肠道微生物降解植物多糖的机制研究进展

doi:10.16431/j.cnki.1671-7236.2023.10.019

摘要/Abstract

摘要： 植物多糖作为广泛存在于自然界中的一类结构复杂的大分子化合物,具有多种生理调节功能。肠道菌群能够代谢宿主自身无法消化的多糖,与宿主之间存在一种互惠共生关系。进入肠道内的多糖是影响肠道菌群生理状态和组成的重要因素,植物中的非淀粉多糖被肠道微生物降解后,能够显著调节肠道菌群的组成结构和肠道健康,不同的肠道共生菌对进入肠道内的多糖具有不同的偏好性,且降解途径复杂多样。作者简述了植物中非淀粉多糖的种类、总结了植物多糖对肠道环境的改善作用,对可降解植物中非淀粉多糖的肠道菌群及其具体降解机制进行综述,并介绍了代表性肠道益生菌中拟杆菌的各类植物多糖降解系统,以便为后续肠道微生物在多糖降解方面的功能研究及新型微生态制剂的开发利用提供理论基础。

关键词: 植物多糖; 肠道微生物; 多糖降解机制

Abstract: Plant polysaccharides,as a group of structurally complex macromolecular compounds widely found in nature,have a variety of physiological regulatory functions.The intestinal microbiota is able to metabolize polysaccharides that the host itself cannot digest and has a reciprocal symbiotic relationship with the host.Polysaccharides entering the gut are important factors influencing the physiological state and composition of the intestinal microbiota,and the degradation of non-starch polysaccharides in plants by intestinal microbiota can significantly modulate the composition and structure of the intestinal microbiota and intestinal health.Different intestinal symbiotic bacteria have different preferences for polysaccharides entering the intestinal tract,and the degradation pathways are complex and diverse.The authors briefly introduce the types of non-starch polysaccharides in plants,summarize the effects of plant polysaccharides on the intestinal environment,review the intestinal microbiota that can degrade non-starch polysaccharides in plants and their specific degradation mechanisms,and introduce the various plant polysaccharide degradation systems of representative intestinal microbiota,with a view to providing a theoretical basis for subsequent functional studies of intestinal microbiota in polysaccharide degradation and the development and utilization of novel microecological agents.

Key words: plant polysaccharides; intestinal microbiota; polysaccharide degradative mechanism

中图分类号:

莫潜渊, 肖德琴, 朱勇文, 杨琳, 王文策. 肠道微生物降解植物多糖的机制研究进展[J]. 中国畜牧兽医, 2023, 50(10): 4058-4069.

MO Qianyuan, XIAO Deqin, ZHU Yongwen, YANG Lin, WANG Wence. Research Progress in the Mechanism of Degradation of Plant Polysaccharides by Intestinal Microorganisms[J]. China Animal Husbandry and Veterinary Medicine, 2023, 50(10): 4058-4069.

