsorption step
was used, the products were a mixture of cello-oligosaccharides with a DP > 6 (0.11 g/g), DP 2–6
(0.10 g/g) and monosaccharides (0.11 g/g) when AWS was employed [110].

4.2.2. Hemicellulose
Hemicellulose is a hetero-polysaccharide that constitutes an important part of the cell wall. This
complex polysaccharide is the most abundant after cellulose [111]. Due to its composition and structure,
to ensure its complete enzymatic hydrolysis, several enzyme activities should work together in a
synergistic way, being the most important collected in Table 6. The principal component in most
hemicelluloses is xylan, whose structure is a chain of β-D-xylose bonded through β(1→4) linkages [112].
Just as in the case of the enzymatic hydrolysis of cellulose, enzymatic commercial mixtures
contain different enzyme activities. The analysis and determination of these activities is fundamental
in order to estimate what kind of oligosaccharide mixtures can be achieved (their composition and
molecular weight). Hespell et al. evaluated that corn fiber biomass subjected to a pretreatment of
ammonia-explosion contains around 30% hemicellulose. Testing the xylanase activity of different
enzymatic mixtures with colorimetric methods on this substrate, certain mixtures that were enriched in
a single enzyme (e.g., β-glucosidase), presented hemicellulose activity, when apparently they should
not. The reaction took place for 72 h with a 5% w/w DS at pH 4.8. After this reaction time, between
30%-40% of the hydrolysis products could be oligosaccharides [113]. The evaluation of xylanolytic
activity is only a part of the hemicellulase activity because in hemicellulose breakdown numerous
enzymes (collected in Table 5) are involved.
Mazlan et al. studied the most important operational factors that may affect the production of
xylooligosaccharides from oil palm frond bagasse [114]. The optimal conditions resulting from the
experimental design were a substrate loading of 1% (w/w) and a 50 U/mL of xylanase activity from a
commercial mixture (Cellic Htec2®). Enzymatic activity was measured via 3,5-dinitrosalycilic acid assay
using birchwood xylan as substrate. Under these conditions, a yield of 0.175 g of xylooligosaccharides
(XOS) per gram of dry substrate was obtained. Jagtap et al. evaluated the use of wheat husk as
substrate employing solid substrate loading ranging from 1% to 5% w/w DS, a certain value favored
the production of XOS (1 g/L to 3.5 g/L, respectively). After hydrolysis optimization of enzymatic
doses and time of reaction, maximum of XOS (10.8 g/L) was reached. Nevertheless, the increasing of
substrate concentration to 10% w/w DS did not cause an improvement in XOS production, maybe due
to the higher viscosity of the reaction liquid [115].
Another important factor is the source of xylanolytic enzymes. If the XOS recovery of commercial
xylanase action is compared that due to microbial extracts, different results come forth when hydrolyzing
the same substrate. In the work of Azevedo et al., different behaviors are appreciated when comparing
the action of various microbial extracts that contain enzymes with xylanase activity and commercial
preparations employing the same conditions (50 ◦ C, pH 5, 1–96 h and hemicellulose from sugar
cane bagasse) [116]. The concentrations reached with commercial enzymes are lower (0.50 g/L) than
those obtained from the best microbial extract from Aspergillus fumigatus M51 (1.04 g/L). Microbial
extract generated mostly xylobiose and xylotriose (0.59 g/L and 0.45 g/L, respectively) and a lower
amount of high degree polymerization oligosaccharides (0.01 g/L). Optimization process employing
Aspergillus fumigatus M51 xylanase reach a yield of 0.38 g/g after 72 h of reaction time. In the case of
Fermentation 2020, 6, 31 15 of 27

