Xylooligosaccharides production process from lignocellulosic biomass and bioactive effects

Accepted Manuscript Xylooligosaccharides production process from lignocellulosic biomass and bioactive effects Caroline de Freitas, Eleonora Carmona, Michel Brienzo PII:

S2212-6198(18)30019-6

DOI:

https://doi.org/10.1016/j.bcdf.2019.100184

Article Number: 100184 Reference:

BCDF 100184

To appear in:

Bioactive Carbohydrates and Dietary Fibre

Received Date: 13 March 2018 Revised Date:

1 October 2018

Accepted Date: 26 April 2019

Please cite this article as: de Freitas C., Carmona E. & Brienzo M., Xylooligosaccharides production process from lignocellulosic biomass and bioactive effects, Bioactive Carbohydrates and Dietary Fibre (2019), doi: https://doi.org/10.1016/j.bcdf.2019.100184. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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ACCEPTED MANUSCRIPT Xylooligosaccharides production process from lignocellulosic biomass and bioactive effects

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Caroline de Freitas1, Eleonora Carmona1, Michel Brienzo2*

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Biochemistry and Microbiology Department, Universidade Estadual Paulista (UNESP), Rio Claro-SP, Brazil

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Bioenergy Research Institute (IPBEN), Universidade Estadual Paulista (UNESP), Rio Claro-SP, Brazil

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Corresponding author: Michel Brienzo. E-mail: [email protected].

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Abstract

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Xylooligosaccharides (XOS) are sugar oligomers made with xylose units.

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They are recognized by its great prebiotic potential and nutritional benefits,

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promoting growth of the probiotic bacteria in the intestinal tract. Other

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advantages of XOS consumption, which comes from the stimulation of selective

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growth of the beneficial intestinal microflora, includes reduction of glycemic

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indexes and cholesterol in the blood, reduction of pro-carcinogenic enzymes in

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the gastrointestinal tract, improvement of the absorption of minerals in the large

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intestine, in addition to stimulating the immune system. Xylan, the major

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hemicellulosic component of lignocellulosic materials can be used for XOS

44

production. Therefore, plant biomass in agriculture residues can be a source for

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that XOS production in a sustainable and affordable way. Although xylan is the

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most abundant hemicellulose in the majority of cell wall plants, hemicelluloses

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differ from softwoods, hardwoods and annual plants and that can generate

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different types of XOS. The production of XOS can be carried out by chemical

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and enzymatic methods, the latter is preferable in the food industry because

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does not present secondary reactions or the formation of by-products. Prior to

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XOS production, hemicellulose needs to be extracted from the lignocellulosic

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biomass. This study presents XOS as an emerging prebiotic with more

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emphasis on its production processes and bioactive properties.

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Key words: xylooligossacarides, hemicellulose, xylan, biomass, prebiotic, prebiotic.

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1. Hemicelluloses Hemicelluloses or polioses can be defined as the second most abundant

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polysaccharides in nature. Hemicellulose is present in the plant cell wall in close

70

association with cellulose and lignin to contribute to its rigidity. These

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polysaccharides appear in greater quantity in the primary cell wall, and also it is

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found in the secondary cell wall. They are partially soluble in water and soluble

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in dilute alkali, which makes it possible to be separated in this medium.

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(Spiridon e Popa, 2008; Whistler, 1993)

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The hemicellulose structure consists in a linear chain with numerous

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branches consisting of one or several sugar units. The branches are usually of

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a different kind of sugar than those making up the main chain (Whistler, 1993).

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The hemicellulose can contain pentoses (β-D-xylose, α-L-arabinose), hexoses

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(β-D-mannose, β-D-glucose, α -D-galactose) and/or uronic acids (α -D-

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glucuronic, α -D-4-O-methylgalacturonic and α -D-galacturonic acids) (Gírio et

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al, 2010). The diversity of sugars in the main chain classifies the hemicellulose

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as heteropolysaccharides (Whistler, 1993).

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The hemicelluloses can have different polysaccharides in their chain:

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xylan,

glucuronoxylan,

arabinoxylan,

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galactoglucomannan. Some of them and the composition of this molecules on

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the chain will vary depending on the plant species, sub-cellular location and

87

developmental

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hemicelluloses, such as their solubility and three-dimensional conformation.

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(Spiridon e Popa, 2008; Wyman et al., 2005). Xylans are usually available in

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huge amounts as by-products of forest, agriculture, agro-industries, wood and

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pulp and paper industries. Mannan-type hemicelluloses like glucomannans and

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galactoglucomannans are the major hemicellulosic components of the

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secondary wall of softwoods. (Gírio et al, 2010).

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and

that

will

determine

glucomannan

some

properties

and

of

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stages,

mannan,

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These polysaccharides constitute about 20-30 per cent of the total mass

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of both annual and perennial plants, approximately one-third of the total mass

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(Whistler, 1993). They have low-molecular-weight and average degree of

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polymerization is in the range of 100-200, varying according to the number of 3

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xylose units in the molecule (Peng et al., 2012). The molecular size, degree of

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branching and the monosaccharides that make up the side chains largely

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determine the biological properties of hemicelluloses and its use in the industry

101

(Cantu-Jungles et al, 2017). The hemicellulose most relevant and commonly found in nature is xylan.

