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Isolation and Structure of Lycium barbarum Polysaccharides: Comparison
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Please note this is a comparison between Version 2 by Conner Chen and Version 1 by Shuang Song.

Lycium barbarum, also named Goji berry, Gouqizi, and wolfberry, is a perennial shrubbery of Solanaceae that is widely cultivated in China, Japan, Korea, North America, and Europe. Lycium barbarum polysaccharides (LBPs) have attracted increasing attention due to their multiple pharmacological activities and physiological functions. The elucidation of precise structures of LBPs is the prerequisite to unraveling the relationships between structures and functions.

  • Lycium barbarum polysaccharides
  • structural characteristics
  • gut microbiota
  • immunity

1. Introduction

The human gut microbiota is a complex and abundant community composed of up to 1014 microorganisms with about 1150 species [1]. The community is dominated by Firmicutes and Bacteroidetes, which account for more than 80–90%, and then followed by Proteobacteria, Actinobacteria, Verrucomicrobia, Fusobacteria, Cyanobacteria, and Spirochaetes as minor components [2]. The gut microbiota is regarded as a neglected human organ to some extent in the human–microbe superorganism [3]. Furthermore, the dysbiosis of gut microbiota not only affects the host physiological functions (e.g., nutrient digestion, absorption, and metabolism), but triggers diseases (e.g., immune dysregulation responses and metabolic syndrome) [4,5,6][4][5][6]. Therefore, the balance of gut microbiota, including microbial diversity, richness, composition, and functionality, is critical for the health of the host. Numerous studies have demonstrated that several factors, such as genetics, antibiotics, age, and diet, can influence the gut microbiome [6,7][6][7]. Among these factors, a short-term diet can lead to significant microbial changes. More importantly, non-digestible polysaccharides can be degraded and utilized by gut microbiota instead of the host, which encode the carbohydrate active enzymes (CAZymes), such as glycoside hydrolases (GHs), polysaccharide lyases (PLs), glycosyltransferases (GTs) and carbohydrate esterases (CEs), thereby improving beneficial metabolites (e.g., SCFAs) [8,9][8][9].
Lycium barbarum, also named Goji berry, Gouqizi, and wolfberry, is a perennial shrubbery of Solanaceae that is widely cultivated in China, Japan, Korea, North America, and Europe [10]. Currently, China is the largest supplier in the world, and a majority of L. barbarum fruits are distributed in the northwest regions of China, such as Ningxia, Xinjiang, Tibet, Inner Mongolia, Qinghai, and Gansu [11,12][11][12]. Notably, L. barbarum fruits from Ningxia region are the only species included in the Pharmacopoeia of the People’s Republic of China for many years due to their excellent quality [13]. Various bioactive constituents have been isolated and identified from L. barbarum fruits, including polysaccharides, carotenoids, vitamins, flavonoids, alkaloids, anthraquinones, anthocyanins, and organic acids. Among them, the polysaccharides, accounting for 5–8% of dried fruits, have been recognized one of the principal active components [10]. In recent decades, a great deal of research has now confirmed that L. barbarum polysaccharides (LBPs) have various biological functions, such as immunoregulation, anti-inflammation, anti-tumor activities, hypoglycemic/lipidemic activities, and retinal protection [14,15,16,17,18,19][14][15][16][17][18][19]. LBPs mainly include arabinogalactans, acidic heteropolysaccharides, glucans, and other polysaccharides [20,21,22,23,24][20][21][22][23][24]. Increasing evidence suggests that the molecular weight, monosaccharide composition, and glycosidic linkage of LBPs could influence their bioactivities, although the structure–activity relationship of polysaccharides is not yet clear. Therefore, elucidating the structures of LBPs would be beneficial to understand the mechanisms of their health effects and further develop their industrial application. However, many studies have shown that most LBPs are resistant to human digestive enzymes and can almost entirely reach the colon where they are digested and metabolized by gut microbiota, indicating that gut microbiota plays a crucial role in the beneficial effects of LBPs [25,26][25][26]. Currently, although the extraction, purification, structural characterization, and functional activities of LBPs have been summarized and reviewed [27[27][28][29],28,29], few reviews have discussed their structural types and summarized the modulation of LBPs on gut microbiota and the role of gut microbiota in the health effects of LBPs, as well as their potential mechanism based on their structural types.

