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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 |
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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.
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Received: 09 July 2019
Published: 17 July 2020
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Corresponding Authors:
Jiakun WANG
E-mail: gloria1942@163.com;jiakunwang@zju.edu.cn
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瘤胃微生物多糖利用位点研究进展
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
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|
[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
|
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|
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