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Its structure is variable, ranging from a linear backbone of β-1,4 linked xylose

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residues to highly branched heteropolysaccharides, where the xylose sugars

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are substituted by branches containing acetyl, arabinosyl and glucoronosyl

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residues, according to the species (Figure 1). (Spiridon e Popa, 2008; Scheller

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& Ulvskov, 2010; Rennie & Scheller, 2014; Bajpai, 2014). Xylan deposition in

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the secondary cell wall is required for normal plant growth and development and

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increases cell wall recalcitrance as well, helping to defend the plant against

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herbivores and pathogens (Rennie & Scheller, 2014).

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1.1.

Hemicelluloses from softwood, hardwood and grasses

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Although xylan is the most abundant hemicellulose in the majority of cell

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wall plants, hemicelluloses differ from softwoods, hardwoods and annual plants.

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In softwoods, the most abundant hemicellulose is a partially acetylated

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galactoglucomannan, which is composed by β-1,4 linked D-glucopyranose D-

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mannopyranose

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Galactoglucomannan represents 10 to 25% of total hemicellulose found in

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softwoods and can constitute up 10% of dry wood (Whistler, 1993; Peng et al.,

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2012; Peng et al., 2011).

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randomly

distributed

in

the

main

chain.

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units

The hemicellulosic fraction of Pinus, a type of softwood, represents

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approximately 26% of wood dry weight and, hexoses such as glucose,

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mannose and galactose are responsible for 64% of its composition. The

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hemicellulose present on this wood is mostly composed of (1→4)-linked β-

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glucomannans backbone with (1→6)-linked α-D-galactose as a side chain

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attached to C-6 of mannose units (Reyes et al., 2013; Xue, Wen, Xu, & Sun,

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2012).

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In hardwoods, the main hemicellulose is the also acetylated O-acetyl-4-

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O-methylglucurono-β-D-xylan with a small portion of a D-gluco-D-mannan,

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of a backbone of β-1,4 linked D-xylose residues and, on average, about 70% of

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xylose residues contain an acetyl group (Gírio et al, 2010; Peng et al., 2011;

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Puls, 1997). Regarding the annual plants, the most abundant hemicellulose is

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xylan, which are more heterogeneous than the xylans from wood tissues. They

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contain both glucuronic acid and arabinose attached to the xylose units and can

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more than 30% of the dry weight. (Spiridon e Popa, 2008; Aspinall, 1980; Sun

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et al., 2004).

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Besides these main structural units, glucuronoxylans found in hardwoods

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may also contain small amounts of L-rhamnose and galacturonic acid. In xylan

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samples from Eucalyptus, the sugars present are xylose, glucose and galactose

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and the latter is assigned to chemical linkage with the xylan chain through

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uronic acid in O-2. The content of acetyl groups found in Eucalyptus xylan are

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significantly higher than grasses xylan, such as sugarcane bagasse (Peng et

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al., 2011; (Morais et al., 2015).

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Arabinoxylans are the main hemicelluloses of grasses. Their structure

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consists of α-l-arabinofuranose residues attached as branch-points to the β-1,4

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linked D–xylose polymeric backbone chains. This hemicellulose have been

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generally present in a variety of tissue of the main cereals of commerce: wheat,

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rye, barley, oat, rice, corn, and sorghum, as well as other species of this

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botanical family, like sugarcane (Gírio et al, 2010; Peng et al., 2012).

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The xylan present in grasses are similar to hardwood xylan but the

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amount of L-arabinose is higher. Sugarcane bagasse xylan is mainly composed

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by xylose, arabinose, glucose and uronic acids. The main linkage between

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sugars in xylan from bagasse and straw are 4-Xylp, 2,4-Xylp, 3,4-Xylp and t-

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Araf, which suggested that the main xylan in bagasse and straw is the

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arabinoxylan, with branches at O-2 and O-3 of arabinofuranosyl or at O-2 of 4-

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O-methylglucuronic acid unit (Morais et al., 2015; Bian et al., 2012).

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Several plants are cultivated in large amounts in agroindustry and

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generate a great quantity of lignocellulosic residues. The hemicellulose from

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these residues can be applied into a novel food product, with high-value added.

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There is an increasing interest in to develop new applications of hemicelluloses

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as raw materials for chemical industry and also in the food and pharmaceutical

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industries (Spiridon e Popa, 2008). However, in order to transform this 5

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hemicelluloses in new products, isolate it from the lignocellulosic biomass is

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always the first step.

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1.2.

