Seaweed carbohydrates

CHAPTER

Seaweed carbohydrates

7

Laurie-Eve Rioux, Sylvie L. Turgeon Department of Food Science, Institute of Nutrition and Functional Food, Université Laval, Quebec City, QC, Canada

1 INTRODUCTION Algae are very versatile in their usage in several areas of interest such as human and animal nutrition, cosmetics, and fertilizers. The total annual production of algae has a commercial value of 6 billion US dollars, of which 5 billion are for food products for human consumption (McHugh, 2003). In 1990, 5 million tons of fresh seaweed was needed for different sectors annually as compared to 24 million tons required in 2012 (FAO, 2014). The seaweed production mostly comes from cultivated crops while naturally growing (wild) seaweed levels remained similar throughout the years (Figure 7.1). In 2012, Asia was producing 96.3% of the world seaweed market (Figure 7.2) from which 89% of the harvest seaweeds came from China (55%), Indonesia (27%), and the Philippines (7%) (FAO, 2014). These data are not surprising since China, Japan, and Korea are the largest consumers of seaweed as food. Traditionally, algae were consumed fresh or blanched and were found in salads, soups, or toppings (Yuan, 2008). Among the cultivated and wild food preferred brown seaweed, 5.7 million tons of “kombu” (Saccharina japonica) and 2.1 million tons of “wakame” (Undaria pinnatifida) were harvested in 2012 (FAO, 2014). The valuable food algae Porphyra, also called “nori,” is particularly important in Japanese culture, and 1.8 million tons were harvested in 2012 (FAO, 2014). More recently, the consumption of dried seaweed has increased in popularity in Europe and North and South America with the appearance of “sushi” and the migration of the Asian population across the globe. Among the macroalgae, Ulva, Caulerpa (phylum Chlorophyta), Laminaria (phylum Ochrophyta), and Porphyra (phylum Rhodophyta) are traditionally used (Atlas and Bartha, 1998). In Japan, the unicell alga Chlorella (phylum Chlorophyta) is also added to food as a source of vitamins and protein in yogurt, ice cream, etc. (Atlas and Bartha, 1998). Algae are low in fat (below 5%) and contain many minerals and vitamins (Table 7.1) (Holdt and Kraan, 2011). Variable amounts of proteins are found between species. Up to 44% and 50% of protein can be found, respectively, for Ulva and Porphyra species while the maximum content for Undaria is 24%. The amount of polysaccharides in seaweeds can reach up to 76% but usually averages 50%. Among Seaweed Sustainability. http://dx.doi.org/10.1016/B978-0-12-418697-2.00007-6 Copyright © 2015 Elsevier Inc. All rights reserved.

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CHAPTER 7  Seaweed carbohydrates

FIGURE 7.1  Global Production of Seaweed from Cultivated Crops and Naturally Growing (Wild) Seaweed “All” represents the sum of cultivated and wild seaweed. Adapted from FAO (2014).

FIGURE 7.2  Global Production of Seaweed from Cultivated Crops and Naturally Growing (Wild) Seaweed in 2012 for Each Continent Adapted from FAO (2014).

the fibers, hydrocolloids such as alginate, agar, carrageenans, fucoidan, and laminaran are present in large proportions in algae. Many of these polysaccharides are used in foods as thickeners, gelling agents, and emulsion stabilizers. In 2009, 86,100 tons of hydrocolloids were traded, which represents 58% of carrageenan, 31% of alginate, and 11% of agar (Bixler and Porse, 2011). Recently, some have also demonstrated

Table 7.1 Composition* of Different Seaweed Species Based on Phylum Chlorophyta (green)

Ochrophyta (brown) Laminaria and Saccharina Fucus

Ulva Polysaccharides (% of dry weight)

15–65%

Total protein (% of dry weight) Total lipid (% of dry weight) Ash (% of dry weight) Moisture (% of wet weight)

4–44%b,g,o,q,r,w,y,ff,ll 3–21%b,d,e,g,k,jj,ff,kk 1.4–17%b,g,k,ee

t,u,w,y,ee,hh

38–61%

d,k,ee,ff

62–66%

k,ee

Rhodophyta (red)

Ascophyllum

Undaria

Sargassum

Chondrus Porphyra

Gracilaria

Palmaria

42–70%

35–45%

4% ; 68%

55–66%

36% ; 62–63%d,r

38–74%cc,ee,ii

1.2–12%i,k,m,ee

11–24%g,o,p, 9–20%g,s,r

5–23%d,r

8–35%dd, cc,mm

k,ee,gg

p,q

r

r

ee

6–29%b,o,r,t,u 7–50%b,d,q,r,bb,

q,bb,ff

0.3–1.6%b,t,w,y,ee,nn 0.3–2.9%b,d,e,

r

ee,ff,nn

0.5–3.1%b,j,k,ee,oo 1.2–4.8%k,m,ee

1–4.5%j,o,q,t,ff 0.5–3.9%j,r,ee,ff 0.7–3%ee,pp 0.12–2.8%b,.o,q, 0.4–2.6%d,r,qq,rr 0.2–3.8%cc,ee,ss

15–45%d,e,f,g

19–30%b,k,l,g

18–27%m

27–40%g,l,p,q 14%r; 44%s

21%l,g

7–21%b,c,d,l,g,q,bb 8–29%d,r,s

12–37%j, cc,dd

73–94%a,b,c,d

68–87%b,h,J,J

67–87%h,m,n

88%j

72–78%z,aa

77–91%b,c,d

84%cc

k,ee,ff,kk,jj

11–26%b,c,t,u,v; 52–55%w,x,y 78–80%b,c,f

40–76%

d,q,bb,ee

bb,ee,ff,nn

61%j

85%d

Adapted from Holdt and Kraan (2011). Horn (2000); bMarsham et al. (2007); cFoti (2007); dWen et al. (2006); eJensen and Haug (1956); fLamare and Wing (2001); gRuperez and Saura-Calixto (2001); hBaardseth and Haug (1953); iLarsen and Haug (1958); jHerbreteau et al. (1997); kRioux et al. (2007a); lRuperez (2002); mJensen (1960); nJensen (1966); oPlaza et al. (2008); pJe et al. (2009); qMurata and Nakazoe (2001); rMarinho-Soriano et al. (2006); sRobledo and Pelegrín (1997); tOrtiz et al. (2006); uVentura and Castañón (1998); vBobin-Dubigeon et al. (1997); wFoster and Hodgson (1998); xWong and Cheung (2001); yWong and Cheung (2000); zSimpson and Shacklock (1979); aaHoldt (2009); bbArasaki and Arasaki (1983); ccMishra et al. (1993); ddMorgan et al. (1980); eeMorrissey et al. (2001); ffDawczynski et al. (2007); ggTseng (2001); hhSathivel et al. (2008); iiHeo and Jeon (2009); jjHaug and Jensen (1954); kkMcHugh (2003); llBarbarino and Lourenco (2005); mmGalland-Irmouli et al. (1999); nnIndegaard and Minsaas (1991); ooKim et al. (1996); ppTasende (2000); qqKhotimchenko (2005); rrKhotimchenko and Levchenko (1997); ss Morgan et al. (1980). *

a

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CHAPTER 7  Seaweed carbohydrates

Table 7.2  Seaweed Classification Based on Pigmentation Phylum

Subphylum

Class

Genus

Chlorophyta

—

Ulvophyceae

Ochrophyta

—

Phaeophyaceae

Rhodophyta

Bangiophyceae Eurhodophytina

Bangiophyceae Florideophyceae

Caulerpa, Enteromorpha, Monostroma, Ulva Ascophyllum, Chorda, Durvillea, Ecklonia, Eisenia, Fucus, Laminaria, Lessonia, Macrocystis, Sargassum, Undaria Porphyra Ahnfeltia, Anatheca, Caloglossa, Dilsea, Eucheuma, Furcellaria, Gelidiella, Gelidium, Gigartina, Gloiopeltis, Gracilaria, Gynmogongrus, Hypnea, Iridaea, Kappaphycus, Meristotheca, Phyllophora, Pterocladia

Adapted from Guiry and Guiry (2014).

numerous biological activities including anticoagulant, anti-inflammatory, antiviral, and immune system-boosting properties (Fitton et al., 2008; Nagaoka et al., 2000). These activities have been reported for different species of algae and different types of structures. Marine macroalgae are grouped into three classes based on their pigmentation: brown (Ochrophyta), green (Chlorophyta), and red (Rhodophyta) algae (Table 7.2).

1.1  BROWN SEAWEED (OCHROPHYTA) Ochrophyta seaweed are divided into 20 classes (Guiry and Guiry, 2014). In the Phaeophyceae class, over 1800 species of brown algae are found (Guiry and Guiry, 2014). The Dictyotales, Ectocarpales, Fucales, and Laminariales are orders that include the most species. Several species have significant commercial value, such as genera Laminaria, Undaria, Macrocystis, Sargassum, and Fucus (Ito and Hori, 1989). All brown algae are pluricellular, most live in salted water, and are abundant in temperate-coastal zones in cold water.

1.2  RED SEAWEED (RHODOPHYTA) Red algae primarily grow in marine water with a few exceptions (Rindi et al., 2012). Rhodophyta algae are divided into four subphylum and eight classes. The two most important classes regarding hydrocolloid production are the Bangiophyceae and the Florideophyceae, which represent 161 and 6224 species, respectively (Table 7.2) (Guiry and Guiry, 2014). Species of the genus Porphyra, Gelidium, Gloiopeltis, Eucheuma, and Gracilaria are the most widespread all over the globe.

2 Types of carbohydrates

1.3  GREEN SEAWEED (CHLOROPHYTA) Green algae are highly diverse in the terms of morphology, ranging from microscopic unicells to macroscopic multicellular algae (Lewis and McCourt, 2004). In addition, macroalgae are rarely more than a meter long. Green algae are photosynthetic eukaryotes, carrying plastids containing chlorophyll a and b as well as starch (Lewis and McCourt, 2004). They grow in marine- or freshwater lakes and rivers. This phylum contains nine classes. Chlorodendrophyceae (46 species), Chlorophyceae (3046 species), Ulvophyceae (1610 species), and Trebouxiophyceae (672 species) are the four main classes (Guiry and Guiry, 2014). Green algae are slightly more exploited worldwide, and only species of the genus Monostroma, Caulerpa, and Enteromorpha that is a part of the Ulvophyceae class are grown commercially (Figure 7.2).