commercial enzymes, similar amounts of xylobiose but only a small amount of xylotriose are obtained
(0.51 g/L and 0.08 g/L, respectively). These results could be explained because microbial xylanase is an
endo-xylanase, while commercial preparations could contain more xylanolytic enzymes optimized for
xylan saccharification.
In Table 7, some other examples processes for XOS production are given. Residues that contain
high amounts of hemicellulose, mainly as xylans, are wastes from stalks, stems and shell of crops.
Pretreatment of these wastes are important for the isolation of hemicellulose, favoring XOS production.
Temperature conditions are 40–50 ◦ C—sometimes, slightly higher—, while solid dry loadings do not
exceed 10% w/w in all cases.
Hemicellulose is built by a xylan backbone with some lateral substituents that constitute other kind
of oligomeric sugar structure, being one of this side chains manooligosaccharides (MOS). Nguyen et al.
observed that some wastes such as spent coffee ground contain high levels of mannose derived from
hemicellulose. When this residue was pretreated by delignification and defatting and submitted
afterwards to an enzymatic hydrolysis with a 10% w/w dry substrate loading at 45 ◦ C and pH 4.8,
a maximum oligosaccharides production yield is obtained between 4 h and 6 h after hydrolysis
started. The highest yields were observed using a non-commercial pectinase, at 4.1 mg enzyme/g dry
biomass, obtaining 38.2 g/L of DP62 MOS and 24.9 g/L of DP6 MOS (total yield 0.63 g/g DS) [117].
Rungruangsaphakun et al., on the other side, produced MOS using 16.52 U/mL of mannanase, with
a solid loading of 15% of defatted copra meal, 50 ◦ C and pH 6. After 12 h, these authors achieved a
mean of 14.41 g/L MOS (0.095 g/g DS) and, after increasing scale by two orders of magnitude, 16.89 g/L
MOS (0.11 g/g DS) [118].

Table 6. Principal enzymatic activities involved in hemicellulose depolymerization.

Enzyme Commission
Enzyme Name Reaction Product
Number
Endo-1,4-β-xylanase Random endohydrolysis of
3.2.1.8 Xylan oligomers
(Endo-xylanase) (1→4)-β-D-glycosidic bond
Hydrolysis of
Xylan 1,4-β-xylosidase 3.2.1.37 (1→4)-β-D-xylans from their β-D-xylose
non-reducing end
Hydrolysis of terminal non
α-L-arabino-furanosidase 3.2.1.55 reducing α-D-arabinose of α-D-arabinose
arabinan oligomers
Hydrolysis of terminal non
α-D-galactosidase 3.2.1.22 reducing α-D-galactose of α-D-galactose
galactan oligomers
Release acetate by removing
Acetyl esterase 3.1.1.6 Deacetylated xylan
acetyl ester groups
Hydrolysis of ester bond
Ferulic acid and
Feruloyl esterase 3.1.1.73 between monosaccharides
polysaccharide
and ferulic acid
Fermentation 2020, 6, 31 16 of 27

Table 7. Examples of enzymatic hydrolysis of agricultural wastes to xylooligosaccharides (XOS).

Residue Pretreatment Enzymes and Offered Activity Conditions Products Ref.

Endoxylanase from
Autohydrolysis (LSR 10 g water/g dry 50 ◦ C, 4–48h
Thermomyces lanuginosus XOS
Almond shell solid, 180–220 ◦ C isothermal, holding 70 r.p.m. [58]
(Endoxylanase activity, (DP: 2 and 3, Mw< 250 Da)
different times). 1% w/w solid
5, 10 and 15 U/mL)
XOS (DP: 2 to 5)
Viscozyme L®and Aspergillus 40 ◦ C, 6 h Viscozyme L (0.084 g/g DS,
Brazilian syrah grape
Dry and milling niger 3T5B8 (xylanase activity, 200 r.p.m. 100 IU/g) [119]
pomace flour
10–100 IU/g dry substrate) 5% w/w solid Aspergillus niger 3T5B8 (0.081
g/g DS, 100 IU/g)
Organic acid pretreatment (13.33% of
solids and different lactic acid Cellulase mixture provided by
50 ◦ C, 72 h
Corn straw concentrations) and deep eutectic Genencor (China) (Cellulase XOS (DP: 2 to 4) [120]
2% w/w solid
solvents pretreatment (5% of solids, activity, 10 FPU/g dry substrate)
120 ◦ C from 2–6 h),
Diluted acid pretreatment (1% of solid, Xylanase from Bacillus
70 ◦ C, 48 h
Corncob 0.1 sulfuric acid, 60 ◦ C and 12 h) aerophilus KGJ2 (xylanase, XOS (DP: 2 to 4) [121]
10% w/w solid
filtering and autoclaved 1 h 120 ◦ C. 20 UI)
Extraction with boiling water (1:25) 2 h Manannase (manannase
45 ◦ C, 40 h
Plantago major L. stirring. Filtering and precipitation activity, 0.2–4 U/mL) and XOS and AROS (DP: 2 and 3) [122]
1% w/w solid
with ethanol (95%) and dry hemicellulase (50–250 U/mL).
Endoxylanase from
Dry almond shells alkaline extraction 50 ◦ C, 2–48 h and XOS (DP: 2 (0.35 g/g) 3 (0.09
Almonds shells Thermomyces lanuginosus [123,124]
with NaOH (1–2 M) 121 ◦ C 1h. 2–6% w/w solid g/g) to 4 (0.01 g/g xylan))
(5, 10 and 15 U/mL)
Alkaline (0.25–0.75%) and acid Xilanase activity 66 UI/g dry
50 ◦ C, 8 h, 40 h XOS
Reed pulp (0.55–1.65%) extraction of substrate and cellulose activity [125]
5% w/w solid (0.144 g/g DS)
hemicellulose 150–160 ◦ C, 30 min. 10 FPU/g dry substrate
Fermentation 2020, 6, 31 17 of 27