Isolation of hemicelluloses (pre-treatments)

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Hemicellulose is intimal associated in the plant cell wall with cellulose

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and lignin (Figure 2). Cellulose, the main structural constituent of plant cell wall,

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is a homopolyssacharide composed of D-glucose molecules, linked through O-

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glycosidic bonds of the β-1,4 type. Due to the linearity of its chain, the cellulose

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molecules aggregate giving rise to the fibers, which are embedded by a matrix

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composed of hemicellulose and lignin (Balat, 2011). Lignin is a complex and

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aromatic heteropolysaccharide, basically composed of phenylpropane units,

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which confers rigidity to the plant cell wall. In the cell plant structure, the lignin is

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bound to the side groups of the hemicelluloses through covalent bonds, forming

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a complex matrix that surrounds the cellulose fibers (Rodrigues et al, 2010)

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The hemicelluloses have relatively strong bonds with lignin and cellulose

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in the plant cell wall and therefore it is difficult to separate them without a

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significant change in their structure, requiring some processes to separate

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these fractions (Sun et al., 2004; Brienzo, Siqueira, & Milagres, 2009). To

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isolate hemicellulose from lignocellulosic biomass, different physical, thermal

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and chemical methods can be effective. (Farhat et al., 2017). However, for an

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effective biomass fractionation and recovery of the hemicellulose some

186

requirements must be followed. Lignocellulosic biomass recalcitrance must be

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overcome in order to deconstruct the three-dimensional structure of

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lignocellulose, avoid carbohydrates degradation and in particular preserve the

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utility of the hemicellulose fraction, and also be a low-cost treatment (Yang &

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Wyman, 2008; (Alvira et al., 2010).

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Several types of physical processes have been developed, such as

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milling, grinding, extrusion, and irradiation. These methods are more often

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satisfactory when used in combination with chemical ones, improving the

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process efficiency. The objective of this process is a reduction of the particle

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size, leading to an increase in the available surface. However, these

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mechanical treatments requires high energy, and depending on the type of 6

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biomass and the particle size desired, they can become economically

199

unfeasible (Hendriks & Zeeman, 2009). Hemicelluloses can be obtained by process aiming its isolation, for

201

example, using alkaline medium and oxidative chemicals in alkaline medium.

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On the other hand, hemicellulose can be obtained as residue in same

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pretreatment that aim to modify the lignocellulosic material to increase its

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digestibility. Among these technologies are steam explosion, diluted acid,

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organic solvents, etc. However, using some of these methods the hemicellulose

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is extracted as monosaccharides or oligomers.

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Chemical treatments can be diluted acid or alkaline. Xylan can be

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effectively extracted with acid or alkaline reagents, although glucomannan its

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harder to extract with this method, being able to solubilize only in extreme

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alkaline medium. The main objective of both acid and alkaline treatments is the

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solubilization of the hemicelluloses (Hendriks & Zeeman, 2009).

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Through diluted acid treatment, the hemicellulose is fractionated into

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oligosaccharides or monosaccharides, since the acid cleaves the glycosidic

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bonds of the chain. The chain break is random and depends on the acid type

215

and concentration used, in addition to conditions such as reaction time and

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temperature (Brienzo, Carvalho, Figueiredo & Neto, 2016).

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The hydrogen bonds between cellulose and hemicellulose are disrupted

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through the hydroxide ions present in the alkaline reagents, solubilizing the

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hemicellulosic material. The alkaline extraction also liberate the hemicelluloses

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by cleaving the ester bonds between lignin and hemicellulose, removing the

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lignin without degrading the other components.

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treatment will depend on the lignin content in the biomass (Farhat et al., 2017;

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Alvira et al., 2010; Brienzo et al, 2016).

The effectiveness of this

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Steam explosion is a method that uses hydrothermal treatment to break

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the structure of the lignocellulose material. Subjected to a high pressure steam

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at a high temperature, the biomass is rapidly depressurized causing the

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destruction of the fibrils structure. During this thermal process most of the

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hemicelluloses will solubilized, but its backbone and branching composition will

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determine its stability (Hendriks & Zeeman, 2009; Palm & Zacchi 2003). This

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treatment is mainly used on biomass with higher xylan content, such as agro-

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industrial waste (Brienzo et al, 2016). 7

ACCEPTED MANUSCRIPT Organic solvents such as ethanol also have great potential to isolate

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hemicelluloses, since they are capable of precipitating the polysaccharides from

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the biomass, separating them from the lignin. However, this treatment should be

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used after cellulose separation. Through this treatment, much of the

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hemicellulose can be recovered, but part of it will remain in solution (Peng et al.,

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2012).

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The optimum conditions of the extraction will strictly depend on the

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characteristics of each raw material, mostly its chemical composition, as well as

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on the final purpose of the process itself. Regardless of the extraction method,

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after its separation from the other components of the lignocellulosic biomass,

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the hemicellulose has to be in desirable conditions and able to be transformed

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into new products.

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1.3.

Products from hemicellulose

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Different hemicelluloses can generate specific products depending on their

structure.

Multiple

and

varied

processes

are

needed

for

the

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biotransformation of the hemicellulose into useful products, with high-value

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added (Ebringerová, Hromádková, & Heinze, 2005; Silva et al., 2012).