2. Isolation and Structure of LBPs

The elucidation of precise structures of LBPs is the prerequisite to unraveling the relationships between structures and functions. Numerous studies have demonstrated that the biological activities of LBPs are principally related to their primary and advanced structures [10,28][10][28]. Actually, the current studies mainly focus on the primary structures of LBPs due to the limitations of techniques and analysis. The primary structure characterization of LBPs covers molecular weight, types and ratios of monosaccharides, positions of glycosidic linkages, anomeric carbon configuration, and branched chains, which influence their biological activities to varying degrees [18,24][18][24]. Herein, the research progress on the extraction, purification, and structure of LBPs were summarized below.

2.1. Extraction and Purification

The isolation principle of LBPs is to keep the properties of polysaccharides unaltered during the procedure of extraction and purification. Based on this principle, several extraction methods for crude LBPs have been developed, which include cold or hot water extraction, microwave-assisted extraction, enzyme-assisted extraction, ultrasonic-assisted extraction, and supercritical fluid extraction [10,27][10][27]. Indeed, water extraction is the most commonly used method to obtain crude LBPs due to its convenient operation and high yield [27,30][27][30]. For example, high molecular weight polysaccharides were obtained from dried wolfberries using cold water extraction in a yield of 2–3%, however, the yields of the polysaccharides could be further improved by prolonged high-temperature extraction or enzymatic treatment [30]. Furthermore, it demonstrated that a ratio of water to raw material 31.2, temperature 100 °C, time 5.5 h, and number of extraction 5 were the optimal extraction conditions to obtain LBPs using the Box–Behnken statistical design (predicted yield 23.13%), which was verified by validation experiments (real yield 22.56 ± 1.67%) [31]. Given the excellent solubility of LBPs in water, several scholars have argued that the increased LBPs contain more pectic, cellulose, and hemicellulosic polysaccharides by extended treatments, such as high temperature, enzymatic treatment, and microwave-assisted treatments [31,32][31][32]. Generally, the water-soluble extracts using the above extraction methods contain many impurities, such as inorganic salts, pigments, monosaccharides, oligosaccharides, and proteins, which interfere with the structure determination of LBPs. Therefore, effective measures have to be adopted to further purify the above crude LBPs. Hydrogen peroxide, as a chemical reagent, is widely applied in depigmentation and the Sevag method is frequently applied in deproteinization for their simple procedures [33]. Subsequently, the methods for LBP purification can be performed by membrane separation (e.g., ultrafiltration and microfiltration), column chromatography (e.g., gel filtration chromatography, ion-exchange chromatography, affinity chromatography, and cellulose column chromatography), and chemical precipitation (e.g., fractional precipitation with ethanol) alone or in combination [27,33][27][33]. Of note, column chromatography is most commonly used in these methods [27]. As we prevFiously reported, five arabinogalactan fractions (LBP1~5) from crude LBPs (extracted by water at room temperature) were separated by DEAE-cellulose chromatography [34]. Afterwards, LbGp1 with a molecular weight of 49.1 kDa was isolated and purified from LBP1 by Sepharedax G-100 column chromatography in yields of 0.018% [22]. Similarly, another five fractions (LRP1, LRP2, LRP3, LRP4, and LRP5) were also isolated from crude L. ruthenicum  polysaccharides (extraction by 70 °C water) on DEAE-Cellulose-52 anion-exchange column followed by gradient elution in our  one previous  studies [35]. Subsequently, LRGP1 (Mw 56.2 kDa) and LRGP3 (Mw 75.6 kDa) were further purified on Sephadex G-100 column in yields of 0.003% and 0.008%, respectively [35,36][35][36]. Moreover, LBP3b (Mw 5 kDa) was purified from crude LBPs extracted with hot water (60 °C) using DEAE-cellulose column and Sephadex G-150 column, which was identified as glucan [24]. In addition, a novel arabinogalactan LBP1A1-1 (Mw 45 kDa) was purified from L. barbarum on DEAE Sepharose Fast Flow column and Sephacryl S-200 HR column in yields of 0.1% [37]. These  studies have indicated that the polysaccharide fractions purified by column chromatography are difficult to investigate for the activities in vivo, as well as the structure–function relationship due to low yield and complex operation. Then, we  one group developed fractional precipitation with 30%, 50%, and 70% (V/V) ethanol to purify arabinogalactan in yields of 0.38%, which was simpler and more efficient than column chromatography [17].

