瘤胃微生物多糖利用位点研究进展

doi:10.3785/j.issn.1008-9209.2019.07.091

浙江大学学报（农业与生命科学版）

2020, Vol. 46

Issue (3): 263-270 DOI: 10.3785/j.issn.1008-9209.2019.07.091

综述

瘤胃微生物多糖利用位点研究进展

高歌(

),王佳堃(

)

浙江大学动物科学学院奶业科学研究所，杭州 310058

Research advances in polysaccharide utilization loci of rumen microorganism

Ge GAO(

),Jiakun WANG(

)

Institute of Dairy Science, College of Animal Sciences, Zhejiang University, Hangzhou 310058, China

全文: PDF(1146 KB) HTML

摘要：

多糖利用位点（polysaccharide utilization loci, PULs）是一组编排特定多糖降解的基因簇，编码细胞表面多糖结合蛋白、外膜转运蛋白、碳水化合物活性酶和转录因子。通过多糖利用位点，拟杆菌可更好地协同多个蛋白的合作，实现对植物多糖识别、捕获和降解的一体化，具备高效利用多糖的能力。拟杆菌在瘤胃微生物中占比丰富，揭示瘤胃拟杆菌通过多糖利用位点降解纤维类物质的作用机制是改善瘤胃功能、挖掘高效酶的基础。本文主要对多糖利用位点的作用模式、调控机制及瘤胃微生物多糖利用位点的研究进展进行了综述，旨在为加强多糖利用位点的研究，并将其应用于微生物调控和生物能源开发提供理论依据。

关键词： 瘤胃; 微生物; 拟杆菌; 多糖; 多糖利用位点

Abstract:

Polysaccharide utilization loci (PULs) are gene clusters that orchestrate the breakdown of a specific glycan, encode cell surface polysaccharide binding proteins, outer membrane transport proteins, carbohydrate-active enzymes (CAZymes) and transcription factors. Bacteroidetes are highly abundant in rumen and are considered as efficient degraders of polysaccharides, which can use PULs to arrange the detection, sequestration, digestion of complex carbohydrates. Effective improvement of the rumen function and excavation of high-performance enzymes by Bacteroidetes will be significantly informed by a holistic understanding of the mechanisms of PULs. This paper introduces the mode of action and regulatory mechanism of PULs, reviews the latest developments in rumen PULs research, and is aimed at providing the theoretical basis for the strengthening of PULs study and the application of PULs in microorganism modification and bioenergy development.

Key words: rumen microorganism Bacteroidetes polysaccharide polysaccharide utilization loci

收稿日期: 2019-07-09 出版日期: 2020-07-17

CLC:

S 811.6

基金资助: 国家重点研发计划重点专项子课题“农副产品利用与饲料资源开发技术集成与应用”(2018YFD0501903)

通讯作者: 王佳堃 E-mail: gloria1942@163.com;jiakunwang@zju.edu.cn

作者简介: 高歌（https://orcid.org/0000-0001-9659-5157），E-mail：gloria1942@163.com

	服务
	把本文推荐给朋友
	加入引用管理器
	E-mail Alert
	RSS
	作者相关文章
	高歌
	王佳堃

引用本文:

高歌,王佳堃. 瘤胃微生物多糖利用位点研究进展[J]. 浙江大学学报（农业与生命科学版）, 2020, 46(3): 263-270.

Ge GAO,Jiakun WANG. Research advances in polysaccharide utilization loci of rumen microorganism. Journal of Zhejiang University (Agriculture and Life Sciences), 2020, 46(3): 263-270.