参考文献

[1] ZHAO W,LIU W L,LI J J,et al.Preparation of animal polysaccharides nanofibers by electrospinning and their potential biomedical applications[J].Journal of Biomedical Materials Research.Part A,2015,103(2):807-818.
[2] 蔡瑶.基于固态纳米孔技术的多糖单分子结构解析[D].长春:吉林大学,2020. CAI Y.Molecular structure analysis of polysaccharides based on solid-state nanopore technology[D].Changchun:Jilin University,2020.(in Chinese)
[3] 毛欣雨,梁慧,王行,等.植物多糖对动物肠道的保护作用及其分子机制[J].中国畜牧兽医,2022,49(1):150-160. MAO X Y,LIANG H,WANG X,et al.Protective effects of plant polysaccharides on animal intestine and its molecular mechanism[J].China Animal Husbandry & Veterinary Medicine,2022,49(1):150-160.(in Chinese)
[4] WANG W,XUE C,MAO X.Radioprotective effects and mechanisms of animal,plant and microbial polysaccharides[J].International Journal of Biological Macromolecules,2020,153:373-384.
[5] SILVA I,MACHADO F,MORENO M J,et al.Polysaccharide structures and their hypocholesterolemic potential[J].Molecules,2021,26(15):4559.
[6] SYNYTSYA A,NOVAK M.Structural diversity of fungal glucans[J].Carbohydrate Polymers,2013,92(1):792-809.
[7] PERERA N,YANG F L,CHANG C M,et al.Galactomannan from antrodia cinnamomea enhances the phagocytic activity of macrophages[J].Organic Letters,2017,19(13):3486-3489.
[8] GAO G,CAO J,MI L,et al.BdPUL12 depolymerizes beta-mannan-like glycans into mannooligosaccharides and mannose,which serve as carbon sources for Bacteroides dorei and gut probiotics[J].International Journal of Biological Macromolecules,2021,187:664-674.
[9] AKHTAR M,TARIQ A F,AWAIS M M,et al.Studies on wheat bran Arabinoxylan for its immunostimulatory and protective effects against avian coccidiosis[J].Carbohydrate Polymers,2012,90(1):333-339.
[10] ZHANG B,ZHONG Y,DONG D,et al.Gut microbial utilization of xylan and its implication in gut homeostasis and metabolic response[J].Carbohydrate Polymers,2022,286:119271.
[11] 吕友晶.不同来源果胶多糖的结构解析及抗肿瘤活性研究[D].青岛:中国海洋大学,2015. LYU Y J.Structural characterization and anti-tumor properties of pectin prepared from different plants[D].Qingdao:Ocean University of China,2015.(in Chinese)
[12] SUN Q L,LI Y X,CUI Y S,et al.Structural characterization of three polysaccharides from the roots of Codonopsis pilosula and their immunomodulatory effects on RAW264.7 macrophages[J].International Journal of Biological Macromolecules,2019,130(1):556-563.
[13] NDEH D,ROGOWSKI A,CARTMELL A,et al.Complex pectin metabolism by gut bacteria reveals novel catalytic functions[J].Nature,2017,544(7648):65-70.
[14] 唐硕.落叶松阿拉伯半乳聚糖的分离纯化、结构解析、免疫活性及其功能化的研究[D].南京:南京林业大学,2021. TANG S.Isolation,purification,structure characterization,immunological activity and its functionalization of Larch arabinogalactan[D].Nanjing:Nanjing Forestry University,2021.(in Chinese)
[15] 袁娇.基于β-半乳糖苷酶和L-阿拉伯糖异构酶基因工程菌的构建与D-塔格糖的生物合成[D].镇江:江苏大学,2021. YUAN J.Construction of genetic engineering strain using β-galactosidase and L-arabinose isomerase and biosynthesis of D-tagatose[D].Zhenjiang:Jiangsu University,2021.(in Chinese)
[16] ITO K,FUKUOKA K,NISHIGAKI N,et al.Structural features conserved in subclass of type Ⅱ arabinogalactan[J].Plant Biotechnol (Tokyo),2020,37(4):459-463.
[17] 李静.复合植物多糖对肉鸭生产性能、肠道微生物组及代谢组的影响[D].泰安:山东农业大学,2021. LI J.Effects of compound plant-derived polysaccharides on production performance,intestinal microbiome and metabolome of ducks[D].Tai'an:Shandong Agricultural University,2021.(in Chinese)
[18] WANG Q,WANG X F,XING T,et al.The combined impact of xylo-oligosaccharides and gamma-irradiated Astragalus polysaccharides on growth performance and intestinal mucosal barrier function of broilers[J].Poultry Science,2021,100(3):100909.