2.2. Structure of LBPs

To date, LBPs have been identified as glycoconjugates that mainly consist of five major structural elements: arabinogalactan, pectin polysaccharide, glucan, xylan, and other heteropolysaccharides [21,22,23,24][21][22][23][24]. Their hypothetical structure features, such as monosaccharide composition, repeat unit, and molecular weight, were summarized in Table 1. Additionally, the molecular weight of LBPs is highly subject to the origin, cultivar, and extraction method, ranging from 5 kDa to 2300 kDa [10,24,38][10][24][38].
Table 1.
 Molecular weight, monosaccharide composition, and hypothetic structure of LBPs.
No. Name Mw (kDa) Molar Ratio Possible Structure of Repeat Unit Ref.
1 LBGP70-OL 73 Ara:Gal = 1.0:1.0 Backbone: (1→6)-β-Galp; branches: (1→3)-α-Araf, (1→3)-β-Araf, (1→5)-β-Araf, (1→3)-β-Galp [39]
2 LBP-3 67 Ara:Gal = 1.0:1.6 Backbone: (1→3)-β-Galp; branches: α-(1→3)-Araf, α-(1→4)-Araf, α-(1→5)-Araf and β-(1→6)-Galp [40]
3 LBP-W 113 Ara:Gal:Rha = 55.6:35.5:8.0 Backbone: (1→6)-β-Galp; branches: (1→3)-α-Rhap, (1→3)-β-Galp, (1→3)-α-Araf, (1→5)-α-Araf [41]
4 LBP1A1-1 45 Ara:Gal:Glc:Rha = 47.8:49.8:1.4:1.2 Backbone: (1→3)-β-Galp, (1→6)-β-Galp and (1→4)-β-Glcp; branches: (1→6)-β-Galp on C-3 or (1→3)-β-Galp on C-6. [37]
5 LBP1B-S-2 80 Ara:Gal:Glc:Rha = 53.6:39.4:4.0:3.1 Backbone: (1→3)-β-Galp and (1→6)-β-Galp; branches: (1→4)-β-GlcpA, (1→6)-β-Galp, (1→5)-α-Araf [42]
6 LBLP5-A-OL1 71 Ara:Gal:Rha = 1.0:1.2:0.1 Backbone: (1→3)-linked Galp; branches: (1→6)-linked Galp, (1→3)-linked Galp, (1→3)-linked Araf, (1→4)-linked Araf, (1→5)-linked Araf, and (1→2,4)-linked Rhaf [43]
7 LBPA 470 Ara:Gal:GlcA:Rha = 9.2:6.6:1.0:0.9 Backbone: (1→6)-β-d-Galp; branches: (1→3)-α-Araf, (1→5)-α-Araf, (1→6)-β-GlcpA, (1→4)-α-Rhap [44]
8 LbGp1 49 Ara:Gal = 5.6:1.0 Backbone: (1→ 6)-β-Galp; branches: (1→2)-linked Araf, (1→3)-linked-Araf, (1→3)-linked Galp, and (1→4)-linked Galp [22]
9 LRGP3 76 Ara:Gal:Rha = 14.9:10.4:1.0 Backbone: (1→3)-β-d-Galp; branches: (1→5)-α-Araf, (1→2)-α-Araf, (1→6)-β-Galp, (1→3)-Galp, and (1→2,4)-α-Rhap [36]
10 LRGP1 56 Ara:Gal:Glc:Rha:Man:Xyl =