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Hemicelluloses are an abundant source in nature, their use to

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transformation into products with higher value added would reduce costs of the

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industrial process. Moreover, optimize the use of natural resources is positive,

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reducing environmental damage. The use of hemicelluloses as biopolymers

254

have been studied because of its numerous applications. The advantage of use

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these polysaccharides as biopolymers is the lower cost, if compared to the

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conventional ones (PLA – polylactic acid and PHB – polyhydroxybutyrate), with

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the same biocompatibility and biodegradability properties (Silva et al., 2012).

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Furfural is synthesized in the acid hydrolysis of xylans and used for the

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production of many non-petroleum derived important chemicals. There is no

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synthetic route for furfural production, therefore xylan hydrolysis is important for

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it (Naidu, Hlangothi, & John, 2018). Another important biomacromolecule that

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can be obtained through xylan hydrolysis is chitosan, which has applications in

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food, cosmetics and pharmaceutical industries due to its properties including

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biocompatibility, film-forming and antimicrobial activity. Latic acid, a compound 8

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used to produce biodegradable polymers, can be obtained by fermentation of

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xylan monomeric sugars (Menon, Prakash & Rao, 2010; Luo & Wang, 2013). Xylitol (C5H12O5) is a polyol that has a hydroxyl group attached to each

268

carbon atom in its chain, and possesses a high sweetening power, presenting

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40% fewer calories than sucrose. Xylan derivative, xylitol is a low-calorie

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sweetener used as a preventive agent against dental caries, popularized by its

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use in chewing gums, toothpastes and products for diabetics. It’s used as a

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sugar substitute in the food industry because of its low caloric and anti-

273

carcinogenic properties (Irmak, Canisag, Vokoun, & Meryemoglu, 2017). Xylitol

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can be produced by chemical, thermochemical and biotechnological processes.

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Although, the production cost of xylitol is very high and it is mainly based on

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chemical reduction of xylose derived from birch wood chips and sugarcane

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bagasse (Albuquerque, Silva, Macedo, & Rocha, 2014).

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These products are also prevalent in biorefineries, to produce second

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generation ethanol from waste hemicellulose. In order for this to take place, the

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sugar units present in xylan must be broken into monomeric sugars through the

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hydrolysis process. Currently, diluted acid hydrolysis is the most used for this

282

purpose. The xylose units that are produced from hydrolysis can then be

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converted to ethanol using either bacteria or fungi. Ideally the microorganisms

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used for this conversion should operate under a wide range of temperature and

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pH, show high tolerance to ethanol, osmotic pressure and inhibiters as well as

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high purity, production rate and yield of ethanol (Naidu et al., 2018). However,

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this process is still restricted because microorganisms naturally capable of

288

fermenting xylose are generally poor ethanol producers (Deuschmann &

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Dekker, 2012).

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Because of its hydrophilic characteristics, hemicelluloses can be

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considered a good barrier, in film material, for oils and fats. Hemicellulose film

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has low oxygen and aroma permeability also making it suitable for packing

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applications (Naidu et al., 2018). Besides that, other possibilities for the use of

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xylan would be to convert it into other high value-added products such as

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compounds of chemical and pharmaceutical application (Carvalho, Neto, Silva,

296

& Pastore, 2013). Xylooligosaccharides are unusual oligomers that are

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considered soluble dietary fibers that contain prebiotic activity, favoring the

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improvement of intestinal functions (Carvalho et al., 2013; McKendry, 2002). 9

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Based on that important application, the next topic will discuss its structure and

300

characteristics.

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2. Hydrolysis methods for XOs production The production of xylo-oligosaccharides occurs through the breakdown of

304

the glycosidic linkage in the xylan chain. Such hydrolysis may occur using

305

chemical reagents, temperature or biological agents, such as enzymes.

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2.1.

Chemical and physical-chemical treatments

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In acid hydrolysis, the β-1,4 glycosidic bonds are cleavage and the

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polysaccharides are fractionated to oligosaccharides or monosaccharides. The

311

concentration of the acid reagent should be low to avoid the hydrolysis of the

312

hemicellulose

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monosaccharides can be degraded in products such as furfural or

314

hydroxymethyl furfural (Figure 3). The breaking of the xylan chain through acid

315

hydrolysis can occur through random attack, reducing the degree of

316

polymerization and liberating oligomers or through depolymerization, which

317

depends on chain size and monosaccharides are released (Figure 3). To

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maximize the production of XOS, these two types of reaction need to be

319

controlled, and the random attack should occur more frequently (Brienzo et al,

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2016; Hilpmann et al., 2016; Akpinar, Erdogan, & Bostanci, 2009).

such

as xylose.

In

addition,

released

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Autohydrolysis, in which biomass is treated with only water at elevated

322

temperatures, leads to the production of acetic acid released by the cleavage of

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the acetyl groups in the xylan chain, since the ester linkages are unstable in

324

high temperatures. These acetyl groups on hemicellulose are responsible for

325

acidifying the medium, which pH is around 4, and they will determine the yield

326

and degree of polymerization of XOS produced. In this hydrothermal

327

pretreatment the concentration of XOS will depend on the equilibrium between

328

the breakdown of xylan to XOS and their further decomposition to xylose.