2  TYPES OF CARBOHYDRATES Polysaccharide content in algae is influenced by several biological, physical, and environmental factors. For example, the harvest period, the algal species, and the extraction protocol influence yields of polysaccharide and their structures. This has a significant impact on the functional properties of the polysaccharides. The molecular weight, the nature of building units, the content of sulfate groups and their positions, the type of glycosidic bond, and the geometry of the molecule (Melo et al., 2002; Shanmugam and Mody, 2000) are very important structural characteristics. Most algal polysaccharides are a part of the cell wall of the algae with an exception of storage carbohydrates, which are located in the plastid. Each of them plays different roles in the algae.

2.1  STORAGE POLYSACCHARIDES Unlike plant metabolism, storage carbohydrates in algae serve as a photosynthetic reserve and some of them as osmoregulators. Their amounts vary according to the seaweed species and the environmental factors (temperature, the water’s nutrients and salinity, water movement, etc.). Several low molecular weight organic solutes were found in different algal species under elevated salinity conditions (Ben-Amotz and Avron, 1983) as mannitol (Phaeophyceae, Florideophyceae), sucrose (Ulvophyceae), floridoside (Florideophyceae), isofloridoside (Florideophyceae), and digeneaside (Bangiophyceae) (Ben-Amotz and Avron, 1983; Edwards et al., 1987; Reed, 1989). Some of them will be briefly introduced in Section 2.5.3. Other larger storage polysaccharides are also found in macroalgae and they play a central role in the algae life cycle as their principal source of energy (Busi et al., 2014). In Rhodophyta, the main storage carbohydrate, Floridean starch (Section 2.5.3.1), is deposited in the cytoplasm. However, for Chlorophyta, the reserve polysaccharide, starch, is located under the form of grains inside the chloroplast. In Orchrophyta, the main reserve polysaccharide is laminaran (Section 2.5.2), which is found in a vacuole inside the chloroplast (Barsanti and Gualtieri, 2014).

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2.2  CELL-WALL POLYSACCHARIDES The cell wall/extracellular matrix of macroalgae has a structural function. It protects against dehydration, waves, ice, etc. (Percival, 1979). It also regulates turgor, solute accumulation, cell differentiation (development), and innate immunity (Brownlee, 2002; Reed, 2010). The cell wall constitutes different polysaccharides based on the algae class (Table 7.3). In Florideophyceae (Rhodophyta), sulfated galactan (agar and carrageenan) represents ∼70% of the cell wall constituents, and cellulose represents 7–24% according to the seaweed species (Barsanti and Gualtieri, 2014; Cronshaw et al., 1958). In Bangiophyceae, however, a low level of cellulose (3.5%) was found for Porphyra ssp. (Cronshaw et al., 1958). The terminal cellulose complexes form single rows in red algae, resulting in a flat ribbon-like or a rectangular-parallelepiped structure (Collén et al., 2014; Tsekos, 1999). Other cell wall polysaccharides such as xylan, mannan, and hemicellulose (glucomannan, sulfated mixed-linkage glucan, xylan) are also present but will not be covered in this chapter. Readers are referred to review papers on this topic (Craigie, 2010; Kloareg and Quatrano, 1988; Painter, 1982; Popper et al., 2011; Usov, 2011). Red algae are well known for their gelling compounds such as agar (Section 2.4.1) and carrageenan (Section 2.4.3), which will be described in the next sections. Anticoagulant (Farias et al., 2000) and antiviral (Carlucci et al., 1997) activities have been demonstrated for those polysaccharides. In brown algae, sulfated fucans and alginates represent up to 45% of the algal dry weight (Kloareg and Quatrano, 1988), while cellulose only accounts for 1–8%. Table 7.3  Major Cell-Wall Polymers Present in Different Algal Classes* Ulvophyceae

Bangiophyceae/ Florideophyceae Cellulose ; (1→4)-b-dmannan§; (1→4)-b-d-xylan¶,††; (1→3)-b-d-xylan¶,†† Glucomannan‡‡; Sulfated (1→3),(1→4)-b-d-glucan‡‡; (1→3),(1→4)-b-d-xylan§,¶,††

Phaeophyceae Cellulose§

Crystalline polysaccharides

Cellulose**

Hemicelluloses

Xyloglucan†,‡; Mannans§; Glucuronan‡ (1→3)-b-glucan

Matrix carboxylic polysaccharides Matrix sulfated polysaccharides

Ulvans†

–

Sulfated xylofucoglucan§,††; Sulfated xylofucoglucuronan§,††; (1→3)-b-glucan Alginates††

Ulvans†

Agars§,††; Carrageenans§

Homofucans§,††

Adapted from Popper et al. (2011). Tsekos (1999). † Lahaye et al. (1994). ‡ Lahaye and Robic (2007). § Painter (1982). ¶ Craigie (2010). †† Kloareg and Quatrano (1988). ‡‡ Lechat et al. (2000). *

**

§

2 Types of carbohydrates

FIGURE 7.3  Cell-Wall Model of Seaweed from the Fucales Order (Ochrophyta) Reprinted from Deniaud-Bouët et al. (2014). Chemical and enzymatic fractionation of cell walls from Fucales: insights into the structure of the extracellular matrix of brown algae. Annals of Botany, First view, with permission of Oxford University Press.

Some Laminaria ssp. can contain up to 20% of cellulose (Cronshaw et al., 1958). The terminal cellulose complexes form single rows in brown algae, resulting in a “flat ribbon-like shape of cellulose microfibrils” (Tamura et al., 1996; Tsekos, 1999). Additional components such as proteins, phlorotannins (protein phenol), and iodine are also found and contribute to the matrix structure (Mabeau and Kloareg, 1987). Their organization and interaction were summarized in a model based on the Fucales order cell wall (Figure 7.3). Hemicellulose is also present and contributes to the matrix structure but will not be described here. Readers are referred to review papers for additional information (Kloareg and Quatrano, 1988; Painter, 1982). The main cell wall polysaccharides, alginate (Section 2.4.2), and fucose-containing sulfated polysaccharides (Section 2.5.1) will be discussed in the subsequent sections. In Ulvophyceae (green algae) between 19% and 41% of cellulose was found (Cronshaw et al., 1958), and for some of them, cellulose was under the form of granule bands (Tsekos, 1999). Hemicellulose is also present and contributes to the cell wall structure but will not be covered in this chapter. Readers are referred to review papers for additional information (Lahaye et al., 1994; Lahaye and Robic, 2007; Painter, 1982). Significant amounts of proteins were also detected (13.9%) (Lahaye et al., 1994). Ulvan is also present in high proportion (8–29%) (Lahaye and Robic, 2007). Its organization and interaction was summarized in a model based on the Ulva cell wall (Figure 7.4). The valuable cell wall polysaccharide, ulvan, will be described in Section 2.5.3.3.

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FIGURE 7.4  Cell-Wall Model of Seaweed of Ulva ssp. (Chlorophyta) Reprinted with permission from Lahaye and Robic (2007). Structure and function properties of Ulvan, a polysaccharide from green seaweeds. Biomacromolecules, 8, 1765–1774. Copyright (2007) American Chemical Society.

2.3  FIBERS DEFINITION Algae are usually recognized as good sources of fiber due to their high polysaccharide content undigested by humans. The term “dietary fiber” usually refers to indigestible carbohydrates of dietary origin. They pass the small intestine intact and can be fermented partly or nearly completely into the large intestine. This term, introduced in the 1940s, initially referred to carbohydrates that resisted digestion and improved laxation. The wide variety of carbohydrates falling into that category represents a challenge to determining an accurate methodology allowing dietary fiber quantification. In 2013 the CODEX Alimentarius Commission (FAO/WHO, 2013) defined dietary fiber in the following manner: Dietary fiber means carbohydrate polymers1 with 10 or more monomeric units2, which are not hydrolysed by the endogenous enzymes in small intestine of humans and belong to the following categories: 1. Edible carbohydrate polymers naturally occurring in the food as consumed. 2. Carbohydrate polymers, which have been obtained from food raw material by physical, enzymatic or chemical means and which have been shown to have a physiological effect of benefit to health as demonstrated by generally accepted scientific evidence to competent authorities.

May include fractions of lignin and/or other components associated with polysaccharides in the plant cell walls. 2 Some countries may decide to include carbohydrates from 3 to 9 monomeric units in the fiber content. 1

2 Types of carbohydrates

3. Synthetic carbohydrate polymers, which have been shown to have a physiological effect of benefit to health as demonstrated by generally accepted scientific evidence to competent authorities.

2.3.1  Classification of types of fibers: soluble versus insoluble Dietary fiber refers to the total fiber content of an ingredient or a food. However, depending on the oligosaccharide or polysaccharide nature, its solubility as well as its physiological effect varies. The part of polysaccharides that leach out of cell walls upon plant “broyage” and water solubilization are often referred to as soluble fibers. These fibers contribute to increase the viscosity in the gut while insoluble fibers go through the first part of the gastrointestinal tract, reach the colon, and contribute to the bulk of feces, reducing its transit time. From these definitions it is clear that when consumed as food, an important part of algae can be considered as fiber. The content of total dietary fibers ranges from 33 to 50 g/100 g of algae (dry weight) (Lahaye, 1991; Ruperez and Saura-Calixto, 2001). High values reaching more than 60% dry weight were reported in Hizikia fusiforme whereas Laminaria ssp. had the lowest content of fiber (36%) (Dawczynski et al., 2007).

2.4  FOOD-GRADE POLYSACCHARIDES 2.4.1 Agar 2.4.1.1 Source Agar is extracted from red algae and has been used since the seventeenth century in Japan (Armisen, 1995). Gelidium and Gracilaria genera are the most exploited sources of algae for the extraction of agar (McHugh, 2003). These seaweeds are widespread around the coasts of Chile, India, Japan, Madagascar, Mexico, Morocco, Senegal, Spain, Philippines, Portugal, and southern the United States (McHugh, 1991). The cell wall of Gelidium holds 20–30% of agar (Freilepelegrin et al., 1995) and 15–20% in Gracilaria (Santelices and Doty, 1989). These amounts are influenced by the season, species, and growth conditions (Lahaye and Rochas, 1991; Santelices and Doty, 1989). Other genera such as Pterocladia (Portugal and New Zealand) and Gelidiella (Egypt, Madagascar, and India) are also used as sources of agar (Armisen and Galatas, 1987).

2.4.1.2 Structure Agar is made up of calcium, magnesium, potassium, and sodium sulfate esters of d- and l-galactose units, linked by alternating a-(1,3)-d-galactose and b-(1,4)-lgalactose units (Figure 7.5) (Lahaye and Rochas, 1991; Murano, 1995; Stanley, 2006). A large amount of (3,6)-anhydrogalactoses rings are also found, which dictates the gelation process. Agar is a heterogeneous polysaccharide, and additional residues may be present on the structure. Small amounts of sulfate groups (<4.5%) are found at position six of the b-(1,4)-galactose and sometimes in positions four and six of the a-(1,3)-galactose unit (Imeson, 2009a; Murano, 1995). Methyl groups, pyruvate, b-d-xylopyranose, and 4-o-Me-a-l-galactopyranose may also be present

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CHAPTER 7  Seaweed carbohydrates

FIGURE 7.5  Agar Structural Heterogeneity Adapted from Lahaye and Rochas (1991); Usov (2011).