10.7:10.4:1.0:0.7:0.7:0.3		 Backbone: (1→3)-linked Gal; branches: (1→2)-linked Ara, (1→5)-linked Ara, (1→3)-linked Gal, (1→4)-linked Gal, (1→6)-linked Gal, and (1→2)-linked Rha [35]
11 AGPs ND Gal:Ara:GlcA:Rha:GalA

44.3: 42.9:7.0 3.3:2.4		 Backbone: (1→3)-β-d-Galp; branches: (1→5)-α-Araf, T-α-Araf, T-β-Araf, T-α-Rhap, and T-β-GlcpA [45]
12 WSP1 ND Ara:Gal:Glc:HexA:Xyl:Rha:Man = 51.4:25.9:7.3:7.4:4.8:1.6:1.2: Backbone: (1→3)-Galp; branches: Araf and Galp substituted on O-6 [46]
13 LbGp4 215 Gal:Ara:Rha:Glc =2.5:1.5:0.43:0.23 Backbone: (1→4)-β-Gal; branches: (1→3)-β-Gal with T-α-Ara-(1→ and T-β-Rha-(1→ [47]
14 LbGp2 68 Ara:Gal = 4:5 Backbone: (1→6)-β-Galp; branches: (1→3)-β-Araf and (1→3)-β-Galp with T-α-Araf-(1→ [48]
15 LbGp4-OL 181 Ara:Gal:Rha = 1.3:1.0:0.1 Backbone: (1→4)-linked Galp; branches: (1→3)-β-Galp, (1→3)-α-Rhap, (1→3)-β-Araf, (1→5)-β-Araf [49]
16 LbGp1-OL 40 Ara:Gal = 1:1 Backbone: (1→6)-β-Galp; branches: (1→3)-β-Galp, (1→3)-β-Araf, and T-α-Araf-(1→ [50]
17 LbGp3 93 Ara:Gal = 1:1 Backbone: (1→4)-β-Galp; branches: (1→3)-β-Araf and (1→3)-α-Galp with T-α-Araf-(1→ [51]
18 LBPA3 66 Ara:Gal = 1.2:1.0 Heteropolysaccharide with (1→4), (1→6)-β-linkage. [52]
19 p-LBP 64 GalA:Ara:Gal:Rha:Glc:GlcA:Xyl: Fuc = 137.0:54.8:23.0:6.4:4.1:3.4:3.0: 1.0 Backbone: (1→4)-α-GalpA; branches: (1→2)-α-Rhap on C4 and (1→3)-β-Galp on C-6 [23]
20 WSP2 ND GalA:Ara:Gal:Xyl:Glc:Rha = 76.0:12.3:6.3:1.8:1.5:1.4 (1→4)-GalpA [46]
21 LBP-1 2250 GalA:Ara:Man:Rha:Gal:Xyl =

8.2:7.9:3.0:1.0:0.7:0.4		 Backbone: α-(1→5)-l-Ara and α-(1→4)-d-GalA; branches: →1)-Man-(3→6) and T-Man-(1→ [38]
22 LBP3a-1/2 103/82 GalA α-(1→4)-GalA [53]
23 LBP3b 5 Glc:Man:Rha:Xyl:Gal = 28.1:5.5:5.1:1.7:1.0 β-glucan [24]
24 LBP3p 157 Glc:Man:Xyl:Rha:Ara:Gal = 2.1:2.0:1.8:1.3:1.1:1.0 β-d-Glc linkage [54]
25 LBP1a-1/2 115/94 Glc α-(1→6)-d-glucan [53]
26 LBPC4 10 Glc α-(1→4) (1→6)-glucan [55]
27 LBPC2 12 Xyl:Rha:Man = 8.8:2.3:1.0 Heteropolysaccharide with (1→4) (1→6)-β-linkage [55]
28 CWM-4M KOH ND Xyl:Ara:HexA:Glc:Gal:Man:Rha =