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Although, in moderate conditions the yield of XOS should be high, there is a

330

production of undesirable compounds, such as xylose and degradation

331

productions of sugars and lignin (Brienzo et al, 2016; Otiedo & Ahring, 2012,

332

Nabarlatz, Ebringerová, & Montamé, 2007).

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333

XOS

production,

the

hemicellulose

present

in

the

lignocellulosic material should be isolated through alkaline extraction. The

335

hydroxide ions present in the alkaline reagents break the hydrogen bonds

336

between cellulose and hemicellulose, solubilizing the hemicellulose portion of

337

the material. In addition, alkaline extraction liberates the hemicellulose by

338

breaking the ester bonds with the lignin, removing it without degrading other

339

compounds (Farhat et al., 2017; Brienzo et al, 2016).

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2.2.

344

The production of xylooligosaccharides (XOS) through enzymatic

345

hydrolysis requires two steps. First, the hemicellulose present in the

346

lignocellulosic material should be isolated through the different pre-treatments.

347

For that purpose, it’s important to remember that the selection of the pre-

348

treatment should be based on the desirable final characteristics of the

349

hemicellulose recovered, as polysaccharide or monosaccharide (Brienzo et al,

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2016).

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The xylan molecule has a wide variety of bonds and types of branching.

352

Complex structures are interconnected by covalent and ionic bonds that provide

353

a physical barrier limiting the action of some enzymes, because for the reaction

354

to occur, a direct contact between enzyme and substrate is necessary. The

355

structure of the substrate, influenced by the characteristics of the material and

356

the interactions of the enzyme with this substrate, which depends on the nature

357

and origin of the enzymatic complex, are factors that can influence the

358

performance of the enzymatic hydrolysis. Another factor that must be taken into

359

account is the heterogeneity of the lignocellulosic material, so for better action

360

of the enzyme it is necessary to isolate the polysaccharide of interest (Moreira &

361

Filho, 2016; Sant’anna, Souza, & Brienzo, 2014).

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The next step is the enzymatic hydrolysis of xylan, which must be

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performed by the enzyme endo-β-1,4-xylanase, with little or no activity of the β-

364

xylosidase enzyme, since the objective is the production of oligomers and not of

365

monosaccharides (xylose). However, xylanases with different substrate

366

specificities generate different hydrolysis products, having a difficulty in 11

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controlling the degree of polymerization of the XOS produced (Akpinar,

368

Erdogan, Bakir, & Yilmaz, 2010). The endo-β-1,4-xylanase enzyme acts on the xylan backbone and

370

generates low degree of XOS polymerization. For complete hydrolysis of

371

hemicellulose, accessory enzymes acting on the backbone branches are

372

necessary and the its presence or absence may generate XOS with or without

373

branching. Branched xylooligosaccharides can be produced by enzymatic

374

hydrolysis without the presence of auxiliary enzymes and such branching may

375

influence the rate of hydrolysis of xylan, which depends strongly on the amount

376

of these enzymes (Brienzo et al, 2016; Puchart & Biely, 2008).

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The endoxylanases of the GH 10 and GH 11 families differ in specificity

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to the substrate. Those of the GH 10 family are less specific to xylan as the

379

substrate and are capable of hydrolyzing substituent forms of the xylan chain

380

producing oligosaccharides containing substituents at the non-reducing terminal

381

of the molecule. Endoxylanases of the GH 11 family, known as true xylanases,

382

are restricted to xylan hydrolysis and act on unbranched regions of the

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polysaccharide. Thus, the endoxylanases of the GH 10 family produce XOS

384

with a lower degree of polymerization than those of the GH 11 family (Moreira &

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Filho, 2016).

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The enzymatic hydrolysis of hemicellulose is a complex solid-liquid two-

387

stage catalytic reaction process, where the enzymes are adsorbed from the

388

liquid phase to the solid substrate. The adsorbed enzymes catalyze the

389

insoluble substrate in the solid phase simultaneously with the dissolved

390

enzymes that catalyze the soluble substrate in the liquid phase. The solid phase

391

hydrolysis consists on several steps, such as the adsorption of the enzyme on

392

the surface of the substrate, with conformational changes, occurs formation of a

393

complex by the electrostatic interaction, ending with breakdown of bonds and

394

solubilization of short chain xylooligosaccharides in the liquid phase. (Dutta &

395

Chakraborty, 2015).