[19] 王丹,崔卫涛,王纯,等.发酵中药制剂对肉鸡生产性能、免疫功能、肠道形态及盲肠菌群影响的研究[J].湖北农业科学,2021,60(24):164-168. WANG D,CUI W T,WANG C.Study on the application of fermented Chinese medicine preparation to replace antibiotics in broiler diet[J].Hubei Agricultural Sciences,2021,60(24):164-168.(in Chinese)
[20] 梁海阳.怀山药粗多糖对肉仔鸡生产性能、肠道消化酶活性及形态结构的影响[D].新乡:河南科技学院,2021. LIANG H Y.Effect of Chinese yam polysaccharides on digestive enzymes and morphological structure in broilers[D].Xinxiang:Henan Institute of Science and Technology,2021.(in Chinese)
[21] SANG T,GUO C,GUO D,et al.Suppression of obesity and inflammation by polysaccharide from sporoderm-broken spore of Ganoderma lucidum via gut microbiota regulation[J].Carbohydrate Polymers,2021,256:117594.
[22] 代书景,石学魁,佟雷,等.红花多糖对肠道微生态失调小鼠肠黏膜sIgA、血浆内毒素和肠道菌群的影响[J].中国微生态学杂志,2022,34(1):12-17. DAI S J,SHI X K,TONG L,et al.The effect of Carthamus tinctorius polysaccharides on intestinal mucosa slgA,plasma endotoxin and intestinal flora in mice with intestinal microecological disorders[J].Chinese Journal of Microecology,2022,34(1):12-17.(in Chinese)
[23] 周兆海,梁浩钊,陈刚,等.玉屏风多糖脂质体对雏鸡黏膜免疫的影响[J].动物医学进展,2019,40(10):54-59. ZHOU Z H,LIANG H Z,CHEN G,et al.Effect of Yupingfeng polysaccharide liposomes on mucosal immunity of chicks[J].Progress in Veterinary Medicine,2019,40(10):54-59.(in Chinese)
[24] YAN N,WANG L,LI Y,et al.Metformin intervention ameliorates as in apoe-/- mice through restoring gut dysbiosis and anti-inflammation[J].PLoS One,2021,16(7):e254321.
[25] 张金洲,苗志国,赵伟鑫,等.山药多糖对仔猪生长性能与肠道菌群的影响[J].中国饲料,2020,23:57-61. ZHANG J Z,MIAO Z G,ZHAO W X,et al.Effect of yam polysaccharide on growth performance and intestinal microflora of piglets[J].China Feed,2020,23:57-61.(in Chinese)
[26] NIU X,SHANG H,CHEN S,et al.Effects of Pinus massoniana pollen polysaccharides on intestinal microenvironment and colitis in mice[J].Food & Function,2021,12(1):252-266.
[27] SONG B,LI P,YAN S,et al.Effects of dietary astragalus polysaccharide supplementation on the Th17/Treg balance and the gut microbiota of broiler chickens challenged with necrotic enteritis[J].Frontiers in Immunology,2022,13:781934.
[28] LI Y,XIANG D,WANG B,et al.Oil-in-water emulsions stabilized by ultrasonic degraded polysaccharide complex[J].Molecules,2019,24(6):1097.
[29] 曾良欢.一种广谱型多糖降解酶的生化特征、酶学特性与催化机理的研究[D].济南:山东大学,2021. ZENG L H.Studies on biochemical characteristics,enzymatic properties and catalytic mechanism of a multifunctional polysaccharide degrading enzyme[D].Jinan:Shangdong University,2021.(in Chinese)
[30] STERN J,MORAIS S,LAMED R,et al.Adaptor scaffoldins:An original strategy for extended designer cellulosomes,inspired from nature[J].mBio,2016,7(2):e83.
[31] ARTZI L,MORAG E,SHAMSHOUM M,et al.Cellulosomal expansin:Functionality and incorporation into the complex[J].Biotechnol Biofuels,2016,9:61.
[32] PEREIRA G V,ABDEL-HAMID A M,DUTTA S,et al.Degradation of complex arabinoxylans by human colonic Bacteroidetes[J].Nature Communications,2021,12(1):459.
[33] LAPEBIE P,LOMBARD V,DRULA E,et al.Bacteroidetes use thousands of enzyme combinations to break down glycans[J].Nature Communications, 2019,10(1):2043.
[34] FENG J,QIAN Y,ZHOU Z,et al.Polysaccharide utilization loci in Bacteroides determine population fitness and community-level interactions[J].Cell Host & Microbe,2022,30(2):200-215.
[35] SOLDEN L M,NAAS A E,ROUX S,et al.Interspecies cross-feeding orchestrates carbon degradation in the rumen ecosystem[J].Nature Microbiology,2018,3(11):1274-1284.
[36] BRAVO M F,PALANICHAMY K,SHLAIN M A,et al.Synthesis and binding of mannose-specific synthetic carbohydrate receptors[J].Chemistry,2020,26(51):11782-11795.
[37] 原野,胡彦波,周义发.糖苷水解酶——生物转化制备活性糖苷与苷元的有效工具[J].微生物学报,2017,57(8):1219-1234. YUAN Y,HU Y B,ZHOU Y F.Glycosidase:An effective tool for the preparation of active glycosides and aglycone[J].Acta Microbiologica Sinica,2017,57(8):1219-1234.(in Chinese)