4.2.3. Pectin
Pectin is, in a great percentage, composed by homogalacturonan [126]. Consequently, pectinolytic
activity of the enzymes employed in pectin depolymerization processes is tested mainly employing
polygalacturonic acid as substrate. Despite the pectinolytic activity test, and due to the number
of enzymes involved in the pectin breakdown (Table 8), the use of same activity units for different
enzymatic mixtures of diverse origin can be misleading [127].

Table 8. Main enzymatic activities involved in pectin depolymerization.

Enzyme Commission
Enzyme Reaction Product
Number
Random hydrolysis of
Oligomers of
Endo-polygalacturonase 3.2.1.15 galacturonic acid backbone in
1,4-α-D-galacturonoside
pectin
Hydrolysis of the first α(1→4)
Exo-polygalacturonase 3.2.1.67 bond from non-reducing end α-D-Galacturonic acid
of polygalacturonic acid
Second α(1→4) bond from
Exo-poly-α-digalacturonosidase 3.2.1.82 non-reducing end of Digalacturonate
polygalacturonic acid
Eliminate α(1→4) bond in 4-deoxy-α-D-galact-4-enuronosyl
Pectate lyase 4.2.2.2
galacturonic acid backbone groups
Hydrolyse α-D-galacturonic Oligosaccharides with
Rhamnogalacturonan
3.2.1.171 acid-(1→2)-α-L-rhamnose β-D-galacturonic acid at the
hydrolase
bond reducing end
Eliminate α-D-galacturonic 4-deoxy-4,5-unsaturated
Rhamnogalacturonan
4.2.2.23 acid-(1→2)-α-L-rhamnose D-galactopyranosyl uronic
endolyase
bond acid

According to the pectin source, the composition of its side sugar chains varies, as in the case
of potato peel wastes that contain 75% of rhamnogalacturonan structure (constituted regions of
galacturonic acid and rhamnose units). Rhamnogalacturonan chains can have galactose and arabinose
oligosaccharides as side substituents. The balance of hydrolytic activities about these regions, presented
in the different enzymatic preparations, allows getting specific oligomers of its sugars. Khodaei and
Karboune isolated pectin from potato peel using a concentration of 0.5% w/w dry substrate, adding
0.2 U/mg of Depol 670L ® [128]. After 4 h, the oligosaccharides yield production was 0.94 g/g and, from
the oligosaccharides obtained, 89.7% has a DP between 2 and 12, which indicates that the arabinanase
to galactananase ratio of Depol 670L ®permits the specific release of arabinanan and galactanan
oligosaccharides [129].
Citrus peel wastes, such as lemon peel, are a huge source of pectin. Gomez et al. studied the
enzymatic hydrolysis after a washing step, in order to remove free sugars from the lemon peel. The
conditions of the enzymatic reaction were 37 ◦ C, pH 5, 5% w/w of dry solid loading and 5 U/mL
of pectinase activity of different enzyme preparations that have different lytic activities towards
arabinanan, arabinogalactan and galactan regions [130]. This study demonstrated that the use of
enzyme mixtures with different activities changes the product distribution. The highest yield obtained
under selected optimal conditions was 0.19 g/g. [128].
In recent years, there are some examples of processes to obtain pectinoligosaccharides (POS).
All studies contained in Table 9 include a previous step of biomass pretreatment whose aim is the
fractionation of raw materials. The reaction conditions in all cases are very similar, ranging from
45 ◦ C to 50 ◦ C at a low solid loading. When products were analyzed, the polymerization degree was
determined, being possible to determine its size and weight.
Fermentation 2020, 6, 31 18 of 27

Table 9. Examples of enzymatic hydrolysis of agricultural wastes to obtain POS.