(Lahaye and Rochas, 1991). The number of sulfate groups and methyl pyruvate is higher in Gracilaria than Gelidium, which could affect the gelling properties (Murano, 1995). The molecular weight of the laboratory extract of agar varies between 340 and 380 kDa (Murano, 1995), whereas commercial agar varies between 36 and 144 kDa (Lahaye and Rochas, 1991). High molecular weight agar is desirable to realize stronger gels. Unlike carrageenans, agar is much more resistant to hydrolysis under acidic conditions, because it contains significantly fewer sulfate groups (Stanley, 2006) (Figure 7.6). Agar may be divided into two subgroups: agarose and agaropectin (Araki, 1937). Agarose is a neutral and linear polysaccharide while agaropectin is an acid polymer carrying sulfate, methyl, and methyl pyruvate groups (Imeson, 2009a; Lahaye and Rochas, 1991; Marinho-Soriano and Bourret, 2005). Their individual molecular weights are 120 kDa for agarose (Armisen and Galatas, 1987) and 12.6 Da for agaropectin (Imeson, 2009a). Agar is soluble in hot water (>85°C) and after cooling there is formation of a thermoreversible gel (Stanley, 2006). The viscosity of agar solutions is less than that of the carrageenans due to the presence of weak charged groups such as sulfates.

2.4.1.3  Extraction method Algae are first washed to remove sand and salt; thereafter, Gelidium may be pretreated with a diluted acid solution to improve agar extraction (Imeson, 2009a), while Gracilaria is submitted to an alkali pretreatment after washing (Figure 7.6). This pretreatment is used to modify the structure of agar by increasing the amount of the (3,6)-anhydrogalactose ring for better gelling properties (Armisen, 1995). Then, the seaweed is further washed, and the neutralized solution is subjected to an extraction under pressure with hot water as for Gelidium, followed by hot filtration to remove residual algae fragments (McHugh, 2003). The filtrate is then cooled to form a gel and subsequently frozen; the ice crystals that break the gel while thawing release water, which concentrates agar (McHugh, 2003). The agar is then dried and milled. Since freezing is a costly step, the release of water may be induced by syneresis

2 Types of carbohydrates

FIGURE 7.6  Manufacturing Steps of Agar Adapted from Imeson (2009b).

by applying pressure on the gel, which is then dried and milled (80–100 mesh or 100–150 mm) (Imeson, 2009a). Agar obtained by syneresis contains fewer impurities than freeze-thaw agar (Armisen, 1995).

2.4.1.4  Food utilization Agar is used in many food processes because of its gelling and stabilizing properties. Agar may form a gel at low concentrations, typically between 0.5% and 2% in food product and over a wide range of pH. It is soluble in hot water and, while cooling (between 32°C and 43°C) it forms a gel, which has the ability to remain stable up to

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a temperature of 85°C. The gelling mechanism is different from that of carrageenan, since it only involves hydrogen bonds, whereas for carrageenan, hydrogen bonds and cations are both required (Armisen, 1995). As for carrageenan, agar forms double helices that aggregate to form a gel, holding water within the openings, when a hot solution-containing agar is cooled (Imeson, 2009a; Menon, 2011). Studies show that the kinetics of gel formation may be influenced by the rate of decrease in temperature (Boral et al., 2008; Wang et al., 2013). Gel strength is influenced by the number of 3,6-anhydrogalactose rings: the higher it is the stronger the gel is. Unlike those of other polysaccharides, agar gels are odorless and tasteless, because they do not require the addition of potassium or calcium salt to gel. This feature allows the addition of agar in a wide range of products. Gel syneresis may be controlled by agar concentration, holding time, apparent gel strength, rigidity coefficient, pressurization, and total sulfate contents (Stanley, 2006). While being masticated, syneresis occurs for agar-gelled food products, resulting in in-mouth juiciness (Nussinovitch and Hirashima, 2013a). Agar is used as a stabilizer and gelling agent in bakery products, water gels, confectionery, dairy products, canned meat and fish products, soups and sauces, and beverages (Imeson, 2009a). It is also used in pie fillings, icings, and meringue (McHugh, 2003). Agar may be used in candy in combination with large amounts of sugar to increase the gel strength (Menon, 2011). Agar is used in the broth of canned meat and fish products. The high melting point and resistance of agar to autoclaving make it more appropriate than carrageenan for this application. The gel has two purposes: (i) to protect products during shipping and (ii) to prevent compounds found in certain fish from attacking the lining of the can, which would blacken the content (Stanley, 2006). Agar is also used as a stabilizer in ice cream and sorbets. It improves the texture of cheese and cream cheese. In the beverage industry, agar serves as a flocculating and clarifying agent in the preparation of juices and wines (Stanley, 2006). Further, agar extracted from Gelidium only can be used in synergy with locust bean gum to form transparent gels that are firmer and with less syneresis, offering better mouth feel than agar alone (Armisen and Galatas, 1987). Agar is still used in traditional Japanese food confectionery; “yokan” (agar jelly with red bean paste), “mitsumame” (canned fruit salad with agar jelly), and “tokoroten” (noodle-like agar gel) are good examples (Nussinovitch and Hirashima, 2013a; Stanley, 2006).

2.4.2 Alginate 2.4.2.1 Source Alginate is found in the intercellular matrix of brown algae (Moe et al., 1995), specifically in the cell wall. It gives flexibility to algae, prevents desiccation, and is involved in the exchange of ions (calcium and magnesium) with seawater (Kloareg and Quatrano, 1988). Alginate is found in significant amounts in brown algae, consisting of 18–40% of the biomass on a dry basis (Moe et al., 1995; Whistler and Be Miller, 1997). Several algae species are cultivated to produce the alginate required for the industry: Ascophyllum nodosum, Durvillaea antarctica, Durvillaea potatorum, Laminaria digitata, Laminaria hyperborea, Laminaria saccharina, Laminaria

2 Types of carbohydrates

FIGURE 7.7  Alginate Structure Adapted from Moe et al. (1995).

japonica, Ecklonia maxima, Macrocystis pyrifera, Lessonia nigrescens, and Lessonia trabeculata are among the most widespread (Helgerud et al., 2009; McHugh, 2003). The Ecklonia ssp. is collected in South Africa, Australia, and New Zealand while the Lessonia ssp. is located in Chile (Helgerud et al., 2009). In North America, Ascophyllum nodosum, Laminaria, and Macrocystis ssp. are mostly collected for alginate manufacturing (Helgerud et al., 2009; Nussinovitch and Hirashima, 2013b). The Laminaria ssp. is also located in Northern Europe and Japan (Helgerud et al., 2009).

2.4.2.2 Structure Alginate is a sodium, calcium, or magnesium derivative of alginic acid (COOH vs. COONa for sodium alginate). Alginate is the linear polysaccharide composed of b-d-mannuronic acid (M) and a-l-guluronic acid (G) bound with b-(1,4) (or a-(1,4) in the case of GG block) (Figure 7.7). The ratio of mannuronic and guluronic acid is generally 1:1, but these proportions may change, depending on the age and species of algae as well as the season and harvest location (Graham and Wilcox, 2000). For example, Moe et al. (1995) reported an M:G ratio of 2:1 for A. nodosum. Alginate’s structure varies according to the arrangement of the monomers on the chains. When two monomers form MM or GG type blocks, they are called homogeneous segments, while MG or GM blocks are called mixed segments (Figure 7.7). According to the arrangement of the segments, the position of the glycosidic bond is called diequatorial (MM), diaxial (GG), equatorial-axial (MG), or axial-equatorial (GM). Guluronic acid has a great importance in the mechanism of gelation of alginates (see Section 2.4.2.4). It determines the gel strength; a high number of GG segments lead to a firm and rigid gel (Draget et al., 1997). Guluronic acid molecules have a helical structure characterized by two symmetrical axes (Figure 7.7) (Mackie et al., 1983). This structure is found when guluronic groups are present in the ionized form (–COO), allowing hydrogen bonds between GG units. Moreover, the chain conformation 1C4, carbons 1 and 4, are respectively located above and below the average plane of the molecule, implying that the position of the glycosidic bond between two guluronic acids is diaxial. This causes the polymer chain to adopt a “folded” structure (Mackie et al., 1983). This GG conformation prevents rotation around the glycosidic bond, favoring a firm structure (Moe et al., 1995). The electronegative cavities formed by two consecutive guluronic acid molecules can house cations. These cations act as a junction zone between adjacent chains throughout electrostatic

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interactions, allowing interchain interaction. The gelling mechanism of alginate has been described by the egg-box model (Braccini and Perez, 2001). The MM block does not have hydrogen bonding or a similar cavity to house divalent cations (Figure 7.7). MM chains are similar to a flat ribbon, while MG or GM chains change the direction of the chains (Chourpa et al., 1999). The structure of mixed segments suggests the presence of cavities that can serve as binding sites for cations. Furthermore, these sites show much greater selectivity for divalent ions than MM blocks (Draget et al., 2000), which modifies the properties of alginate gels. Alginates have different solubilities; some are soluble in hot water and others in cold water. Alginic acid is insoluble and gels in the acidic condition or in the presence of an ion such as calcium. Being a polyelectrolyte, alginate’s solubility depends on pH, polymer concentration, and ions present in the medium (Lahaye and Kaeffer, 1997; Moe et al., 1995). Additionally, the algal species from which alginate originates may affect its solubility. Alginate from A. nodosum contains more mixed sequences (MG/ GM) than that extracted from the Laminaria ssp., which contains more homogeneous segments, promoting precipitation and reducing its ability to gel via the formation of crystalline areas stabilized by hydrogen bonds (Moe et al., 1995). Also, the molecular weight of alginate varies considerably, from 150 to 1700 kDa, depending on the source and extraction method (Moe et al., 1995). Its degree of polymerization (the number of monosaccharide units) ranges between 80 and 1000 (Whistler and BeMiller, 1997). At acid pH below the carboxylic groups’ pKa of 3.5, alginate is partly protonated and loses its negative charge, resulting in a low affinity for divalent ions and positively charged proteins. Due to the presence of esterified carboxylic groups, propylene glycol alginate (PGA) is more tolerant to acidic conditions (Helgerud et al., 2009).