AC C

EP

386

396

The conditions of the enzymatic hydrolysis of hemicellulose in xylo-

397

oligosaccharides should be optimized in order to obtain a more economical

398

bioprocess through a higher yield. Some microbiological and biochemical

399

aspects of the enzymatic hydrolysis by the endoxylanases can influence the

400

production of xylooligosaccharides, and for that reason reaching the ideal 12

ACCEPTED MANUSCRIPT 401

enzyme and substrate concentration, reaction time and temperature are

402

necessary for the optimization of this bioprocess. In addition, the presence of

403

small amounts of β-xylosidases is important to obtain a higher concentration of

404

XOS and little conversion of these to xylose (Brienzo et al, 2016; Carvalho et

405

al., 2013). The enzymatic hydrolysis is a widely studied process for lignocellulosic

407

materials, since the bioconversion of agroindustry residues, besides generating

408

molecules of greater added value, can also help in reducing the environmental

409

impact caused by its accumulation. This type of hydrolysis, unlike acid

410

hydrolysis and auto hydrolysis, does not present secondary reactions or the

411

formation of by-products. In addition, reactions occur in a mild way and do not

412

require high temperature or pressure (Brienzo et al, 2016).

SC

RI PT

406

414

M AN U

413

3. Xylooligosaccharides (XOS)

Oligosaccharides can be defined as naturally occurring carbohydrates

416

that consist of 2 to 10 monosaccharide units, linear or branched, connected by

417

α- and/or β-glycosidic linkages, according to the IUB-IUPAC nomenclature.

418

These molecules can be composed by different monosaccharides and the main

419

classes are composed by units of fructose, galactose, glucose and xylose (Zhao

420

et al., 2017). They can be used in the food industry as a partial substitute of

421

sugars, but they also have prebiotic qualities because they promote the growth

422

of beneficial bacteria. These properties can improve the quality of many foods

423

as well as the health of the consumer (Kumar, Pushpa & Prabha, 2012).

EP

AC C

424

TE D

415

Xylooligosaccharides (XOS) are sugar oligomers constituted of xylose

425

units linked through β-1,4 glyosidic bonds (Figure 4). There are xylobiose,

426

xylotriose, xylotetrose, xylopentose and so on, depending of the quantity of

427

monomers that comprises the molecule chain. They can be found in fruits,

428

vegetables, milk and honey. Moreover, XOS can be produced from xylan from

429

the lignocellulosic residues, which can contain 25-50% in dry mass (Samanta et

430

al., 2015). Varying the xylan source for XOS production, their structure will be

431

different in degree of polymerization and quantity of monomeric units. Xylan is

432

usually found in combination with side groups such as arabinofuranosyl

13

ACCEPTED MANUSCRIPT 433

residues and acetyl groups, which can lead to the formation of branched XOS

434

with diverse biological properties (Aachary & Prapulla, 2010). Among their physico-chemical properties, XOS are crystalline solid and

436

its color depends on the source of xylan. The molecular mass can vary and their

437

sweetness correspond to approximately 30% of sucrose and possess no off-

438

taste (Samanta et al., 2015). They are stable over a wide range of pH (2,5 –

439

8,0) and temperatures (up to 100ºC), have an acceptable odour, are non-

440

cariogenic and low-calorie, what are good properties for food ingredients. They

441

also present higher hygroscopicity than xylose, but similar to glucose (Vázquez,

442

Alonso, Domínguez & Parajó, 2000; Hiryama, 2002).

SC

RI PT

435

Xylooligosaccharides are non-digestible oligosaccharides, meaning that

444

they are not degraded in the human stomach and reach the intestinal tract intact

445

thanks to the lack of enzymes capable of hydrolyzing β-bonds in the human

446

body. Besides that, XOS promotes the proliferation of the beneficial

447

microorganisms. However, the prebiotic property of these oligomers is only one

448

of the many biological properties that they can present (Carvalho et al., 2013).

M AN U

443

XOS that contain uronic acids as branch are known to present

450

antioxidant and antialergic properties, due to its phenolic substituents (Jain,

451

Kumar, & Satyanarayana, 2015). Research shows that XOS presented

452

antioxidant activity in rats experimentally induced with diabetes, increasing

453

plasma concentration of antioxidant enzymes and reducing plasma glucose,

454

cholesterol and creatinine levels. Although the mechanism of reduction of

455

adverse effects of oxidative stress by XOS is not well known, a diet containing

456

XOS decreased the symptoms of oxidative stress (Samanta et al., 2015;

457

(Gobinath, Madhu, Prashant, Srinivasan & Prapulla, 2010).

EP

AC C

458

TE D

449

XOS can present a beneficial effect in metabolic conditions of diabetes

459

because of their ability to control body weight, glucose and lipid homeostasis

460

and insulin sensitivity. These characteristics can be attributed to the production

461

of SCFA in colon, which increases sodium and water absorption in distal

462

intestine improving polydipsia (Alisteo, Duarte, & Zarzuelo, 2008). Another

463

biological function of XOS is the reduction of muscle protein degradation for

464

energy production, because during the fermentation of the oligomers, acetic

14

ACCEPTED MANUSCRIPT 465

acid is produced, absorbed by the circulatory system and used as an energy

466

source (Singh, Banerjee, & Arora, 2015). The biological activity of XOS will depend on their degree of

468

polymerization that can vary from 2 to 12. Those with less than four monomeric

469

units have prebiotic applications because they promote the proliferation of

470

beneficial bacteria in the human intestinal tract, such as bifidobacteria, which

471

inhibit the growth of pathogenic bacteria. These bacteria selectively utilize the

472

XOS for their growth resulting in the production of short chain fatty acids

473

(SCFA), which is related to the prevention of colon cancer (Carvalho et al.,

474

2013).

