3,978
Views
17
CrossRef citations to date
0
Altmetric
Research Paper

Linear and branched β-Glucans degrading enzymes from versatile Bacteroides uniformis JCM 13288T and their roles in cooperation with gut bacteria

ORCID Icon, ORCID Icon, &
Article: 1826761 | Received 24 Jul 2020, Accepted 15 Sep 2020, Published online: 10 Oct 2020

References

  • Almeida A, Mitchell AL, Boland M, Forster SC, Gloor GB, Tarkowska A, Lawley TD, Finn RD. A new genomic blueprint of the human gut microbiota. Nature. 2019;568(7753):499–504. doi:10.1038/s41586-019-0965-1.
  • Ndeh D, Gilbert HJ. Biochemistry of complex glycan depolymerisation by the human gut microbiota. FEMS Microbiol Rev. 2018;42:146–164.
  • Xu J, Mahowald MA, Ley RE, Lozupone CA, Hamady M, Martens EC, Henrissat B, Coutinho PM, Minx P, Latreille P, et al. Evolution of symbiotic bacteria in the distal human intestine. PLoS Biol. 2007;5:e156.
  • Rakoff-Nahoum S, Foster KR, Comstock LE. The evolution of cooperation within the gut microbiota. Nature. 2016;533:255.
  • Koh A, De Vadder F, Kovatcheva-Datchary P, Backhed F. From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell. 2016;165:1332–1345.
  • Grice EA, Segre JA. The human microbiome: our second genome. Annu Rev Genomics Hum Genet. 2012;13:151–170.
  • Lapebie P, Lombard V, Drula E, Terrapon N, Henrissat B. Bacteroidetes use thousands of enzyme combinations to break down glycans. Nat Commun. 2019;10:2043.
  • Foley MH, Dejean G, Hemsworth GR, Davies GJ, Brumer H, Koropatkin NM. A cell-surface GH9 endo-glucanase coordinates with surface glycan-binding proteins to mediate xyloglucan uptake in the gut symbiont Bacteroides ovatus. J Mol Biol. 2019;431:981–995.
  • Glenwright AJ, Pothula KR, Bhamidimarri SP, Chorev DS, Basle A, Firbank SJ, Zheng H, Robinson CV, Winterhalter M, Kleinekathofer U, et al. Structural basis for nutrient acquisition by dominant members of the human gut microbiota. Nature. 2017;541:407–411.
  • Vetvicka V, Vannucci L, Sima P, Richter J. Beta Glucan: supplement or drug? From laboratory to clinical trials. Molecules. 2019;24.
  • Vannucci L, Krizan J, Sima P, Stakheev D, Caja F, Rajsiglova L, Horak V, Saieh M. Immunostimulatory properties and antitumor activities of glucans (Review). Int J Oncol. 2013;43:357–364.
  • Jayachandran M, Chen J, Chung SSM, Xu B. A critical review on the impacts of beta-glucans on gut microbiota and human health. J Nutr Biochem. 2018;61:101–110.
  • Saita H, Misaki A, Harada T. The comparison of the structure of curdlan and pachyman. Agric Biol Chem. 1968;32:1261–1269.
  • Zhang H, Row KH. Extraction and separation of polysaccharides from Laminaria japonica by size-exclusion chromatography. J Chromatogr Sci. 2015;53:498–502.
  • Aimanianda V, Clavaud C, Simenel C, Fontaine T, Delepierre M, Latge JP. Cell wall beta-(1,6)-glucan of Saccharomyces cerevisiae: structural characterization and in situ synthesis. J Biol Chem. 2009;284:13401–13412.
  • Morales D, Rutckeviski R, Villalva M, Abreu H, Soler-Rivas C, Santoyo S, Iacomini M, Smiderle FR. Isolation and comparison of alpha- and beta-D-glucans from shiitake mushrooms (Lentinula edodes) with different biological activities. Carbohydr Polym. 2020;229:115521.
  • Manners DJ, Masson AJ, Patterson JC. The structure of a beta-(1 leads to 3)-D-glucan from yeast cell walls. Biochem J. 1973;135:19–30.
  • Sathyanarayana BK, Stevens ES. Theoretical study of the conformations of pustulan [(1—-6)-beta-D-glucan]. J Biomol Struct Dyn. 1983;1:947–959.