2.4.2.3  Extraction method Different commercial types of alginates may be prepared, the most common form being sodium alginate. It is prepared from ground algae stirred with a hot solution of sodium carbonate (Figure 7.8). After 2 h, the soluble alginate is in the form of sodium alginate, and it is then isolated to remove seaweed residues and cellulose. Subsequently, two methods can be used to purify alginate: transformation in alginic acid or calcium alginate (McHugh, 2003). Transformation in alginic acid consists of precipitating the alginates in the presence of hydrochloric acid to form a gel, which can easily be separated from the medium by flotation, centrifugation, and screw press. Then, the gel is mixed with ethanol (or isopropanol) to give a 50:50 water–ethanol mixture. Sodium carbonate is added gradually to form a paste of sodium alginate, which is extruded, dried, and milled. The conversion in calcium alginate is obtained in the presence of calcium chloride, which allows it to form fibers. This fibrous material is easily isolated on a sieve and then washed to remove the excess calcium. These fibers are then mixed with hydrochloric acid to form alginic acid, having the same texture as fibrous calcium alginate. Sodium carbonate is added to the mixture to form a paste of sodium alginate, which is extruded, dried, and milled. Although this method appears to be longer, it avoids the use of ethanol, which is an expensive solvent.

2 Types of carbohydrates

FIGURE 7.8  Manufacturing Steps of Sodium Alginate Adapted from McHugh (2003).

Other types of alginate may be prepared by replacing sodium carbonate with potassium carbonate (potassium alginate), ammonium carbonate (ammonium alginate), calcium carbonate (calcium alginate), or propylene oxide (propylene glycol alginate) (Helgerud et al., 2009). These have different gelling properties, pH stability, etc.

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2.4.2.4  Food utilization Alginate is regularly used by the food industry in the manufacture of several types of foods. Alginate may be used as a stabilizing, emulsifying, gelling, and thickening agent. The viscosity of a solution containing alginate may be modulated by the addition of calcium. Alginate is a thickener, especially in ice creams, ready-to-eat soups, ketchup, mayonnaise, margarine, Alfredo sauces, caramels, granola bars, dehydrated soups, and purées (Moe et al., 1995; Whistler and BeMiller, 1997). In canned meat meals, alginate is used to facilitate heat exchange during sterilization (Helgerud et al., 2009). Slow soluble calcium salt is used in combination with sodium alginate to delay the gel formation during the heat treatment. The heat exchange is thus faster in the presence of low viscosity sauce in comparison to pregelled products, allowing shorter heat cycles. Alginate may also be used as a stabilizer or emulsifier, for example, to maintain in suspension insoluble particles found in juices, oil-in-water emulsions, etc. (Whistler and BeMiller, 1997). It is also found in frozen meals, desserts, and cake icings (Moe et al., 1995). In ice cream, the sizes of ice crystals are reduced when alginate is added. Also, the ice cream texture is smoother, syneresis is prevented, and meltdown is delayed (Helgerud et al., 2009). In acidic food products and beverages, PGA may be used as a stabilizer. Below pH 3.5, part of the carboxylic acid groups are not protonated for PGA since those are esterified, preventing its precipitation. The remaining carboxylic acid groups can retain some negative charge at pH 2.75, allowing weak interactions with divalent ions and proteins containing a positive charge. Drinking yogurt and beverages containing pulp are stabilized by the addition of PGA (Helgerud et al., 2009). Alginate is capable of gelling in the presence of divalent ions such as calcium or magnesium. Gel formation is influenced by several factors such as ionic strength, pH, divalent ion concentration, molecular weight, and the concentration and distribution of guluronic acid chains. Alginate gels according to a mechanism involving a multilayer junction zone (Thibault and Colonna, 1986), which implicates polyguluronic groups (Grant et al., 1973; Larsen et al., 2003). Homogeneous chains come closer to form a gel supported by the addition of divalent cations such as calcium. The ions join the chains to form an egg-box structure with the assistance of electrostatic bonds, chelation, and hydrogen bonding with surrounding water molecules (water bridging) (Braccini and Perez, 2001; Plazinski, 2011; Stewart et al., 2014). An MM or MG/GM sequence interrupts the organized areas composed of GG blocks (Thibault and Colonna, 1986). Mannuronic acid also has the ability to capture calcium ion but only when neighboring a guluronic acid segment (mixed sequence) (Barbotin and Nava Saucedo, 1998). The nature and strength of the gel depend on the proportion of homogeneous and mixed sequences in addition to the M:G ratio. In general, a gel rich in mannuronic acid is soft and elastic due to the formation of multilayer junction zones, ensuring the cohesion of the network. Gel rich in guluronic acid is strong but brittle, since MM junction zones are longer (Thibault and Colonna, 1986). Thus, different functionalities may be obtained, resulting in many food product usages.

2 Types of carbohydrates

Sodium alginate is used in many foods for its gelling character. It is found especially in jams, puddings, and mashed potatoes. Furthermore, it can be used to restructure food. For example, the chili found inside green olives is made with sodium alginate (Whistler and BeMiller, 1997). Onion rings may also be restructured with onion powder and sodium alginate (Helgerud et al., 2009). Restructured food products usually pass into a calcium chloride bath, where calcium ions diffuse inside to form a gel until the desired consistency is obtained. Alginates have good film-forming properties and are useful in several food applications to reduce water loss, control diffusion, and manage the shape of a food product (Helgerud et al., 2009). They can be used in pastries to prevent fruit fillings from moistening the cake or to avoid the adhesion of cake icing to the packaging. Also, films/casings for breakfast pork sausages are formed from gelatin/sodium alginate blends using extrusion technology (Liu et al., 2007). Others containing alginate and 1% protein (soy, gelatin, or whey) have also been developed (Harper et al., 2013). Edible coatings made of alginate were also developed to extend shelf life, to maintain the appearance of the product (reduce browning), and to decrease the respiration rate and ethylene production of fresh-cut fruits (Díaz-Mula et al., 2012; Maftoonazad et al., 2008; Olivas et al., 2007; Rojas-Graü et al., 2007). Alginate edible coatings sometimes contain essential oils or seed extracts that control postharvest decay, browning, water and firmness losses, and fungal activity to prevent food spoiling (Aloui et al., 2014; RoblesSánchez et al., 2013; Sipahi et al., 2013). Fast-dissolving alginate films under the form of breath strips offer many possibilities for the delivery of pharmaceutical ingredients and vitamins. When placed in the mouth, these films dissolve within 1 min, which makes them attractive for local action or rapid release products. Alginate films are brittle when dry but may be plasticized by the inclusion of glycerol, which reduces the hydrogen bonds between neighboring chains (Dea et al., 2011). Finally, alginate is a suitable encapsulating agent for drugs, proteins, probiotics, and many other products (Gray and Dowsett, 1988; Lupo et al., 2014; Sathyabama et al., 2014; Shinde et al., 2014). It can serve as a matrix to protect sensitive bioactives during gastric digestion so that they can reach their active sites without deterioration (Sathyabama et al., 2014). Commonly used encapsulation techniques for alginate are extrusion, emulsification, and coating (Reis et al., 2006). Many scientific papers have been published on this topic and readers are referred to relevant review papers for more information (Cook et al., 2012; Drury and Mooney, 2003; George and Abraham, 2006; Gombotz and Wee, 1998).

2.4.3 Carrageenan 2.4.3.1 Source Carrageenans are extracted from red algae of the Rhodophyceae class. In the 1960s, the seaweed Chondrus crispus was the most important source of carrageenan, and it is currently found around the coasts of the North Atlantic. This species has been replaced by Kappaphycus alvarezii and Eucheuma denticulatum, formerly known as Eucheuma spinosum and Eucheuma cottonii, respectively (Bixler and Johndro, 2000; McHugh, 2003). These algae are widely distributed on the coasts

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of the Philippines, Indonesia, and other islands in the Far East (Imeson, 2009b). Other genera such as Ahnfeltia, Anatheca, Furcellaria, Gigartina, Gynmogongrus, Hypnea, Iridaea, Meristotheca, and Phyllophora are also used as a source of carrageenan (FAO, 2007a). Gigartina ssp. is collected in South America in the cold, deep coastal waters of Chile and Peru while Furcellaria ssp. are distributed in Northern Europe and Asia (Imeson, 2009b). Furcellaria lumbricalis is today a source of furcellaran (Nussinovitch and Hirashima, 2014), a polysaccharide structurally related to carrageenan. This polymer is an approved food additive under the same category “carrageenan” for the European Union and the United States (Blakemore and Harpell, 2009). Carrageenans represent between 30% and 80% of the cell wall constituents of algae (Whistler and BeMiller, 1997). These concentrations are influenced by season, species, and growth conditions of algae. Furthermore, depending on the species used, carrageenans do not have the same structure.

2.4.3.2  Structure and physical properties Carrageenan is made up of ammonium, calcium, magnesium, potassium, and sodium sulfate esters of d-galactose and (3,6)-anhydro-d-galactose units linked by a-(1,3) and b-(1,4) (FAO, 2007a; Whistler and BeMiller, 1997). One or two sulfate groups are found on the galactose unit in positions two and/or six. The main structures of carrageenan are in the form of kappa (k), iota (ι), and lambda (l) (Table 7.4). Other structures, mu- and nu-carrageenans, are precursors of k- and ι-carrageenans after alkali modification during the extraction (Imeson, 2009b). Kappa-carrageenan is composed of alternating d-galactose-4-sulfate and (3,6)-anhydro-d-galactose units. Iota-carrageenan only differs from k-carrageenan by the addition of sulfate groups in position two on the (3,6)-anhydro-d-galactose units. At the opposite, l-carrageenan has no (3,6)-anhydro-d-galactose units but alternating units of (1,3)-d-galactose2-sulfate and (1,4)-d-galactose-2,6-disulfate. Carrageenans differ by the number of sulfate groups and (3,6)-anhydro-d-galactose rings (Table 7.4), and these structural variations influence hydration properties, strength, texture, and temperature of gel formation and gel syneresis (Imeson, 2000). For example, l-carrageenan has a significant amount of sulfate group but contains little or no (3,6)-anydro-d-galactose ring, which hinders gelation of this type of carrageenan. Furcellaran is structurally related to k-carrageenan. It contains between 16% and 20% of sulfate groups (Imeson, 2009b), 3,6-anhydro-d-galactose (30%), and galactose residues partly sulfated in positions four and six (Tuvikene et al., 2010). The molecular weight of the water-extracted furcellaran is 290 kDa (Tuvikene et al., 2010). This polymer is structurally related to carrageenan and according to the FAO, falls under the carrageenan group (Section 2.4.3.1). The different forms of carrageenan are algae dependent. C. crispus primarily contains a mixture of k- and l-carrageenans not within the same alga but in individual plants (sporophytic or gametophytic plants) (McCandless et al., 1973). K. alvarezii and E. denticulatum predominantly contain k-carrageenan and ι-carrageenan, respectively (McHugh, 2003). Gigartina and Furcellaria both contain k- and

Table 7.4  The Structure and Physicochemical Properties of Carrageenans ι-

κ-

λ-

32 30

25 34

35 n/a

>70 40–70 50–80 4–10 Ca2+

>70 30–60 40–75 4–10 K+ and Ca2+

Cold n/a n/a 4–10 No

Structure

Adapted from Prajapati et al. (2014).