链接本文:

http://www.zjujournals.com/agr/CN/10.3785/j.issn.1008-9209.2019.07.091 或 http://www.zjujournals.com/agr/CN/Y2020/V46/I3/263

图 1 多糖利用位点功能示意图[12]Sus：淀粉利用系统；GH：糖苷水解酶；PUL：多糖利用位点；Reg.：调控因子。

图2 瘤胃中多糖利用位点底物选择示意图PUL：多糖利用位点；Reg.：调控因子；GH：糖苷水解酶；Sus：淀粉利用系统；Trans.：转运蛋白；Epim.：甘露二糖-2-表异构酶；CE：碳水化合物酯酶；Hypo.：假定蛋白；Est.：酯酶。

表1 瘤胃中栖瘤胃普雷沃菌和布氏普雷沃菌菌株中的多糖利用位点[40]

1	THOMAS F, HEHEMANN J H, REBUFFET E, et al. Environmental and gut Bacteroidetes: the food connection. Frontiers in Microbiology, 2011,2:93. DOI:10.3389/fmicb.2011.00093 doi: 10.3389/fmicb.2011
2	BJURSELL M K, MARTENS E C, GORDON J I. Functional genomic and metabolic studies of the adaptations of a prominent adult human gut symbiont, Bacteroides thetaiotaomicron, to the suckling period. Journal of Biological Chemistry, 2006,281(47):36269-36279. DOI:10.1074/jbc.M606509200 doi: 10.1074/jbc.M606
3	NGUYEN L N, NGUYEN A Q, JOHIR M A H, et al. Application of rumen and anaerobic sludge microbes for bio-harvesting from lignocellulosic biomass. Chemosphere, 2019,228:702-708. DOI:10.1016/j.chemosphere.2019.04.159 doi: 10.1016/j.chemosphere.2019.04.159
4	BAGENHOLM V, WIEMANN M, REDDY S K, et al. A surface-exposed GH26 β-mannanase from Bacteroides ovatus: structure, role, and phylogenetic analysis of BoMan26B. Journal of Biological Chemistry, 2019,294(23):9100-9117. DOI:10.1074/jbc.RA118.007171 doi: 10.1074/jbc.RA118.007171
5	REDDY S K, BAGENHOLM V, PUDLO N A, et al. A β-mannan utilization locus in Bacteroides ovatus involves a GH36 α-galactosidase active on galactomannans. FEBS Letters, 2016,590(14):2106-2118. DOI:10.1002/1873-3468.12250 doi: 10.1002/1873-3468.12250
6	GILES K, PLUVINAGE B, BORASTON A B. Structure of a glycoside hydrolase family 50 enzyme from a subfamily that is enriched in human gut microbiome Bacteroidetes. Proteins, 2017,85(1):182-187. DOI:10.1002/prot.25189 doi: 10.1002/prot.25189
7	TANCULA E, FELDHAUS M J, BEDZYK L A, et al. Location and characterization of genes involved in binding of starch to the surface of Bacteroides thetaiotaomicron. Journal of Bacteriology, 1992,174(17):5609-5616. DOI:10.1128/ jb.174.17.5609-5616.1992 doi: 10.1128/
8	DELLA J N, SALYERS A A. Effect of regulatory protein levels on utilization of starch by Bacteroides thetaiotaomicron. Journal of Bacteriology, 1996,178(24):7180-7186. DOI:10.1128/jb.178.24.7180-7186.1996 doi: 10.1128/jb.178.24.7180-7186.1996
9	MARTENS E C, KOROPATKIN N M, SMITH T J, et al. Complex glycan catabolism by the human gut microbiota: the Bacteroidetes sus-like paradigm. Journal of Biological Chemistry, 2009,284(37):24673-24677. DOI:10.1074/jbc.R109.022848 doi: 10.1074/jbc.R109
10	RENZI F, MANFREDI P, DOL M, et al. Glycan-foraging systems reveal the adaptation of Capnocytophaga canimorsus to the dog mouth. mBio, 2015,6(2):e02507. DOI:10.1128/mbio.02507-14 doi: 10.1128/mbio
11	BARBEYRON T, THOMAS F, BARBE V, et al. Habitat and taxon as driving forces of carbohydrate catabolism in marine heterotrophic bacteria: example of the model algae-associated bacterium Zobellia galactanivorans DsijT. Environmental Microbiology, 2016,18(12):4610-4627. DOI:10.1111/1462-2920.13584 doi: 10.1111/1462-2920.13584