[38] 冯丹.糖苷水解酶的异源表达及酶学性质研究[D].济南:山东大学,2018. FENG D.Heterologous expression and enzymology characteristics research of glycoside hydrolase[D].Jinan:Shangdong University,2018.(in Chinese)
[39] SOBALA L F,SPECIALE G,ZHU S,et al.An epoxide intermediate in glycosidase catalysis[J].ACS Central Science,2020,6(5):760-770.
[40] KMEZIK C,KRSKA D,MAZURKEWICH S,et al.Characterization of a novel multidomain ce15-gh8 enzyme encoded by a polysaccharide utilization locus in the human gut bacterium Bacteroides eggerthii[J].Scientific Reports,2021,11(1):17662.
[41] PILGAARD B,WILKENS C,HERBST F A,et al.Proteomic enzyme analysis of the marine fungus Paradendryphiella salina reveals alginate lyase as a minimal adaptation strategy for brown algae degradation[J].Scientific Reports,2019,9(1):12338.
[42] CHU Y,HAO Z,WANG K,et al.The GH10 and GH48 dual-functional catalytic domains from a multimodular glycoside hydrolase synergize in hydrolyzing both cellulose and xylan[J].Biotechnol Biofuels,2019,12:279.
[43] DEJEAN G,TAMURA K,CABRERA A,et al.Synergy between cell surface glycosidases and glycan-binding proteins dictates the utilization of specific beta(1,3)-glucans by human gut bacteroides[J].mBio,2020,11(2):e00095-20.
[44] LA ROSA S L,LETH M L,MICHALAK L,et al.The human gut Firmicute roseburia intestinalis is a primary degrader of dietary beta-mannans[J].Nature Communications,2019,10(1):905.
[45] GALVEZ E,ILJAZOVIC A,AMEND L,et al.Distinct polysaccharide utilization determines interspecies competition between intestinal Prevotella spp.[J].Cell Host & Microbe,2020,28(6):838-852.
[46] ILJAZOVIC A,ROY U,GALVEZ E,et al.Perturbation of the gut microbiome by Prevotella spp.enhances host susceptibility to mucosal inflammation[J].Mucosal Immunology,2021,14(1):113-124.
[47] CARASSO S,FISHMAN B,LASK L S,et al.Metagenomic analysis reveals the signature of gut microbiota associated with human chronotypes[J].FASEB Journal,2021,35(11):e22011.
[48] PAL D,NASKAR M,BERA A,et al.Chemical synthesis of the pentasaccharide repeating unit of the o-specific polysaccharide from Ruminococcus gnavus[J].Carbohydrate Research,2021,507:108384.
[49] REICHARDT N,VOLLMER M,HOLTROP G,et al.Specific substrate-driven changes in human faecal microbiota composition contrast with functional redundancy in short-chain fatty acid production[J].The ISME Journal,2018,12(2):610-622.
[50] SCHWALM N R,GROISMAN E A.Navigating the gut buffet:Control of polysaccharide utilization in Bacteroides spp.[J].Trends in Microbiology,2017,25(12):1005-1015.
[51] TURRONI F,MILANI C,DURANTI S,et al.Glycan utilization and cross-feeding activities by Bifidobacteria[J].Trends in Microbiology,2018,26(4):339-350.
[52] LUIS A S,BRIGGS J,ZHANG X,et al.Dietary pectic glycans are degraded by coordinated enzyme pathways in human colonic Bacteroides[J].Nature Microbiology,2018,3(2):210-219.
[53] BRIGGS J A,GRONDIN J M,BRUMER H.Communal living:Glycan utilization by the human gut microbiota[J].Environmental Microbiology,2021,23(1):15-35.
[54] MACKIE R I,CANN I.Let them eat fruit[J].Nature Microbiology,2018,3(2):127-129.
[55] HAO Z,WANG X,YANG H,et al.PUL-mediated plant cell wall polysaccharide utilization in the gut Bacteroidetes[J].International Journal of Molecular Sciences,2021,22(6):3077.
[56] GUL L,MODOS D,FONSECA S,et al.Extracellular vesicles produced by the human commensal gut bacterium Bacteroides thetaiotaomicron affect host immune pathways in a cell-type specific manner that are altered in inflammatory bowel disease[J].Journal of Extracellular Vesicles,2022,11(1):e12189.
[57] AKTAR R,PARKAR N,STENTZ R,et al.Human resident gut microbe Bacteroides thetaiotaomicron regulates colonic neuronal innervation and neurogenic function[J].Gut Microbes,2020,11(6):1745-1757.