SC

RI PT

467

XOS can be substitutes of antibiotics in animal feed, since they have

476

positive effects in animal health and similar to the antibiotics, without the

477

possibility of causing resistance to pathogenic bacteria. They can also be used

478

in agriculture, for the development of growth stimulants and in the

479

pharmaceutical industry, for the production of drugs related to the control of

480

obesity and treatment of gastrointestinal infections (Vázquez et al., 2000;

481

Moure, Gullón, Domínguez, & Parajó, 2006).

482

Currently,

Japan

is

M AN U

475

the

largest

producer

and

consumer

of

xylooligosaccharides, but the market and consumption of these non-digestible

484

oligosaccarides has gradually grown worldwide, as there is a growing concern

485

about quality of life and health, increasing interest in food which have functional

486

substances (Brienzo et al, 2016; Barreto, Zancan, & Menezes, 2015). Because

487

they possess diverse biological activities, XOS can be incorporated as

488

ingredients in foods in order to promote the improvement of health. However, its

489

dosage should be made carefully, since the recommended daily amount of its

490

consumption is between 2 and 5 grams (Gobinath et al., 2010; Mussato &

491

Manchila, 2007).

493

EP

AC C

492

TE D

483

4. XOS effects on micro-organisms

494

A prebiotic can be defined as a “ingredient fermented selectively that

495

results in specific changes on the composition and/or activity of gastrointestinal

496

microbiota, conferring benefits to host health”. Gibson, Scott, Rastall, &

497

Buddington, 2010). To be considered as a prebiotic, the compound must

498

withstand the digestion, absorption and adsorption processes of the host, be 15

ACCEPTED MANUSCRIPT 499

fermentable by the microbiota present in the gastrointestinal system and

500

selectively stimulate the growth and activity of at least one of the probiotic

501

bacteria present in the gastrointestinal tract (Petrova & Petrov, 2017). XOS are considered prebiotic because of their selective potential to

503

stimulate growth of beneficial microorganisms in the intestinal tract. They are

504

able to increase the growth and multiplication of bifidobacteria and lactobacillus,

505

thus reducing the activity of harmful bacteria and the concentration of toxic

506

fermentation products (Samanta et al., 2015). Studies to evaluate the prebiotic

507

effects have been done in vitro for humans and animals, considering the

508

microorganisms common in both humans and animals guts and verifying the

509

potential of stimulating growth of beneficial microorganisms and inhibiting the

510

pathogenic ones (Brienzo et al, 2016). major

probiotic

M AN U

The

511

SC

RI PT

502

bacteria

that

are

present

in

the

human

gastrointestinal tract are of the genus Bifidobacterium and Lactobacillus.

513

Bifidobacteria are able to efficiently ferment oligo or polysaccharides composed

514

of xylose, but the ability of bifidobacteria to metabolize XOS depends on the

515

efficiency of their xylanolytic enzyme systems. Both genera produce enzymes

516

that degrade carbohydrates and ferment non-digestible oligosaccharides,

517

producing short chain fatty acids that promote metabolic energy for the host as

518

well as help with acidification of the intestine (Madhukumar & Muralikrishna,

519

2011).

TE D

512

The main prebiotic effect of XOS, that is to promote the growth of

521

probiotic bacteria, has been studied since 1990. Thereafter, results have shown

522

that these bacteria grow more efficiently in xylose, xylobiose and xylotetrose

523

than in other carbon sources. Also, XOS inhibit the growth of several

524

pathogenic

525

Staphylococcus aureus. Among the probiotic bacteria, those that respond best

526

to XOS are those of the genus Bifidobacterium, presenting a significant

527

increase in their growth, whereas the bacteria of the genus Lactobacillus are

528

little affected (Table 1) (Petrova & Petrov, 2017).

AC C

EP

520

bacteria

such

as

Clostridium

perfringens,

E.

coli,

and

529 530 531 16

ACCEPTED MANUSCRIPT Conclusion

533

Due to the increase in the amount of agroindustrial waste generated

534

each year, the use of these materials for the development of higher value-

535

added products has been the subject of much research. An important part of

536

these residues are the hemicelluloses, which provides many potential

537

applications such as the generation of chemicals, packing materials, drug

538

delivery and biomedical applications.

RI PT

532

One important application is their conversion into xylooligosaccharides.

540

Several types of process can the used to hydrolysis xylan for the formation of

541

XOS. Enzymatic hydrolysis is a more sustainable process and, when carried out

542

under the optimum conditions, higher yields can be obtained. There is the

543

advantage of no by-product (degradation products) formation. However, for

544

industrial application, enzymatic hydrolysis still needs more improvement in

545

order to reach feasibility.