12	FOLEY M H, COCKBURN D W, KOROPATKIN N M. The Sus operon: a model system for starch uptake by the human gut Bacteroidetes. Cellular and Molecular Life Sciences, 2016,73(14):2603-2617. DOI:10.1007/s00018-016-2242-x doi: 10.1007/s00018-016-2242-x
13	LUIS A S, BRIGGS J, ZHANG X Y, et al. Dietary pectic glycans are degraded by coordinated enzyme pathways in human colonic Bacteroides. Nature Microbiology, 2018,3(2):210-219. DOI:10.1038/s41564-017-0079-1 doi: 10.1038/s41564-017-0079-1
14	GLENWRIGHT A J, POTHULA K R, BHAMIDIMARRI S P, et al. Structural basis for nutrient acquisition by dominant members of the human gut microbiota. Nature, 2017,541(7637):407-411. DOI:10.1038/nature20828 doi: 10.1038/nature20828
15	KAPPELMANN L, KRüGER K, HEHEMANN J H, et al. Polysaccharide utilization loci of North Sea Flavobacteriia as basis for using SusC/D-protein expression for predicting major phytoplankton glycans. The ISME Journal, 2019,13(1):76-91. DOI:10.1038/s41396-018-0242-6 doi: 10.1038/s41396-018-0242-6
16	FLINT H J, BAYER E A, RINCON M T, et al. Poly-saccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nature Reviews Microbiology, 2008,6(2):121-131. DOI:10.1038/nrmicro1817 doi: 10.1038/nrmicro1817
17	BAYER E A, LAMED R, WHITE B A, et al. From cellulosomes to cellulosomics. The Chemical Record, 2008,8(6):364-377. DOI:10.1002/tcr.20160 doi: 10.1002/tcr.20160
18	MORAIS S, BARAK Y, CASPI J, et al. Cellulase-xylanase synergy in designer cellulosomes for enhanced degradation of a complex cellulosic substrate. mBio, 2010,1(5):e00285-10. DOI:10.1128/mBio.00285-10 doi: 10.1128/mBio.00285-10
19	NAAS A E, MACKENZIE A K, MRAVEC J, et al. Do rumen Bacteroidetes utilize an alternative mechanism for cellulose degradation? mBio, 2014,5(4):e01401-14. DOI:10.1128/mBio.01401-14 doi: 10.1128/mBio.01401-14
20	CUSKIN F, LOWE E C, TEMPLE M J, et al. Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism. Nature, 2015,517(7533):165-169. DOI:10.1038/nature13995 doi: 10.1038/nature13995
21	ROGOWSKI A, BRIGGS J A, MORTIMER J C, et al. Glycan complexity dictates microbial resource allocation in the large intestine. Nature Communications, 2015,6(1):7481. DOI:10.1038/ncomms8481 doi: 10.1038/ncomms8481
22	SOLDEN L M, NAAS A E, ROUX S, et al. Interspecies cross-feeding orchestrates carbon degradation in the rumen ecosystem. Nature Microbiology, 2018,3(11):1274-1284. DOI:10.1038/s41564-018-0225-4 doi: 10.1038/s41564-018-0225-4
23	TERRAPON N, LOMBARD V, DRULA E, et al. PULDB: the expanded database of polysaccharide utilization loci. Nucleic Acids Research, 2018,46(D1):D677-D683. DOI:10.1093/nar/gkx1022 doi: 10.1093/nar/gkx1022
24	REEVES A R, D’ELIA J N, FRIAS J, et al. A Bacteroides thetaiotaomicron outer membrane protein that is essential for utilization of maltooligosaccharides and starch. Journal of Bacteriology, 1996,178(3):823-830.
25	ROGERS T E, PUDLO N A, KOROPATKIN N M, et al. Dynamic responses of Bacteroides thetaiotaomicron during growth on glycan mixtures. Molecular Microbiology, 2013,88(5):876-890. DOI:10.1111/mmi.12228 doi: 10.1111/mmi.12228
26	MARTENS E C, ROTH R, HEUSER J E, et al. Coordinate regulation of glycan degradation and polysaccharide capsule biosynthesis by a prominent human gut symbiont. Journal of Biological Chemistry, 2009,284(27):18445-18457. DOI:10.1074/ jbc.m109.008094 doi: 10.1074/