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Sulfate groups (%) 3,6-anydrogalactose ring (%) Solubility (˚C) Gelling (˚C) Melting (˚C) pH stability Cation added to gel

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l-carrageenans (Imeson, 2009b). Therefore, the algae species is important since each contains carrageenan forms in various amounts, though the resulting mixture has different functional properties. Food-grade carrageenans are heterogeneous polymers of high molecular weight ranging from 200 kDa to 800 kDa (Blakemore and Harpell, 2009). Processed Eucheuma carrageenan is slightly higher with a molecular weight of 615 kDa (Hoffmann et al., 1996). Fractions of lower molecular weight (10–20 kDa) polygeenan or acid-degraded carrageenan should not be mistaken with carrageenan. Those fractions are used for medical treatments (Blakemore and Harpell, 2009) and were reported to induce adverse effect in animals when mixed in drinking water. Several derivatives of carrageenan as carrageenans enriched with sulfate groups can be generated by chemical modification, in some cases to amplify a biological activity, but are not used as food ingredients. A food-grade carrageenans solution (1.5%) must not be lower than 5 cps at 75°C (FAO, 2007a), which corresponds to a molecular weight of 100 kDa (Imeson, 2009b). All carrageenans are soluble in hot water. However, l-carrageenan and sodium salt of k- and ι-carrageenans are soluble in cold water (Whistler and BeMiller, 1997). Lambda-carrageenan does not gel, but it increases the viscosity of the solutions. Kappa- and ι-carrageenans form gels upon cooling, according to the added cation (calcium or potassium) at low concentrations (0.5%) (Whistler and BeMiller, 1997). Kappa-carrageenan gels are stronger in the presence of potassium than calcium. The gels made with k-carrageenan are stronger but brittle in the presence of calcium and tend to show syneresis (separation of liquid from its gel). Flexible gels with few syneresis are also formed with ι-carrageenan in the presence of calcium (Whistler and BeMiller, 1997). In an acid medium (pH < 4.3), solutions of carrageenan have a lower viscosity and gels are weaker (Imeson, 2000) due to hydrolysis of 3,6-anhydrogalactose rings. The hydrolysis is faster at high temperatures and in the presence of a low concentration of cations. Once carrageenans are gelled in the presence of potassium, the interaction between sulfate groups and potassium ions helps to prevent hydrolysis reactions. Consequently, carrageenans have to be added at the last minute in acidic food products in order to limit their degradation.

2.4.3.3  Extraction method Seaweeds are washed and then heated with an alkaline solution for several hours (Figure 7.9). This step removes some sulfate groups and increases the formation of a 3,6-anhydrogalactose ring in order to form a stronger gel (McHugh, 2003). The seaweed residues from the previous step are removed by centrifugation, filtration, or a combination of both. Then, seaweeds are filtered under pressure to obtain a clear solution of carrageenan. The filtrate is then mixed with a potassium chloride solution to form a gel. This gel is frozen and the ice crystals formed during this process break the gel network. Water is then released during thawing, which concentrates the gel. Since freezing is an expensive step, it is possible to initiate the release of water by applying pressure on the gel. Then, the k-carrageenan is dried and milled. For

2 Types of carbohydrates

FIGURE 7.9  Manufacturing Steps of Carrageenan Adapted from Imeson (2009b).

nongelling carrageenans, it is possible to make an alcohol precipitation in order to recover important amounts of carrageenan. Carrageenan is precipitated as a fibrous coagulum and then isolated by centrifugation or sieving. The coagulum is pressed to remove as much liquid as possible and then washed with alcohol to increase dehydration. Subsequently, it is dried and ground (McHugh, 2003). Other carrageenan varieties, called carrageenan PES (processed Eucheuma seaweed), semirefined carrageenan (SRC), alternatively refined carrageenan, alkali-modified flour (AMF), or PNG (Philippines natural grade) are also available (Imeson, 2009b; Whistler and BeMiller, 1997). They exclusively refer to carrageenans prepared from Eucheuma ssp. harvested in the Philippines or Indonesia. Seaweeds are mixed with potassium hydroxide, which limits carrageenan solubilization and pigment release. Only the soluble low molecular weight compounds are released. The residual seaweed is dried and ground. It contains a mixture of carrageenan (k- or ι-carrageenan, according to the species) and cell wall components (Whistler

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Table 7.5  Principal Food Application of Carrageenans in Dairy Products Application

Function

Carrageenan

Flan Cold-prepared custard Pudding and pie filling Ready-to-eat desserts Milkshakes

Gelling, mouth feel Thickening, gelling Reduced starch, lower burn-on Syneresis, mouth feel Suspension, mouth feel, stabilize overrun Stabilize overrun Stabilize overrun and emulsion Suspension and mouth feel Suspension and mouth feel Suspension and mouth feel Stabilize emulsion Improve slicing and grating, control melting Gelling, water binding

Kappa, kappa + iota Kappa, iota, lambda Kappa Iota Lambda

Whipped cream Desserts (mousse) Pasteurized chocolate milk Sterilized chocolate milk Soy beverages Evaporated milk Processed cheese (slice and blocks) Cream cheese

Lambda Kappa Kappa, kappa + lambda Kappa, lambda Kappa + iota Kappa Kappa Kappa + locust bean gum

Adapted from Imeson (2000).

and BeMiller, 1997). Insoluble algal cellulose is limited to 15% and may include salts for specific gelling and thickening properties (FAO, 2007b). Only seaweeds Kappaphycus alvarezii or Eucheuma denticulatum, which contain the k- and ι-carrageenan, are accepted as PES/SRC/PNG (Bixler and Johndro, 2000; FAO, 2007b).

2.4.3.4  Food utilization Carrageenans have several food applications according to their structure, especially as gelling agents, stabilizers, or thickeners (Table 7.5). Kappa- and ι-carrageenans form gels upon cooling to a temperature around 40–60°C, depending on the ions present in the solution (Figure 7.10). The gels are stable at room temperature and thermally reversible (Imeson, 2000) when heating the gel above the gelation temperature, resulting in a carrageenan solution. This gel temperature may again be lowered

FIGURE 7.10  Gelation Mechanism of Carrageenan Adapted from Whistler and BeMiller, (1997).

2 Types of carbohydrates

below the gel point to form a gel. Gelation of k- and ι-carrageenans involves the formation of a double helix when cooling the solution in the presence of cations (calcium or potassium) (Whistler and BeMiller, 1997). The cations help the formation of the helix and junctions zone made up of aggregated chains (Imeson, 2000). Increasing the cations concentration increases the stability and aggregation of the helices, two important factors in the gelling mechanism (Burey et al., 2008). There are two main categories of applications for carrageenan: in water-based or dairy products. In water-based gelled desserts and cake frostings, k-carrageenan forms a strong and brittle gel whose properties can be modified by the addition of ι-carrageenan (Imeson, 2000). The mixture of k- and ι-carrageenan enables the creation of vegetarian products with a texture similar to gelatin but stable at room temperature. Similar gels are made for canned meat and cooked sliced meat. For the latter, carrageenan improves water retention, cutting, texture, and mouth feel (juiciness of the meat). In fruit juices, sodium salts of l- or k-carrageenan are added to give body and mouth feel (Piculell, 1995). For pet foods, a mixture of k- and ι-carrageenan with locust bean gum or pectin reduces lipid separation and improves the gravy texture. Carrageenans are used in dairy products, for example, in puddings, cream desserts, mousses, and flan (Imeson, 2000). A mixture of l- and k-carrageenan is used to obtain a creamy gel. Kappa-carrageenan has the capacity to interact with milk proteins to form complexes with the k-casein. This allows, for example, an increase in the viscosity of chocolate milk in order to maintain the cocoa particles in suspension (Whistler and BeMiller, 1997). The thickening effect of k-carrageenan is 5–10 times greater in milk than in water. Carrageenans are also used in the preparation of ice cream, milkshakes, and creams to prevent whey separation (Imeson, 2000). Carrageenan cannot be used alone in acidic dairy products (e.g., yogurt) because there is an increase in electrostatic interactions between milk proteins and carrageenan at low pH, leading to the formation of unstable aggregates, causing phase separation (Imeson, 2000). However, the addition of locust bean gum in mixtures with carrageenan is highly effective in reducing syneresis and providing a creamy texture to the acidic product (see below the synergistic effects of polysaccharides). (Table 7.5) includes the main uses of carrageenan in dairy products. Carrageenans act synergistically with other polymers to improve the functionality of each individual polymer, both in water and in dairy products. Kappa-carrageenan and locust bean gum act synergistically to form strong and elastic gels with little syneresis when cooled below 50–60°C (Imeson, 2000). The combination of these two polymers, among others, are used to keep particles in suspension such as fruit in yogurt or as gelling agents in precooked meats, canned pet foods, puddings, and pie fillings (Whistler and BeMiller, 1997). Kappa-carrageenan and konjac gum formed even stronger gels than locust bean gum gels. They are used in the production of “surimi” and pet food (Imeson, 2000) to prevent the separation of lipids (Piculell, 1995). Iota-carrageenan and starch interact synergistically to form gels over four times stronger than starch alone (Imeson, 2000). The addition of starch with ι-carrageenan in gelled milk desserts improves the body and texture of the product. The strength

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of the gels can be modulated by changing the concentration of polymers to obtain strong gels similar to crème caramel and softer custard-type gels (Imeson, 2000). PES/PNG are used as food additives, as they are much less expensive than pure polysaccharides. Approximately 90% of PES/PNG are found in meats and dairy products (Bixler and Johndro, 2000). In meat, PES/PNG are used as texturizing agents, and they reduce water release in cooked meat under a vacuum as ham, turkey breast, chicken, roast beef, bacon, and fish (Bixler and Johndro, 2000). The cellulose network found in PES reduces the hydration time during heating and allows for the use of a higher temperature before increasing viscosity (Imeson, 2009b). In dairy products, PES/PNG are mainly used in chocolate milk to keep the cocoa particles in suspension and in ice cream to prevent whey separation (Bixler and Johndro, 2000). AMF are mostly used in pet food or food to be sterilized after production since their microbiological limits are different than PES. AMF are often used in gravies or gelled products in combination with locust bean gum (Imeson, 2009b). Edible coatings made of carrageenan have also been reported (Karbowiak et al., 2007). In combination with an antibrowning agent, carrageenan can extend the shelf life of fresh-cut apples (Lee et al., 2003) and bananas (Sadili Bico et al., 2010). Aroma encapsulation has also been realized with ι-carrageenan films (Fabra et al., 2009; Hambleton et al., 2009).