Residue Pretreatment Enzymes and Offered Acti4vity Conditions Product Ref.

Fungal enzyme cocktail: xilanase (50 POS
Water washing (4%, 6h, 30 ◦ C,
U/mL), pectinase(48,3 U/mL) 4% of solid, 45 ◦ C, 6 h and (DP 6 (0.06 g/g), 9 (0.28
Orange Peel Wastes 170 r.p.m. rotational stirring) [130]
cellulase (0,2 U/mL) and 170 r.p.m. g/g), 19 (0.04 g/g extracted
oven dry 65 ◦ C 48 h
endo-celulase(2,8 U/mL) DS))
50 g/L of dry and grinded Viscozyme
45 ◦ C, 15–30 min, 200 POS
biomass extracted with sodium L®(endo-polygalacturonidase
Onion skins r.p.m., 2.5–5% w/w dry (DP 2 to 8) [131]
hexametaphosphate (2%) activity, 82.7 U/mL, 41.4 U/mL and
solid(membrane reactor) 22.0 g/(L·h)
95 ◦ C, 0.5 h 20.7 U/mL)
Acid hydrolysis with HCl
Endo-polygalacturonidase-M2
(pH1.5), 80 ◦ C, 1h. Cooling,
(Endopolygalacturonidase activity, POS
filtering and adjusted at pH 3.5 50 ◦ C, 2–15 min
Sugar beet 9.55 U/mL) and Rapidase Smart (DP 2 to 9; [132]
with KOH. Finally, etanolic 0.5% w/w solid
®(Pectinmethylesterase activity, 0.52 MW 400–2000 Da)
precipitation and
U/mL)
demethoxylation step.
Pectinex®Ultra-Olio (pectinase
Pectin extraction enzymatically POS
◦ activity, 6.75 U/mL), Glucanex
assisted (Celluclast 1.5 L) at 50 C. 50 ◦ C, 0.5–4 h, 750 r.p.m. (DP 2 (0.023 g/g),3 (0.047 [133,
Novel artichoke ®200G (pectinase activity, 0.63 U/mL)
Filtering and ethanolic 2% w/w solid g/g), >3 (0.225 g/g pectin); 134]
and Pentopan®Mono-BG (pectinase
precipitation MW 78–3500 Da)
activity, 0.54 U/mL)
POS
Biomass was homogenate and
Endopolygalacturonidase from ◦ C, (MW < 700 Da (0.12–0.20
Hardy kiwi (Actinidia defatted. Filtering 50 3h [135,
Rhizopus sp. (endo-pectinase activity, g/g), 700 > MW > 3000
arguta) deproteinization (Sevag method) 2% w/w solid 136]
0.2 U/mL) (0.66–0.68 g/g) and MW >
and ethanolic precipitation
3000 (0.10–0.06 g/g pectin)
Viscozyme L ®, Pectinase from
1 g of onion skins extracted with
Sigma Aldrich and POS (DP 2 (0.03 g/g DS), 3
2% sodium hexametaphosphate 45 ◦ C, 2h, 150 r.p.m.
Onion skins endo-polygalacturonase M2 (0.06 g/g DS), 4 (0.06 g/g [137]
95 ◦ C 0.5 h. Centrifugation and 10% w/w solid
(endo-polygalacturonidase activity, DS) to 5)
supernatant collection
82.7 U/mL, 52.2 U/mL and 5.2 U/mL)
Fermentation 2020, 6, 31 19 of 27