31.9:19.1:18.0:15.1:10.1:4.8:1.8		 (1→4) xylan [46]
29 LBP-IV 420 Glc:Ara:Xyl:Rha:Gal =

7.5:3.8:3.4:1.6:1.0		 Backbone: α/β-Ara/Glc; branches: T-Rha [56]
30 LBP ND Glc:Man:Rha:Gal:Ara:Xyl = 6.5:2.2:0.8:0.2:0.2:0.1 ND [26]
Abbreviations: Gal, galactose; Glc, glucose; Rha, rhamnose; Man, mannose; Ara, arabinose; Xyl, xylose; GalA, galacturonic acid; GlcA, glucuronic acid; HexA, hexuronic acid; ND: not detect. Among the above numbers, No.1–No.18 belong to arabinogalactan; No.19–No.22 belong to pectin type; No.23–No.26 belong to glucan type; No.27–No.28 belong to xylan type; No.29–No.30 belong to other type.

2.2.1. Arabinogalactans

Structural characterization of L. barbarum arabinogalactan-protein has been investigated by multiple research groups, and it has been demonstrated that there are a large number of →3,6)-Galp-(1→ residues based on the methylation analysis. The current controversies about its structure are as follows: (1) L. barbarum arabinogalactan is composed of →6)-β-Galp-(1→ as the backbone, and large amounts of α/β-Araf as branch chains which substituted at C-3 [22,41,48][22][41][48] (Figure 1A); (2) it is a highly branched polysaccharide with a backbone of →3)-β-Galp-(1→ substituted at C-6 with Araf [40,45][40][45] (Figure 1B); (3) the fraction possesses both β-(1→6)-linked Galp and β-(1→3)-linked Galp as the backbones with partial substitution at the C-3 site and C-6 site, respectively [37,42][37][42] (Figure 1C). The backbone structure of arabinogalactan in LBPs may be different due to diverse origin and various isolation methods. As mentioned above, a combination of ion exchange column and gel filtration column chromatography is commonly employed for the purification of arabinogalactan fraction from L. barbarum  glycoconjugates; however, it is not suitable  for large-scale preparation of arabinogalactan due to complex operation, time-consuming processes, and low yield. Recently, our  one research team revisited the structure of L. barbarum arabinogalactan using a set of chemical methods and analytical techniques, including partial acid hydrolysis, methylation analysis, alkaline degradation, monosaccharide composition analysis, 1H and 13C spectroscopy, and ESI-MSn [39] on the basis of the ethanol precipitation method reported [17]. And the results indicated that it was a highly branched polysaccharide with a backbone of →6)-β-Galp-(1→ and branched chains of →3)-β-Glap (1→, →3)-α-Araf-(1→ and →5)-β-Araf-(1→ substituted at the C3 position, which had an average of 9 branches per 10 sugar backbone units. Additionally, the anti-aging activity of L. barbarum arabinogalactan was significantly higher than the backbone fraction (Gal percentage = 91%) obtained by partial acid hydrolysis (0.02 M H2SO4), indicating that the anti-aging activity was closely relevant to the arabinose branched chains. These results implied that the biological activities of LBPs were considerably influenced by their structures, especially branched chains and spatial configuration [39].
Foods 11 03177 g001
Figure 1. The hypothetical structures of LBPs. The representative arabinogalactan with backbone of (1→6)-linked β-Galp [39] (A), (1→3)-linked β-Galp [36] (B), (1→3)(1→6)-linked β-Galp [37] (C), the typical structure of pectin [23] (D), glucan [53] (E) and xylan [46] (F).