2.4.4 Others 2.4.4.1 Mannitol d-Mannitol is a six-carbon sugar alcohol widely distributed in bacteria (Wisselink et al., 2002), fungi (Allaway and Jennings, 1970), plants (Stoop et al., 1996), and algae (Black, 1948; Karsten et al., 1992; Richter and Kirst, 1987). In these organisms mannitol has numerous functions, including osmoregulator, scavenger of reactive oxygen species, and reducing agent (Iwamoto and Shiraiwa, 2005). In brown algae, mannitol is a storage carbohydrate (Black, 1948) and can act as an osmoprotectant or local osmolyte (Dittami et al., 2011). It can represent 20–30% of brown seaweed’s dry weight (Reed et al., 1985), depending upon the harvest period and the amount of nutritive salt present in the water (Chapman and Craigie, 1977; Schiener et al., 2015). It is also found in red macroalgae Caloglossa (Karsten et al., 1992) and in microalgae Dixoniella grisea and Rhodella ssp. (Karsten et al., 1999). The biosynthesis of mannitol for red algae is unusual, since floridoside, isofloridoside, and digeneaside (Section 2.5.3.2) are the well-known photosynthesis products (Iwamoto and Shiraiwa, 2005), suggesting that some genetic variations occur between species. Therefore, the presence of specific carbohydrates in certain red algae, such as mannitol in Caloglossa, could be explained by reactivation of formerly silenced genes (Karsten et al., 1999). Mannitol in response to photosynthesis is also present in green microalgae Platymonas subcordiformis (Richter and Kirst, 1987), Tetraselmis, Nannochloris, and Stichococcus (Craigie et al., 1966). Mannitol is extracted from brown seaweed using a hydrochloric acid solution (0.09 N). This mixture is evaporated, dried, and treated with boiling methanol (5 h).

2 Types of carbohydrates

The precipitation is realized at 5°C during 16 h. The precipitate is isolated and dried (Black et al., 1951). Sometimes the extraction with dilute acid is omitted, and the extraction of mannitol is realized with ethanol or methanol (Black et al., 1951; Mian and Percival, 1973). Mannitol is authorized as a food and drug ingredient. However, the mannitol found on the market is mostly produced by the hydrogenation of fructose or sucrose (Jamieson, 2011). Mannitol is quite attractive for several food applications due to its low glycemic and insulinemic indexes (∼0) (Livesey, 2003). In addition, only 25% of ingested mannitol is absorbed by the organism and thereafter completely excreted in the urine. The remaining 75% is fermented by the microbiota. Mannitol is also tooth friendly and low caloric, which allows it to be a good sweetener in regular and sugar-restricted food (Jamieson, 2011; Livesey, 2003). Its physicochemical properties, such as low hygroscopicity and strong inertness, make it an excellent bulking agent in food. For diabetic patients, mannitol is used for the manufacture of sugar-free chocolates and coatings that would subsequently enrobe ice cream, marshmallows, and butter creams (Jamieson, 2011). It is also found in chewing gum in small percentages both in the gum and on the surface to prevent it from sticking to equipment and wrapping (Jamieson, 2011). Mannitol is gaining popularity in pharmaceutical applications due to its physicochemical properties. Its low hygroscopicity, strong inertness, and good compactibility (high stability and low friability tablet) (Ohrem et al., 2014) make it suitable for such applications. Mannitol is used in chewable tablets and granulated powders. In medicine, mannitol is also used in intravenous fluids as a diuretic agent (Soetaert et al., 1999). The accumulation of mannitol and laminaran in seaweed is also regarded as a source of carbon for ethanol production (Adams et al., 2009; Horn et al., 2000).

2.5  NONFOOD GRADE POLYSACCHARIDES 2.5.1  Fucose-containing sulfated polysaccharides/fucoidan 2.5.1.1 Source Fucose-containing sulfated polysaccharides (FCSP), of which fucoidan is the most well known, are structural polysaccharides present in the cell wall of brown algae. FCSP are present in significant quantities (2–10%) (Indegaard and Minsaas, 1991) in algae, which varies depending on the species and environmental conditions of the algae (Percival and McDowell, 1967). These polysaccharides are mostly found in algae from the family of Fucaceae and Laminariaceae that are distributed worldwide. FCSP (fucoidan) is also found in sea cucumbers and sea urchin eggs (Nagaoka et al., 2000; Pereira et al., 1999), but only FCSP extracted from algae will be discussed in this chapter.

2.5.1.2 Structure FCSP is an inclusive term for sulfated polysaccharides containing fucopyranosyl residues such as ascophyllan, fucan, fucoidan, galactofucan, fucogalacturonan,

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sargassan, etc. (Ale and Meyer, 2013). Since their structure varies according to the seaweed species, each polysaccharide will be described individually. Ascophyllans are composed of mannuronic acid chains with branched fucose residues (3-o-d-xylosyl-l-fucose-4-sulfate) (Mabeau and Kloareg, 1987). Ascophyllan is found in A. nodosum, Fucus serratus, and Laminaria digitata (Mabeau and Kloareg, 1987; Medcalf and Larsen, 1977). Glycuronofucogalactans are composed of linear d-galactose chains with l-fucose-3-sulfate branching and occasionally uronic acids (Mabeau and Kloareg, 1987). There are isolated in A. nodosum (Medcalf et al., 1978) and Sargassum linifolium (Mabeau et al., 1990). Sargassan is a polysaccharide mainly found in S. linifolium. The backbone is composed of residues of glucuronic acid, mannose, and galactose, and the side chains are composed of galactose, xylose, and fucose residues that are partially sulfated (Abdel-Fattah et al., 1974; Mabeau et al., 1990). Galactofucan are sulfated polysaccharides containing equal proportions of l-fucose and d-galactose units (Hemmingson et al., 2006; Rocha et al., 2005). A galactofucan from Undaria pinnatifida (family Alariaceae) consists of a backbone dominated by both a 3-linked fucopyranose-2,4-disulfate and 3-linked galactopyranose, together with a small proportion of 6-linked galactopyranose-3-sulfate (Hemmingson et al., 2006). Another galactofucan from U. pinnatifida showed a backbone dominated by 3-linked fucopyranose with 3-, 4-, and 6-linked galactopyranose residues with sulfate position o-2 on the fucose units and at position o-3 or o-6 on the galactose residues (Lee et al., 2004). For Laminariaceae, Saccharina longicruris galactofucan contained 3-linked fucopyranose-4-sulfate and 6-linked galactopyranose-3-sulfate moieties (Rioux et al., 2010). Fucoidan is a heterogeneous polymer composed mainly of l-fucose (more than 50%) with a more or less large proportion of other monosaccharides, but this term is used with confusion in the literature. The term fucan is sometimes used when the polysaccharide is composed of l-fucose with less than 10% other monosaccharides (Berteau and Mulloy, 2003). Galactofucans are sulfated polysaccharides extracted from brown algae containing large amounts (>50%) of d-galactose (Hemmingson et al., 2006; Rocha et al., 2005), and they are regularly included in the fucoidan family (Lee et al., 2004; Li et al., 2006; Ponce et al., 2003; Shevchenko et al., 2007). In this chapter, the term fucoidan will exclusively be used for polysaccharides extracted from brown seaweed with a-l-fucopyranosyl residue backbone. Since this polysaccharide has gained a lot of attention, more information will be provided for this polysaccharide in particular. Several studies have tried to determine the exact structure of fucoidan. Only a few examples of regularities in the structure were found: linkage, branching, position of the sulfate groups, and other sugars appearing to be variable (Figure 7.11). (Ponce et al., 2003). Fucoidan is generally composed of l-fucose, d-uronic acid, d-galactose, d-xylose, and l-fucose sulfate; the proportions of each varies (Rupérez et al., 2002). Furthermore, the presence of d-glucose and d-mannose was also observed in some algae (Duarte et al., 2001). According to the seaweed families, polymer structure changes. For Fucaceaes, which includes A. nodosum, fucoidan is mainly composed of a-l-fucose linked in a-(1.3) and a-(1.4) (Chevolot et al., 1999, 2001; Daniel

2 Types of carbohydrates

FIGURE 7.11  Possible FCSP Structure from Ascophyllum nodosum (a) and Laminaria japonica (b) Adapted from Ale and Meyer (2013); Chevolot et al. (1999); Fedorov et al. (2013); Wang et al. (2010).

et al., 1999, 2001, 2007; Marais and Joseleau, 2001). The side chains are composed of one or more fucose units branched in position four. Daniel et al. (2001) demonstrated the presence of sulfate groups in position two and possibly in positions three and four on the monomeric unit. In addition, the presence of l-fucose mono and disulfated in position two has been identified (Daniel et al., 2007). For the Fucaceaes species Fucus vesiculosus, two structural models were presented. Briefly, Percival and McDowell (1967) found that fucoidan had two possible structures. The first consists of fucose units linked in a-(1,2) with sulfate groups in position four. The second includes the same elements as the first but with the possibility of finding a-(1.3) linkage between fucose units. Patankar et al. (1993) have suggested that fucose units are rather linked by a-(1,3) for a mixture of commercial fucoidan extract from F. vesiculosus. In opposition, fucoidan from Fucus evanescens and Fucus serratus showed a-(1,3)- and a-(1,4)-l-fucopyranosyl residues substituted or not in positions two and four (Bilan et al., 2002, 2006; Cumashi et al., 2007). For Laminariaceaes, only a partial structure was determined for some species such as Chorda filum, Ecklonia kurome, and Laminaria brasiliensis. These species have a different structure from that of Fucaceaes (Sakai et al., 2004). Fucose units linked in a-(1,2) have been identified in L. brasiliensis with branched sulfated fucose units (Pereira et al., 1999). The presence of fucose linked in a-(1,3) with a-(1,2) branching was also identified for C. filum (Chizhov et al., 1999). The molecular weight of fucoidan has not yet been established because of structural variations. The extraction protocol and the studied alga influence the molecular weight determination. Also, it is regularly considered to be a mixture, justifying a wide distribution of molecular weights. Some researchers argue that the average

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molecular weight is about 100 kDa (Patankar et al., 1993) while others have isolated fractions of low molecular weight (6800 Da) (Nishino et al., 1994). According to Rupérez et al., 2002, the average molecular weight of fucoidan is 1600 kDa with smaller fractions of 43 kDa. Some studies have shown that the use of low molecular weight fucoidan allowed, in some cases, an amplification of the biological activity of the polymer. Fucoidan could be depolymerized with the help of free radicals (Nardella et al., 1996) or by specific enzymes (Daniel et al., 1999, 2001; Descamps et al., 2006; Sakai et al., 2004; Woo-Jung et al., 2008) to reduce its molecular weight (10 kDa or less). It is rather clear that an important structural variation occurs among fucoidan from brown seaweed, which is representative of its natural biodiversity. Even within the same order different compositions and structures are found, preventing any prediction or categorization based on order. This also avoids generalizing a basic structure that would be accurate for all fucoidan sources.