[58] DEMARTINO P,COCKBURN D W.Resistant starch:Impact on the gut microbiome and health[J].Current Opinion in Biotechnology,2020,61:66-71.
[59] TEMPLE M J,CUSKIN F,BASLE A,et al.A bacteroidetes locus dedicated to fungal 1,6-beta-glucan degradation:Unique substrate conformation drives specificity of the key endo-1,6-beta-glucanase[J].The Journal of Biological Chemistry,2017,292(25):10639-10650.
[60] REID C,FRASER N,ROSE D.Crystallization of two alpha-glucosidases found in Bacteroides thetaiotaomicron[J].Acta Crystallographica Section A Foundations and Advances,2019,75(a1):a453.
[61] WU D,ZHENG J,MAO G,et al.Rethinking the impact of RG-Ⅰ mainly from fruits and vegetables on dietary health[J].Critical Reviews in Food Science and Nutrition,2020,60(17):2938-2960.
[62] MARÍLIA L C,DANIELE M F,JORGE L D,et al.Gastroprotective effects and structural characterization of a pectic fraction isolated from Artemisia campestris subsp maritima[J].International Journal of Biological Macromolecules,2018,107(Pt B):2395-2403.
[63] LI M,LI S,GUO X,et al.Discrete genetic loci in human gut Bacteroides thetaiotaomicron confer pectin metabolism[J].Carbohydrate Polymers,2021,272:118534.
[64] LABOUREL A,BASLÉ A,MUNOZ-MUNOZ J,et al.Structural and functional analyses of glycoside hydrolase 138 enzymes targeting chain A galacturonic acid in the complex pectin rhamnogalacturonan Ⅱ[J].The Journal of Biological Chemistry,2019,294(19):7711-7721.
[65] NDEH D,BASLE A,STRAHL H,et al.Metabolism of multiple glycosaminoglycans by Bacteroides thetaiotaomicron is orchestrated by a versatile core genetic locus[J].Nature Communications,2020,11(1):646.
[66] LIU H,HE P,HE L,et al.Structure characterization and hypoglycemic activity of an arabinogalactan from Phyllostachys heterocycla bamboo shoot shell[J].Carbohydrate Polymers,2018,201:189-200.
[67] ZHANG H,ZHONG J,ZHANG Q,et al.Structural elucidation and bioactivities of a novel arabinogalactan from Coreopsis tinctoria[J].Carbohydrate Polymers,2019,219:219-228.
[68] ABDUL B,TING M,JUNQUAN L,et al.Highly efficient degradation of xylan into xylose by a single enzyme[J].ACS Sustainable Chemistry & Engineering,2019,7(13):11360-11368.
[69] 王璐瑶.多形拟杆菌乙酰木聚糖酯酶BTAxe1的理性设计[D].北京:中国农业科学院,2021. WANG L Y.Rational design of acetyl xylan esterase BTAxe1 from Bacteroides thetaiotaomicron[D].Beijing:Chinese Academy of Agricultural Sciences,2021.(in Chinese)
[70] 戴琳.Aspergillus niger An76木聚糖降解酶系的表征及协同机制的研究[D].济南:山东大学,2019. DAI L.Studies on properties and synergistic mechanism of xylan degradation-related enzymes in Aspergillus niger An76[D].Jinan:Shangdong University,2019.(in Chinese)
[71] ROGOWSKI A,BRIGGS J A,MORTIMER J C,et al.Glycan complexity dictates microbial resource allocation in the large intestine[J].Nature Communications,2015,6:7481.
[72] SINGH S,SINGH G,ARYA S K.Mannans:An overview of properties and application in food products[J].International Journal of Biological Macromolecules,2018,119:79-95.
[73] HEHEMANN J H,REINTJES G,KLASSEN L,et al.Single cell fluorescence imaging of glycan uptake by intestinal bacteria[J].The ISME Journal,2019,13(7):1883-1889.
[74] OBA S,WASHIDA K,SHIMADA Y,et al.Yeast mannan increases Bacteroides thetaiotaomicron abundance and suppresses putrefactive compound production in in vitro fecal microbiota fermentation[J].Bioscience,Biotechnology,and Biochemistry,2020,84(10):2174-2178.
[75] OBA S,SUNAGAWA T,TANIHIRO R,et al.Author correction:Prebiotic effects of yeast mannan,which selectively promotes Bacteroides thetaiotaomicron and Bacteroides ovatus in a human colonic microbiota model[J].Scientific Reports,2021,11(1):17351.
[76] BAGENHOLM V,WIEMANN M,REDDY S K,et al.A surface-exposed GH26 beta-mannanase from Bacteroides ovatus:Structure,role,and phylogenetic analysis of BoMan26B[J].The Journal of Biological Chemistry,2019,294(23):9100-9117.