2.2.2. Pectins

Pectins, as a cell wall component of plants, are unique polysaccharides comprising predominantly uronic acids, such as glucuronic acid (GlcA) and galacturonic acid (GalA) [57]. The polysaccharides extracted from L. barbarum fruits also contain pectins (Figure 1D). There are mainly three typical structures in pectins: homogalacturonan (HG), rhamnogalacturonan-I (RG-I), and rhamnogalacturonan-II (RG-II) [58,59][58][59]. A typical pectic polysaccharide (p-LBP) with a backbone of →4-α-GalpA-(1→ (HG) and a partial region of →4-α-GalpA-(1→ and →2-α-Rhap-(1 → (RG-I) was isolated and purified using a series of column chromatographies (e.g., macroporous resin S-8, DEAE column and Sephacryl S400 gel permeation) and analytical techniques (e.g., 1H and 13C spectroscopy) [23]. Another acidic polysaccharide (LBP3a) was also separated from the crude extraction by DEAE-cellulose chromatography, which was identified as HG-type pectin with a backbone of →4)-α-D-GalpA(1→ [53]. HG-type pectin was found in the above studies, perhaps due to the same extraction methods (e.g., hot water) and original place. Besides, the polysaccharides from L. barbarum insoluble cell wall material (CWM) dissolved in the CDTA and Na2CO3 solutions contained 76.3% and 51.9% uronic acid, respectively. Notably, the fraction extracted by CWM-Na2CO3 may be RG-type pectin, which was supported by the increased level of rhamnose (Rha) [46]. Additionally, one homogeneous polysaccharide (LBP-1, Mw 2250 kDa) was purified from crude LBPs using DEAE column, whose structure was identified as pectin with a backbone of α-(1→5)-l-Ara and α-(1→4)-d-GalA, and branched chains of →3)-Man-(1→, →6)-Man-(1→, and T-Man-1(→ [38].

2.2.3. Glucans

Glucans widely exist in the cell walls of various plants and fungi, and there is a small amount in L. barbarum fruits, despite the diversity in conformation and linkages [60]. For instance, LBP1a-1 (Mw 115 kDa) and LBP1a-2 (Mw 94 kDa) were obtained from crude LBPs using DEAE-cellulose and Sephacryl S-400 HR column chromatography, which was identified as glucan with a backbone of →6)-α-d-Glcp (1→ [53]. Moreover, a homogenous polysaccharide with a molecular weight of 4.9 kDa was separated from crude LBPs by the DEAE-cellulose column in combination with Sephadex G-150 column and then identified as a β-glucan by monosaccharide composition and 1H/13C NMR analysis [24]. In addition, an α-(1→4) (1→6) glucan (LBPC4) was isolated and purified from crude LBPs using DEAE-cellulose column and Sephadex G-50 column [55].

2.2.4. Xylans

Xylans are the primary hemicellulose component in plant cells, which are mainly found in hardwood (15–30%), softwoods (7–10%), and annual plants (up to 30%) [61]. Additionally, 4 M KOH-soluble fraction isolated from L. barbarum insoluble cell wall material was a xylan instead of xyloglucan, which was supported by the fact that the xylose content was twice that of the glucose [46]. In addition, a β-(1→4) (1→6)-linked heteropolysaccharide (LBPC2) was separated from crude LBPs using DEAE-cellulose column and Sephadex G-50 column [55]. Interestingly, it was composed of only Xyl, Rha, and Man in a molar ratio of 8.8:2.3:1.0, so LBPC2 was supposed to be a xylan, which needs further confirmation.

2.2.5. Other Polysaccharides

Apart from the above four types, the structural elements of LBPs have been identified as other types from their monosaccharide composition in a few studies. For example, LBP-IV, which is mainly composed of Glc, Ara, and Xyl in a molar ratio of 7.54:3.82:3.44, was separated from crude LBPs on the DEAE-Sephadex A-25 column [56]. Another polysaccharide was isolated from crude LBPs with a macroporous resin S-8 column, which primarily comprised Glc, Man, and Rha in molar ratios of 6.52:2.17:0.81 [26]. These results indicate that LBPs contain other heteropolysaccharides in addition to arabinogalactan, pectin, glucan, and xylan; however, the structures need to be further identified and confirmed.

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