2.5.1.3  Extraction method FCSP can be obtained as a by-product of the extraction of the algal alginate (Section 2.4.2) and laminaran (Section 2.5.2). The type of structure of those polymers will be governed by the extraction method. Reviewed by Ale et al. (2011), Table 7.6 summarizes the extraction methods of FCSP and their chemical composition from different brown seaweed species. FCSP is obtained by hot water extraction (Nishino et al., 1989). Generally, calcium chloride is added to the mixture to prevent the release of the algal alginate. Thereafter, purification steps are performed. Ethanol precipitation or ultrafiltration methods are commonly used for this purpose. Others use a series of successive extractions to isolate FCSP (Mian and Percival, 1973; Ponce et al., 2003), which provides highly purified fractions. However, it can generate lower extraction yields unlike extraction with hot water. Novel techniques have been suggested to effectively improve the extraction process of FCSP (Hahn et al., 2012). For example, microwave, ultrasound, and enzyme-assisted techniques have been used for the extraction of plant molecules. These procedures could reduce the number of purification steps for FCSP and generate new structures.

2.5.1.4  Potential utilization Fucoidan is not used as a food ingredient in Canada or in the United States. However, it is used in Japan as a nutraceutical in beverages and yogurt (Fitton et al., 2008). Several companies offer fucoidan capsules for online purchase. Fucoidan-rich seaweed powder is accepted in the United States as a natural health product, and purified fucoidan is included in several health products in Canada. Fucoidan is not very viscous (Rioux et al., 2007b) as compared to other polysaccharides such as alginate and it does not gel. Once extracted, fucoidan is very soluble in water, even at acidic pH (Rupérez et al., 2002). Functional meats with enriched physicochemical and health-promoting properties have been developed. For example, pig diets supplemented with a laminaran

Table 7.6  Extraction Methods and Chemical Composition of FCSP from Different Brown Seaweed Species Species

Order

Extraction Method

Composition

References

Cladosiphon okamuranus

Chordariales

Fucose, glucose, uronic acid, and sulfate

Nagaoka et al. (1999).

Adenocystis utricularis

Ectocapales

Fucales

Ascophyllum nodosum

Fucales

Fucose, rhamnose, glucose, galactose, xylose, mannose, uronic acid, and sulfate Fucose, xylose, uronic acid, and sulfate Fucose, xylose, glucose, galactose, and sulfate Fucose, xylose, uronic acid, and sulfate

Ponce et al. (2003).

Himanthalia lorea

Seaweed-H2O suspension treated with 30% HCl (pH 3) at 100°C, 15 min. Supernatant was neutralized with NaOH and mixed with CaCl2 and EtOH. Precipitate was hydrated then dried. Pretreated 80% EtOH, 24 h, 70°C and centrifuged. Extracted with water (or 2% CaCl2; or HCl) for 7 h at rt, followed by extraction at 70°C. Acid + alkali or water-acid-alkali sequence at 70°C, 4 h. Extracted at rt and then 70°C with NaCl containing 1% CaCl2. Precipitated in EtOH. Extracted with hot water and dilute alkali, formaldehyde treatment, then extracted with ammonium oxalate-oxalic acid for 6 h at 80°C. Extracted with water 7% (w/v), 12 h, 3×. Precipitated with EtOH and CaCl2 and cetylpyridinium chloride. Soluble fraction fractionated (F1–F6). Extracted with 0.03 M HCl at 90°C for 4 h, precipitated in EtOH.

Fucales

Fucales

Sargassum sp.

Fucales

Sargassum linifolium

Fucales

Fucus evanescens; Fucus distichus

Fucales

Fucose, xylose, glucose, mannose, galactose, uronic acid, and sulfate

Duarte et al. (2001).

Fucose, xylose, glucose, rhamnose, galactose, mannose, uronic acid, and sulfate Xylose, fucose, mannose, galactose, and uronic acid, and sulfate Fucose, xylose, galactose, uronic acid, and sulfate

Ale et al. (2012).

Abdel-Fattah et al. (1974). Bilan et al. (2002, 2004).

169

Extracted with water at pH 1 (HCl), for 3 h at 80°C, neutralized and precipitated with EtOH. Pretreatment MeOH–CHCl3–H2O (4:2:1), extracted 2% CaCl2 for 5 h at 85°C, 5×, precipitated. The precipitate was washed with water, stirred with 20% EtOH solution, and hydrated.

Marais and Joseleau (2001). Percival (1968).

2 Types of carbohydrates

Sargassum stenophyllum

Mian and Percival (1973).

(Continued)

170

Species

Order

Extraction Method

Composition

References

Fucus serratus

Fucales

Fucales

Fucose, galactose, glucose, mannose, xylose, uronic acid, and sulfate Fucose, glucose, xylose, mannose, galactose, rhamnose, arabinose, uronic acid, and sulfate Fucose, xylose, glucose, mannose, galactose, uronic acid, and sulfate

Bilan et al. (2006).

Hizikia fusiforme

Pretreatment MeOH–CHCl3–H2O (4:2:1), extracted 2% CaCl2 for 5 h at 85°C, 5×, centrifuged, combined, dialyzed and lyophilized. Extracted with H2O, 2 h at 70°C, 3×. Precipitated with EtOH and CaCl2 then dried.

Fucose, xylose, glucose, mannose, galactose, uronic acid, and sulfate

Rioux et al. (2010).

Fucose, xylose, mannose, glucose, galactose, uronic acid, and sulfate

Chizhov et al. (1999).

Fucose, xylose, glucose, mannose, rhamnose, galactose, and sulfate Fucose, xylose, glucose, mannose, galactose, uronic acid, and sulfate

Hemmingson et al. (2006).

Laminariales L. saccharina; and Fucales L. digitata; F. vesiculosus; F. spiralis; A. nodosum Saccharina longicruris

Laminariales

Chorda filum

Laminariales

Undaria pinnatifida

Laminariales

Laminaria religiosa

Laminariales

Adapted from Ale et al. (2011).

Extracted with 2% CaCl2 for 5 h at 85°C. Precipitated with Cetavlon, transformation of Cetavlonic salts into calcium salts. Alkaline treatment to remove acetyl groups and to transform fucoidan into sodium salts. Extracted with 1% (w/v) CaCl2 85°C for 4 h then centrifuged. Precipitated with 2% NaCl and EtOH–H2O (95:5, v/v). The precipitate was hydrated, dialyzed, and freeze-dried. Pretreated with CHCl3–MeOH–H2O (2:4:1) and 80% EtOH. Extracted with 2% CaCl2 at 20 and 70°C successively, then with HCl (pH 2) and 3% Na2CO3. Precipitated with calcium salt, dialyzed, and freeze-dried. Extracted 1% H2SO4 at rt, 6 h. Neutralized with 10% NaOH, dialyzed, and lyophilized. Extracted with 0.09 NHCl at 4°C, 2 h. Precipitated with 85% EtOH and dried.

Li et al. (2006).

Cumashi et al. (2007).

Maruyama and Yamamoto (1984).

CHAPTER 7  Seaweed carbohydrates

Table 7.6  Extraction Methods and Chemical Composition of FCSP from Different Brown Seaweed Species  (cont.)

2 Types of carbohydrates

and fucoidan extract from L. digitata enhance the oxidative stability of fresh pork (Moroney et al., 2012). Fucoidan could be a valuable food ingredient for controlling the glycemic index, as in vitro studies revealed an a-amylase and a-glucosidase inhibition (Kim et al., 2014). Also, the antioxidant activity of several fucoidan fractions (Lim et al., 2014) could be valuable for the food industry in order to incorporate more natural ingredients. More work is necessary to convince food authorities that fucoidan and FCSP are valuable for the food industry and safe for consumers. Meanwhile, several seaweed extracts are now available in Canada and the United States as natural health products. Several biological activities were reported for fucoidan. Some authors showed that fucoidan affects the secretion of extracellular matrix proteins (Moon et al., 2008), influences cell proliferation (Haroun-Bouhedja et al., 2000; Koyanagi et al., 2003), and can induce apoptosis (Aisa et al., 2005). Anticoagulant, antitumor, antithrombosis, anti-inflammatory, and antiviral activities are well known for fucoidan (Berteau and Mulloy, 2003; Boisson-Vidal et al., 1995). FCSP and fucoidan bioactivities have been extensively reviewed (Ale et al., 2011; Bedoux et al., 2014; Fedorov et al., 2013; Vo and Kim, 2013; Wijesinghe and Jeon, 2012).

2.5.2 Laminaran 2.5.2.1 Source Laminaran, sometimes called laminarin, is the carbohydrate reserve of marine brown algae. It is found in the plastids of each cell. The amount of laminaran in algae varies from 0% to 18% (Indegaard and Minsaas, 1991); it is preferably present in algae of the order of Laminariaceae. However, laminaran was also isolated in Fucales order seaweed, namely Sargassum fusiforme and Sargassum trichophyllum. Those seaweeds hold very low amounts of laminaran (<1%) (Lee et al., 2011). Its content is influenced by the species and environmental conditions. Indeed, a decrease in nitrite and nitrate in the water stimulates the synthesis of laminaran in the alga (Chapman and Craigie, 1977). Nitrite and nitrate are used by the algae as a source of nitrogen during growth. When the level decreases, the algae cannot grow and thus synthesize laminaran. Laminaran is used as a carbon source by the algae to grow during winter. However, when the levels of nitrite and nitrate are high, the algae cannot stop its growth to synthesize laminaran. Therefore, the alga is no longer able to grow during the winter period (Gagné et al., 1982).