M AN U

SC

539

XOS occupy a significant space in the prebiotic market because of its

547

diverse influences on human health, including improvement in bowel function,

548

calcium absorption, prevention of dental caries and reduction in the risk of colon

549

cancer. Its production derived from abundant and cheap raw material offers a

550

great opportunity for the pharmaceutical industries. In addition, the conversion

551

of xylan to higher value-added products holds promise for the use of a wide

552

variety of agricultural waste that is currently underutilized.

553 554 555

Acknowledgments

557 558 559 560 561 562 563

EP

The authors thank the São Paulo Research Foundation – FAPESP (grant

AC C

556

TE D

546

number 2017/11345-0) for financial support.

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Bifidobacterium

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enzymes

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hemicellulose

Conversion

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RI PT

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wheat

bran

insoluble

dietary

fiber

by

AC C

EP

from

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cellulosic ethanol. Biofuels, Bioproduts & Biorefining, 2, 26–40.

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of oligosaccharides. Trends in Food Science & Technology, 66, 135-145.

RI PT

770

775 776

778

SC

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Table Caption

780 781

M AN U

779

Table 1. Effect of XOS on the growth of beneficial and pathogenic microorganisms.

782

786 787 788 789 790 791 792 793 794

Figure 1. Structure of xylan showing different intermolecular bonds and substitutions.

EP

785

Figure Caption

Figure 2. Disposition of cellulose fibers, hemicellulose and lignin in the plant cell wall (Brandt, Gräsvik, Hallett, & Welton, 2013).

AC C

784

TE D

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Figure 3. Acid action on xylan backbone.

Figure 4. Enzyme action on xylan backbone.

795 796

Figure 5. Xylooligosaccharides structure.

797

25

ACCEPTED MANUSCRIPT Table 1

Source of XOs

Concentration of XOs

Effect

Reference

B. adolescentis

Corncob xylan

10g/L

Growth

B. bifidum

Corncob xylan

10g/L

Growth

L. acidophillus

Corncob xylan

10g/L

B. longum

Wheat bran

5g/L

B. breve

Wheat bran

5g/L

B. adolescentis

Wheat bran

5g/L

Growth

L. plantarum

Bengal gram husk

50g/L

Growth

(Chapla, Pandit, & Shah, 2012) (Chapla, Pandit, & Shah, 2012) (Chapla, Pandit, & Shah, 2012) (Wang, Sun, Cao, & Wang, 2010). (Wang, Sun, Cao, & Wang, 2010). (Wang, Sun, Cao, & Wang, 2010). (Madhukumar &

Wheat bran

Growth

Growth

SC

M AN U

Bengal gram husk

Growth

50g/L

50g/L

Muralikrishna, 2011). Growth

2011). Growth

AC C

(Madhukumar & Muralikrishna, 2011).

50g/L

Growth

(Madhukumar & Muralikrishna, 2011).

Bifidobacteruim genus

Birchwood xylan

400g/L

Growth

S. hominis

Birchwood xylan

200g/L

Growth

S. aureus

Birchwood xylan

200g/L

Inibition

Bifidobacteruim genus Lactobacillus genus E. coli

Miscanthus x giganteus Miscanthus x giganteus Miscanthus x giganteus Miscanthus x

6g/L

Growth

6g/L

Growth

6g/L

Inibition

6g/L

Unaffected

C. perfringens

(Madhukumar & Muralikrishna,

EP

B. adolescentis

Wheat bran

TE D

L. plantarum

B. adolescentis

RI PT

Microorganism

(NietoDomínguez et al., 2017) (NietoDomínguez et al., 2017) (NietoDomínguez et al., 2017) (Chen et al., 2015) (Chen et al., 2015) (Chen et al., 2015) (Chen et al.,

ACCEPTED MANUSCRIPT giganteus L. plantarum

2015)

Wheat husk

35g/L

Growth

(Jagtap, Deshmukh, Menon, & Das, 2017).

Wheat husk

35g/L

Growth

(Jagtap,

RI PT

L. fermentum

Deshmukh,

Menon, & Das,

Wheat husk

35g/L

Growth

M AN U

SC

B. bifidum

100g/L

Growth

E. coli

Corncob xylan

100g/L

Inibition

TE D

Deshmukh,

2017).

Corncob xylan

EP

(Jagtap,

Menon, & Das,

L. acidophillus

AC C

2017).

(Pedraza et al., 2014) (Pedraza et al., 2014)

AC C

EP

TE D

M AN U

SC

RI PT

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AC C

EP

TE D

M AN U

SC

RI PT

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AC C

EP

TE D

M AN U

SC

RI PT

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AC C

EP

TE D

M AN U

SC

RI PT

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AC C

EP

TE D

M AN U

SC

RI PT

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ACCEPTED MANUSCRIPT Highlights •

XOS can be produced from lignocellulosic biomass by chemical and enzyme route. Xylan component of the biomass can be used for XOS production.

•

Hemicelluloses differ from softwoods, hardwoods and grasses, generation

RI PT

•

different XOS.

XOS are emerging prebiotic and present bioactive properties.

•

Different kind of XOS, DP and substitution, can contribute to diverse effects on

SC

•

AC C

EP

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M AN U

microorganisms.