27	N D Ⅲ SCHWALM, TOWNSEND G E Ⅱ, GROISMAN E A. Prioritization of polysaccharide utilization and control of regulator activation in Bacteroides thetaiotaomicron. Molecular Microbiology, 2017,104(1):32-45. DOI:10.1111/mmi.13609 doi: 10.1111/mmi.13609
28	POPE P B, MACKENZIE A K, GREGOR I, et al. Meta-genomics of the Svalbard reindeer rumen microbiome reveals abundance of polysaccharide utilization loci. PLoS One, 2012,7(6):e38571. DOI:10.1371/journal.pone.0104612 doi: 10.1371/journal.pone.0104612
29	WANG L Q, HATEM A, CATALYUREK U V, et al. Metagenomic insights into the carbohydrate-active enzymes carried by the microorganisms adhering to solid digesta in the rumen of cows. PLoS One, 2013,8(11):e78507. DOI:10.1371/journal.pone.0078507 doi: 10.1371/journal.pone.0078507
30	ROSEWARNE C P, POPE P B, CHEUNG J L, et al. Analysis of the bovine rumen microbiome reveals a diversity of Sus-like polysaccharide utilization loci from the bacterial phylum Bacteroidetes. Journal of Industrial Microbiology and Biotechnology, 2014,41(3):601-606. DOI:10.1007/s10295-013-1395-y doi: 10.1007/s10295-
31	GHARECHAHI J, SALEKDEH G H. A metagenomic analysis of the camel rumen’s microbiome identifies the major microbes responsible for lignocellulose degradation and fermentation. Biotechnology for Biofuels, 2018,11(1):216. DOI:10.1186/s13068-018-1214-9 doi: 10.1186/s13068-018-1214-9
32	DAI X, TIAN Y, LI J T, et al. Metatranscriptomic analyses of plant cell wall polysaccharide degradation by microorganisms in the cow rumen. Applied and Environmental Microbiology, 2015,81(4):1375-1386. DOI:10.1128/AEM.03682-14 doi: 10.1128/AEM.03682-14
33	SVARTSTROM O, ALNEBERG J, TERRAPON N, et al. Ninety-nine de novo assembled genomes from the moose (Alces alces) rumen microbiome provide new insights into microbial plant biomass degradation. The ISME Journal, 2017,11(11):2538-2551. DOI:10.1038/ismej.2017.108 doi: 10.1038/ismej.2017.108
34	STEWART R D, AUFFRET M D, WARR A, et al. Assembly of 913 microbial genomes from metagenomic sequencing of the cow rumen. Nature Communications, 2018,9(1):870. DOI:10.1038/s41467-018-03317-6 doi: 10.1038/s41467-018-03317-6
35	DESPRES J, FORANO E, LEPERCQ P, et al. Xylan degradation by the human gut Bacteroides xylanisolvens XB1A(T) involves two distinct gene clusters that are linked at the transcriptional level. BMC Genomics, 2016,17(1):326. DOI:10.1186/s12864-016-2680-8 doi: 10.1186/s12864-016-2680-8
36	DODD D, MOON Y H, SWAMINATHAN K, et al. Transcriptomic analyses of xylan degradation by Prevotella bryantii and insights into energy acquisition by xylanolytic Bacteroidetes. Journal of Biological Chemistry, 2010,285(39):30261-30273. DOI:10.1074/jbc.M110.141788 doi: 10.1074/jbc.M110.141788
37	LARSBRINK J, ROGERS T E, HEMSWORTH G R, et al. A discrete genetic locus confers xyloglucan metabolism in select human gut Bacteroidetes. Nature, 2014,506(7489):498-502. DOI:10.1038/nature12907 doi: 10.1038/nature12907
38	MACKENZIE A K, NAAS A E, KRACUN S K, et al. A polysaccharide utilization locus from an uncultured Bacteroidetes phylotype suggests ecological adaptation and substrate versatility. Applied and Environmental Microbiology, 2015,81(1):187-195. DOI:10.1128/AEM.02858-14 doi: 10.1128/AEM.02858-14