2.5.2.2 Structure Laminaran is part of the beta-glucan family. It is a polymer made of glucose units, and the structure and composition vary, depending on the species (Chizhov et al., 1998). Laminaran is composed of chains of (1,3)-b-d-glucose units (Barry, 1939) with the presence of branching containing (1,6)-b-d-glucosyl (Peat et al., 1958) and (1,2)-b-dglucosyl (Rioux et al., 2010) units. d-Mannitol (M-chain) residues at the end of certain laminaran chains were revealed, while the other ends are composed of d-glucose (G-chain) (Figure 7.12). The ratio of each type of chain depends on the algae species (Chizhov et al., 1998); for example, the commercial source extracted from L. digitata

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FIGURE 7.12  Possible Laminaran Structure with (a) d-Mannitol (M-chain) Residues or (b) d-Glucose (G-chain) Residues at the End of the Chains Adapted from Read et al. (1996).

has a ratio M:G of 3:1 (Read et al., 1996). At the opposite of the b-glucan of plants, laminaran has a low molecular weight (∼5 kDa). Its degree of polymerization is variable but is usually between 20 and 33 units (Chizhov et al., 1998; Kim et al., 2000; Nelson and Lewis, 1974; Read et al., 1996). An unusually high molecular weight laminaran (19–27 kDa) was isolated from Eisenia bicyclis (Men’shova et al., 2013). It was suggested that the location and harvest time of this alga would affect laminaran’s structure when compared to the literature. Laminaran derivatives were also obtained by chemical modification. Sulfated laminaran and oligosaccharides (oligolaminaran) were produced. Both have several biological activities. There are two forms of laminaran: soluble and insoluble. The first is characterized by a complete solubility in cold water, while the second is soluble only in hot water (Black and Dewar, 1973; Rupérez et al., 2002). The solubility of laminaran depends on the number of branches: the higher the number of branching, the higher the solubility in cold water.

2.5.2.3  Extraction method Laminaran can be obtained as a by-product of the extraction of the algal alginate and fucoidan. It is extracted with hot water (Nishino et al., 1989), preferably containing calcium chloride to prevent the solubilization of the algal alginate (Mian and Percival, 1973). Laminaran is extracted together with fucoidan and therefore must be purified. To separate the two polysaccharides, ultrafiltration can be simply performed since the two polymers have very different molecular weights. Laminaran, being a low molecular weight, passes into the filtrate, while fucoidan is found in the retentate. Laminaran must then undergo a step of diafiltration and dialysis with a membrane having a small cutoff (∼1 kDa) to remove salts (calcium chloride) (Rioux et al., 2010).

2 Types of carbohydrates

It is also possible to use an extraction with hot water containing 0.1 M hydrochloric acid (Maeda and Nisizawa, 1968). Thereafter, the solution is stirred with hexadecyltrimethylammonium bromide (cetyltrimethylammonium bromide) to precipitate the acidic polysaccharides (fucoidan and alginate). The supernatant obtained by centrifugation is treated with charcoal to remove traces of impurities and then dialyzed. The laminaran obtained is purified by repeated precipitation with ethanol. Following the extraction with hydrochloric acid, others choose to filtrate the solution on Celite®, dialyze, and precipitate the fraction with ethanol (Jin et al., 2014). Then, laminaran is isolated with anion exchange chromatography.

2.5.2.4  Potential utilization Laminaran is not in use as a food ingredient in Canada or the United States. SigmaAldrich sells a commercial laminaran extract from L. digitata, and Tokyo Chemical Industry Co. Ltd sells a laminaran extract from Eisenia bicyclis, for which both structures vary depending on the lot number. Other companies distribute food supplements containing laminaran often commercialized in combination with alginate and/or fucoidan. Several biological activities are attributed to laminaran. Laminaran has been investigated in terms of a fermentative effect in the gut (Devillé et al., 2004, 2007; Michel et al., 1996, 1999). It is used by the microbial population in the gut, and an important butyrate production has been observed, which could have an important role in the protection against colon cancer (Devillé et al., 2007; Michel et al., 1999). In addition, piglets fed with a laminaran diet showed a significant reduction of enterobacteria without affecting bifidobacteria and lactobacilli populations in the ileum and colon (Sweeney et al., 2012). A weaning pig diet supplemented with laminaran improved gut health and growth performance in these animals (Heim et al., 2014). Additionally, the dietary supplementation of laminaran protects rats against hepatotoxicity induced by lipopolysaccharide by modulating the immune response (Neyrinck et al., 2007). Laminaran may increase the rate of the production of reconstructed dermis and thus could be used in cosmetics to stimulate matrix production (Ayoub et al., 2015). Other activities such as antitumor (Jolles et al., 1963) and antiapoptosis (Kim et al., 2006) were found with native laminaran and oligo-laminaran, while sulfated laminaran derivatives were found to have anticoagulant activity (Ito and Hori, 1989). Meanwhile, several seaweed extracts containing laminaran are now available in Canada and the United States as natural health products.

2.5.3 Others Several other polysaccharides have interesting attributes. They will be briefly presented in the next sections.

2.5.3.1  Floridean starch Floridean starch amylopectin-like glucan is a high molecular weight storage carbohydrate biosynthesized and found in the cytosol of Florideophyceae red algae (Usov, 2011). Seaweed from the Florideophyceae class includes species used for the production of gelling polysaccharides, e.g., Gracilaria ssp. It is considered to be an

173

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FIGURE 7.13  Structure of Floridean Starch Adapted from Usov (2011).

impurity since it has adverse effects on the gel strength of carrageenan and agar (Yu et al., 2002). This polysaccharide is built up of (1,4)-a-d-glucopyranose residues with a small proportion of (1,6)-linkage (Figure 7.13). In addition, (1,3)-linkages were also discovered for Dilsea edulis but were not confirmed in any other seaweed (Barry et al., 1949; Peat et al., 1959). Nonetheless, Floridean starch is structurally related to amylopectin and glycogen with intermediate degrees of branching (similar to maize amylopectin) and an average linear chain length of 18 glucose units (Yu et al., 2002). Floridean starch is obtained with citrate buffer (pH 6.5) and through several differential centrifugation and purification steps (Yu et al., 2002). Floridean starch could be valuable in several food applications such as instant noodles and deep-frozen food due to its low gelatinization and pasting temperatures (Yu et al., 2002). To our knowledge, no pharmaceutical applications have been reported for this polysaccharide.

2.5.3.2  Floridoside, isofloridoside, and digeneaside Floridoside, isofloridoside, and digeneaside are low molecular weight storage carbohydrates that serve as photosynthetic reserves and osmoregulators (Reed, 2010). Their synthesis appears to be highly regulated by the nitrogen content of algal tissue (Macler, 1986). In addition, floridoside can modulate the synthesis of Floridean starch and cell wall polysaccharides (Goulard et al., 2001a, 2001b; Macler, 1988; Simon-Colin et al., 2004). Floridoside is a 2-o-a-d-galactopyranosylglycerol widely distributed in Rhodophyceae (Figure 7.14). d- and l-isofloridosides (1-o-a-dgalactopyranosyl-d-glycerol or 1-o-a-d-galactopyranosyl-l-glycerol) are found in the order of Bangiales such as Porphyra ssp. (Su and Hassid, 1962) while digeneaside, an 2-o-a-d-mannopyranosyl-d-glyceric acid, is found in the order Ceramiales (Figure 7.14) (Kremer, 1978). Floridoside, isofloridoside, and digeneaside are extracted with 12:5:3 MeOH– CHCl3–water for 2 h. The hydroalcoholic phase is concentrated and purified with ion exchange chromatography (Bondu et al., 2007; Claude et al., 2009). Floridoside content represents 1.5–8% on a dry weight basis while the content of digeneaside is 1–2.2% on a dry weight basis (Kirst, 1980). No food applications have been reported for these carbohydrates. However, antioxidant activities (Li et al., 2010), anticomplementary activities (innate immunity)

2 Types of carbohydrates

FIGURE 7.14  Structure of (a) Floridoside, (b) d- and l-Isofloridoside, and (c) Digeneaside Adapted from Usov (2011).

(Courtois et al., 2008), inhibitors of matrix metalloproteinases (Li et al., 2010), substrate for bifidobacteria fermentation, and possibly use as a prebiotic (Muraoka et al., 2008) have been reported.

2.5.3.3 Ulvan Green algae Ulvales (Chlorophyta), namely Ulva and Entermorpha, genera are distributed worldwide. These algae contain a water-soluble polysaccharide, ulvan, which represents about 8–29% of the algae dry weight (Lahaye and Robic, 2007). Ulvan extraction is generally done with hot water (80–90°C) in the presence of a divalent cation chelator (ammonium oxalate) (Abdel-Fattah and Edrees, 1972). Purification is realized by alcohol or quaternary ammonium salt precipitation (Lahaye and Robic, 2007; Shao et al., 2014). As mentioned for other algal polysaccharides, the structure of ulvan is influenced by the extraction method, as reviewed by Alves et al. (2013). Ulvan is a sulfated polysaccharide mainly composed of l-rhamnose, d-xylose, d-glucose, and d-glucuronic acid (Brading et al., 1954). In addition, glucuronic acid and rhamnose are mainly under the form of aldobiuronic acid (4-o-b-d-glucuronosyl-l-rhamnose), and iduronic acid was also discovered (Quemener et al., 1997). Small amounts of sulfate groups are found at position two of the xylose residue while most of them are located in position three of the rhamnose unit (Lahaye et al., 1999;

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FIGURE 7.15  Structure of Ulvan, the Main Ulvanobiuronic Acid Units (a) b-d-Glucuronosyluronic acid-(1,4)-a-l-rhamnose 3-sulfate and (b) a-liduronopyranosic acid-(1,4)-a-l-rhamnose 3-sulfate. Adapted from Jiao et al. (2011).

Lahaye and Robic, 2007). Ulvan is divided in ulvanobiuronic acid A (b-d-glucuronosyluronic acid-(1,4)-a-l-rhamnose 3-sulfate) and B (a-l-iduronopyranosic acid – (1,4)-a-l-rhamnose 3-sulfate) (Figure 7.15) (Lahaye and Ray, 1996; Quemener et al., 1997). Its molecular weight ranges from 150 kDa to 2000 kDa (Paradossi et al., 2002; Siddhanta et al., 2001; Yamamoto, 1980). Interesting rheological properties were attributed to ulvan, allowing it to be considered as a food-grade polysaccharide. An acid extracted ulvan (pH 2, 80°C) exhibited thixotropic behavior characterized by a dense network with interconnected chains, suggesting strong gel formation (Yaich et al., 2014). A semidilute solution of ulvan showed a rod-climbing effect, and cold-set gelation was achieved without the addition of cation (Shao et al., 2014). These results suggest that ulvan could be exploited as a new source of water-soluble gelling polysaccharides. However, the structure of ulvan will strongly influence the rheological properties, e.g., high amounts of uronic acid (∼30%) negatively affect the viscosity of ulvan (Siddhanta et al., 2001). Several bioactivities were reported for ulvan such as an antioxidant activity (Qi et al., 2005) and a potential antihyperlipidemic activity (Pengzhan et al., 2003). In addition, a powder of Ulva lactuca is authorized as a natural heath product in Canada and the United States.

3 CONCLUSIONS Food industries are constantly looking for new functional ingredients. Among the wide range of seaweeds several polysaccharides are found, and each has its own functional properties based on its unique structure. Several bioactivities were

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