5. Conclusions and Future Prospects

In the last years, with the progressive definition and development of biorefineries, biomass is
becoming again a material resource of utmost importance. Its being intimately included in the Earth‘s
element cycles turns it into the ideal renewable resource to obtain foods, feed, chemicals, materials and
even fuels.
On its side, food, as a key vertex of the food-water-energy triangle, is clearly defined as a main
human need, with an increasing importance as human population grows. The need for reducing
food and food-related waste comes in hand with the need to valorize the unavoidable masses from
the food production chain. In particular, polysaccharide related wastes are an evident source of
bioactive compounds, having oligosaccharides a great potential for the development of food-related
new products with elicitor, prebiotic, drug, prodrug and other bioactivities.
Oligosaccharides from cellulose, hemicellulose and pectin can be considered intermediates in
the production of the main biorefinery platform chemicals of the C5 (pentoses) and C6 (hexoses)
type. Though biorefinery upstream processes are mainly focused on the production of such platform
chemicals, the development of new acid, basic, thermal and physicochemical biomass pretreatments
have permitted the observation of operational conditions adequate for oligosaccharide production from
pectin and hemicellulose, more prone to depolymerization than cellulose. Moreover, the advent of new
enzymes, as LPMOs, and the more in-depth study of hydrolytic processes with classical hydrolytic
enzymes and with supported acids have created new opportunities to obtain these bioactive oligomers,
even acting on the more recalcitrant cellulose. While pectin and hemicellulose need of a careful tuning
of operational conditions to avoid excessive hydrolysis, cellulose needs of harsher conditions to get
cellooligosaccharides. In this last case, the use of enzymes reduces the risk of dehydration to aldehydes,
but fine-tuning of acidity and temperature is needed to obtain the same result with hemicelluloses,
using weak acids such as acetic and gluconic acids [138,139].
Finally, controlled process intensification with ultrasounds, microwave heating, hydraulic
cavitation and pulsed electric fields should turn oligomer production into a more productive and less
polluting activity, optimizing food waste valorization. To enhance the oligomer activity, chemical
modifications such as acylations, esterifications, sulfonations, etc. as well as de novo synthesis of
analogs can create more products or enhance the bioactivity of those now in place [140,141].
As a brief graphical abstract, Figure 1 shows some of the procedures and oligomers available
from agrofood waste transformation via acid, supported acid, hydrothermal or autocatalytic and
enzymatic routes.
Fermentation 2020, 6, 31 20 of 27
Fermentation 2020, 6, 31 20 of 27

Figure1.1. Valorization
Figure Valorization routes
routes from
from agro-food
agro-food wastes
wastes totooligomers,
oligomers, oligomer-based
oligomer-based products
products and
and
present/possibleapplications.
present/possible applications. The
The figure
figure indicates
indicates the
the main
mainoperational
operationalvariables,
variables, with
withtheir
theirmost
most
typical
typicalvalues,
values,for
foreach
eachtype
typeofofprocesses
processesand
andtarget
targetoligosaccharides.
oligosaccharides.

Author Contributions: M.L. and J.K. conceived the review; M.L., M.E.C., A.G.-M. and P.C.M. compiled
Author Contributions: M.L. and J.K. conceived the review; M.L., M.E.C., A.G.-M. and P.C.M. compiled literature,
literature, read it and wrote the draft manuscript; J.K., M.L., M.W. and V.E.S. revised the draft version, included
read it and wrote the draft manuscript; J.K., M.L., M.W. and V.E.S. revised the draft version, included new
new references
references and wrote
and wrote the definitive
the definitive version.
version. All All authors
authors have
have read
read and
and agreed
agreed totothe
thepublished
publishedversion
versionof
of
themanuscript.
the manuscript.

Funding: The
Funding: The Spanish
Spanish MINECO
MINECO and
and the
the Agence
Agence Nationale
Nationale de
de lalaRecherche
Recherche (France)
(France) have
havefunded
fundedthis
thiswork
work
through projects CTQ2017-84963-C2-1-R and PCI2018-093114, and ANR-18-SUS2-0001, respectively.
through projects CTQ2017-84963-C2-1-R and PCI2018-093114, and ANR-18-SUS2-0001, respectively.
Conflicts of Interest: The authors declare no conflict of interest. The founding sponsors had no role in the design
Conflicts of Interest: The authors declare no conflict of interest. The founding sponsors had no role in the design
of the study; in the interpretation of literature; in the writing of the manuscript, and in the decision to publish
of the
the study; in the interpretation of literature; in the writing of the manuscript, and in the decision to publish
results.
the results.
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