39	DAI X, ZHU Y X, LUO Y F, et al. Metagenomic insights into the fibrolytic microbiome in yak rumen. PLoS One, 2012,7(7):e40430. DOI:10.1371/journal.pone.0040430 doi: 10.1371/journal.pone.0040430
40	ACCETTO T, AVGUSTIN G. The diverse and extensive plant polysaccharide degradative apparatuses of the rumen and hindgut Prevotella species: a factor in their ubiquity? Systematic and Applied Microbiology, 2019,42(2):107-116. DOI:10.1016/j.syapm.2018.10.001 doi: 10.1016/j.syapm.2018.10.001
41	SAKAMOTO M, UMEDA M, ISHIKAWA I, et al. Prevotella multisaccharivorax sp. nov., isolated from human subgingival plaque. International Journal of Systematic and Evolutionary Microbiology, 2005,55(Pt 5):1839-1843. DOI:10.1099/ijs.0.63739-0 doi: 10.1099/ijs.0.63739-0
42	EMERSON E L, WEIMER P J. Fermentation of model hemicelluloses by Prevotella strains and Butyrivibrio fibrisolvens in pure culture and in ruminal enrichment cultures. Applied Microbiology and Biotechnology, 2017,101(10):4269-4278. DOI:10.1007/s00253-017-8150-7 doi: 10.1007/s00253-017-8150-7
43	JIN W, WANG Y, LI Y F, et al. Temporal changes of the bacterial community colonizing wheat straw in the cow rumen. Anaerobe, 2018,50:1-8. DOI:10.1016/j.anaerobe.2018.01.004 doi: 10.1016/j.anaerobe.2018.01.004
44	LIU J H, ZHANG M L, XUE C X, et al. Characterization and comparison of the temporal dynamics of ruminal bacterial microbiota colonizing rice straw and alfalfa hay within ruminants. Journal of Dairy Science, 2016,99(12):9668-9681. DOI:10.3168/jds.2016-11398 doi: 10.3168/jds.2016-11398
45	TERRAPON N, LOMBARD V, GILBERT H J, et al. Automatic prediction of polysaccharide utilization loci in Bacteroidetes species. Bioinformatics, 2015,31(5):647-655. DOI:10.1093/bioinformatics/btu716 doi: 10.1093/bioinformatics/btu716
46	BAGENHOLM V, REDDY S K, BOURAOUI H, et al. Galactomannan catabolism conferred by a polysaccharide utilization locus of Bacteroides ovatus: enzyme synergy and crystal structure of a β-mannanase. Journal of Biological Chemistry, 2017,292(1):229-243.
47	TAMURA K, FOLEY M H, GARDILL B R, et al. Surface glycan-binding proteins are essential for cereal beta-glucan utilization by the human gut symbiont Bacteroides ovatus. Cellular and Molecular Life Sciences, 2019,76(21):4319-4340. DOI:10.1007/s00018-019-03115-3 doi: 10.1007/s00018-019-03115-3
48	TUNCIL Y E, XIAO Y, PORTER N T, et al. Reciprocal prioritization to dietary glycans by gut bacteria in a competitive environment promotes stable coexistence. mBio, 2017,8(5):e01068-17. DOI:10.1128/mBio.01068-17 doi: 10.1128/mBio.01068-17
49	SHEPHERD E S, DELOACHE W C, PRUSS K M, et al. An exclusive metabolic niche enables strain engraftment in the gut microbiota. Nature, 2018,557(7705):434-438. DOI:10.1038/s41586-018-0092-4 doi: 10.1038/s41586-018-0092-4
50	BOLAM D N, BERG B VAN DEN. TonB-dependent transport by the gut microbiota: novel aspects of an old problem. Current Opinion in Structural Biology, 2018,51:35-43. DOI:10.1016/j.sbi.2018.03.001 doi: 10.1016/j.sbi.2018.03.001
51	MACKENZIE A K, POPE P B, PEDERSEN H L, et al. Two SusD-like proteins encoded within a polysaccharide utilization locus of an uncultured ruminant Bacteroidetes phylotype bind strongly to cellulose. Applied and Environmental Microbiology, 2012,78(16):5935-5937. DOI:10.1128/AEM.01164-12 doi: 10.1128/AEM

[1]	王昂,戴丹超,马旭洲,牟群,于永清,吕为群. 北方稻蟹共作对水体氮素淋溶损失的影响[J]. 浙江大学学报（农业与生命科学版）, 2019, 45(3): 332-342.
[2]	金蓉,谢文华,陈杰标,王念晨,项白雪,王岳,曹锦萍. 超声辅助热水提取对铁皮石斛水溶性多糖得率和结构的影响[J]. 浙江大学学报（农业与生命科学版）, 2019, 45(2): 196-204.
[3]	罗继鹏, 陶琦, 吴可人, 李廷强. 超积累植物内生微生物群落组成特征及其功能研究进展 [J]. 浙江大学学报（农业与生命科学版）, 2018, 44(5): 515-529.
[4]	杨晖, 柯乐芹, 舒若男, 陈雨薇, 朱婷瑜, 王俊, 范锦涛, 汪亮亮. 不同贮藏时间对食用菌多糖含量及其抗氧化活性的影响[J]. 浙江大学学报（农业与生命科学版）, 2018, 44(3): 356-364.
[5]	梁燕婷, 刘云财, 高云, 王华兵, 徐豫松. 高温条件下桑螟肠道微生物的多样性分析[J]. 浙江大学学报（农业与生命科学版）, 2018, 44(2): 215-222.
[6]	孙扬，徐会娟，李晓晶，李永涛，赵丽霞. 二氯喹啉酸对农田生态系统的影响及其微生物降解研究进展[J]. 浙江大学学报(农业与生命科学版), 2017, 43(6): 727-733.
[7]	黄俊伟，闯绍闯，陈凯，凌婉婷，唐翔宇，蒋建东. 有机污染物的植物-微生物联合修复技术研究进展[J]. 浙江大学学报(农业与生命科学版), 2017, 43(6): 757-765.
[8]	李戌清，张雅，田忠玲，吴根良. 茄子连作与轮作土壤养分、酶活性及微生物群落结构差异分析[J]. 浙江大学学报(农业与生命科学版), 2017, 43(5): 561-569.
[9]	李丽, 缪中纬, 辛清武, 朱志明, 章琳俐, 李忠荣, 郑嫩珠. 酵母硒和黄芪多糖对半番鸭屠宰性能、血清生化及抗氧化指标的影响[J]. 浙江大学学报(农业与生命科学版), 2017, 43(4): 502-510.
[10]	叶丽云，解凡，赵丽丽，方菁菁，吴小平. 硒对不同时期开袋灵芝主要活性成分的影响[J]. 浙江大学学报(农业与生命科学版), 2017, 43(4): 462-468.
[11]	周慧芳，王京文，孙吉林，李丹，张奇春. 耐镉菌联合植物吸收对土壤重金属镉污染的修复[J]. 浙江大学学报(农业与生命科学版), 2017, 43(3): 341-349.
[12]	王丽丽，国巍，付春娜，燕红. 可降解苯酚的产电芽孢杆菌WL027的分离筛选及其产电机制初探[J]. 浙江大学学报(农业与生命科学版), 2016, 42(6): 654-664.
[13]	康永波, 孔祥阳, 张晓芳, 郭丽琼, 苏君鸿. 肠道微生物与免疫的研究进展[J]. 浙江大学学报(农业与生命科学版), 2016, 42(3): 282-288.
[14]	曹宇，闫玉芳，杨文佳，熊正利，王丽娟，李灿. 二氧化碳气调对锯谷盗的毒力及其能源物质利用的影响[J]. 浙江大学学报(农业与生命科学版), 2015, 41(6): 631-640.
[15]	韦克苏，胡婷婷，李德仑，涂永高，于良骥，涂光军. 混施有效微生物群（EM）及土壤改良剂对烤烟农艺性状及品质的影响[J]. 浙江大学学报(农业与生命科学版), 2015, 41(4): 439-448.

Viewed

Full text

Abstract

Cited

Shared

Discussed