  • Karnezis T, Fisher HC, Neumann GM, Stone BA, Stanisich VA. Cloning and characterization of the phosphatidylserine synthase gene of Agrobacterium sp. strain ATCC 31749 and effect of its inactivation on production of high-molecular-mass (1–>3)-beta-D-glucan (curdlan). J Bacteriol. 2002;184:4114–4123.
  • Wang XY, Dong JJ, Xu GC, Han RZ, Ni Y. Enhanced curdlan production with nitrogen feeding during polysaccharide synthesis by Rhizobium radiobacter. Carbohydr Polym. 2016;150:385–391.
  • Kenyon WJ, Esch SW, Buller CS. The curdlan-type exopolysaccharide produced by Cellulomonas flavigena KU forms part of an extracellular glycocalyx involved in cellulose degradation. Antonie Van Leeuwenhoek. 2005;87:143–148.
  • Kenyon WJ, Buller CS. Structural analysis of the curdlan-like exopolysaccharide produced by Cellulomonas flavigena KU. J Ind Microbiol Biotechnol. 2002;29:200–203.
  • Becker S, Scheffel A, Polz MF, Hehemann JH. Accurate quantification of laminarin in marine organic matter with enzymes from marine microbes. Appl Environ Microbiol. 2017;83:9.
  • Becker S, Tebben J, Coffinet S, Wiltshire K, Iversen MH, Harder T, Hinrichs KU, Hehemann JH. Laminarin is a major molecule in the marine carbon cycle. Proc Natl Acad Sci U S A. 2020;117:6599–6607.
  • Freitas F, Torres CAV, Reis MAM. Engineering aspects of microbial exopolysaccharide production. Bioresour Technol. 2017;245:1674–1683.
  • Liu Y, Gu Q, Ofosu FK, Yu X. Isolation and characterization of curdlan produced by Agrobacterium HX1126 using alpha-lactose as substrate. Int J Biol Macromol. 2015;81:498–503.
  • Barsanti L, Vismara R, Passarelli V, Gualtieri P. Paramylon (β-1,3-glucan) content in wild type and WZSL mutant of Euglena gracilis: effects of growth conditions. J Appl Phycol. 2001;13:59–65.
  • Henrissat B, Bairoch A. New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J. 1993;293:781–788.
  • Henrissat B. A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J. 1991;280:309–316.
  • Henrissat B, Bairoch A. Updating the sequence-based classification of glycosyl hydrolases. Biochem J. 1996;316:695–696.
  • Henrissat B, Davies G. Structural and sequence-based classification of glycoside hydrolases. Curr Opin Struct Biol. 1997;7:637–644.
  • Helbert W, Poulet L, Drouillard S, Mathieu S, Loiodice M, Couturier M, Lombard V, Terrapon N, Turchetto J, Vincentelli R,et al. Discovery of novel carbohydrate-active enzymes through the rational exploration of the protein sequences space. Proc Natl Acad Sci U S A. 2019;116:6063–6068.
  • Sakamoto Y, Nakade K, Konno N. Endo-beta-1,3-glucanase GLU1, from the fruiting body of Lentinula edodes, belongs to a new glycoside hydrolase family. Appl Environ Microbiol. 2011;77:8350–8354.
  • Takahashi M, Konishi T, Takeda T. Biochemical characterization of Magnaporthe oryzae beta-glucosidases for efficient beta-glucan hydrolysis. Appl Microbiol Biotechnol. 2011;91:1073–1082.
  • van Bueren AL, Morland C, Gilbert HJ, Boraston AB. Family 6 carbohydrate binding modules recognize the non-reducing end of beta-1,3-linked glucans by presenting a unique ligand binding surface. J Biol Chem. 2005;280:530–537.
  • Cheng R, Chen J, Yu X, Wang Y, Wang S, Zhang J. Recombinant production and characterization of full-length and truncated beta-1,3-glucanase PglA from Paenibacillus sp. S09 BMC Biotechnol. 2013;13:105.
  • Temple MJ, Cuskin F, Basle A, Hickey N, Speciale G, Williams SJ, Gilbert HJ, Lowe EC. 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 Biol Chem. 2017;292:10639–10650.
  • Koren S, Walenz BP, Berlin K, Miller JR, Bergman NH, Phillippy AM. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res. 2017;27:722–736.
  • Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30:2068–2069.
  • Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015;12:59–60.
  • Singh RP, Prakash S, Bhatia R, Negi M, Singh J, Bishnoi M, Kondepudi KK. Generation of structurally diverse pectin oligosaccharides having prebiotic attributes. Food Hydrocol. 2020;108.
  • Petersen TN, Brunak S, von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods. 2011;8:785–786.
  • Juncker AS, Willenbrock H, Von Heijne G, Brunak S, Nielsen H, Krogh A. Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci. 2003;12:1652–1662.
  • Miller GL. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem. 1959;31:426–428.
  • Kumagai Y, Okuyama M, Kimura A. Heat treatment of curdlan enhances the enzymatic production of biologically active beta-(1,3)-glucan oligosaccharides. Carbohydr Polym. 2016;146:396–401.
  • Li K, Chen W, Wang W, Tan H, Li S, Yin H. Effective degradation of curdlan powder by a novel endo-beta-1–>3-glucanase. Carbohydr Polym. 2018;201:122–130.
  • Li J, Zhu L, Zheng ZY, Zhan XB, Lin CC, Zong Y, Li WJ. A new effective process for production of curdlan oligosaccharides based on alkali-neutralization treatment and acid hydrolysis of curdlan particles in water suspension. Appl Microbiol Biotechnol. 2013;97:8495–8503.
  • Grandpierre C, Janssen HG, Laroche C, Michaud P, Warrand J. Enzymatic and chemical degradation of curdlan targeting the production of β-(1→3) oligoglucans. Carbohyd Polym. 2008;71:277–286.
  • Yu NY, Wagner JR, Laird MR, Melli G, Rey S, Lo R, Dao P, Sahinalp SC, Ester M, Foster LJ. PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics. 2010;26:1608–1615.
  • Pluvinage B, Grondin JM, Amundsen C, Klassen L, Moote PE, Xiao Y, Thomas D, Pudlo NA, Anele A, Martens EC, et al. Molecular basis of an agarose metabolic pathway acquired by a human intestinal symbiont. Nat Commun. 2018;9:1043.
  • Koropatkin NM, Martens EC, Gordon JI, Smith TJ. Starch catabolism by a prominent human gut symbiont is directed by the recognition of amylose helices. Structure. 2008;16:1105–1115.
  • Dejean G, Tamura K, Cabrera A, Jain N, Pudlo NA, Pereira G, Viborg AH, Van Petegem F, Martens EC, Brumer H. Synergy between cell surface glycosidases and glycan-binding proteins dictates the utilization of specific beta(1,3)-glucans by human gut Bacteroides. Mbio. 2020;11.
  • Lowman DW, West LJ, Bearden DW, Wempe MF, Power TD, Ensley HE, Haynes K, Williams DL, Kruppa MD. New insights into the structure of (1–>3,1–>6)-beta-D-glucan side chains in the Candida glabrata cell wall. PloS One. 2011;6:e27614.
  • Fukuda S, Saito H, Nakaji S, Yamada M, Ebine N, Tsushima E, Oka E, Kumeta K, Tsukamoto T, Tokunaga S. Pattern of dietary fiber intake among the Japanese general population. Eur J Clin Nutr. 2007;61:99–103.
  • Hehemann JH, Correc G, Barbeyron T, Helbert W, Czjzek M, Michel G. Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota. Nature. 2010;464:908–912.
  • Hehemann JH, Kelly AG, Pudlo NA, Martens EC, Boraston AB. Bacteria of the human gut microbiome catabolize red seaweed glycans with carbohydrate-active enzyme updates from extrinsic microbes. Proc Natl Acad Sci U S A. 2012;109:19786–19791.
  • Zhao J, Cheung PC. Fermentation of beta-glucans derived from different sources by Bifidobacteria: evaluation of their bifidogenic effect. J Agric Food Chem. 2011;59:5986–5992.
  • Yan S, Wei PC, Chen Q, Chen X, Wang SC, Li JR, Gao C. Functional and structural characterization of a beta-glucosidase involved in saponin metabolism from intestinal bacteria. Biochem Biophys Res Commun. 2018;496:1349–1356.
  • Kim SG, Becattini S, Moody TU, Shliaha PV, Littmann ER, Seok R, Gjonbalaj M, Eaton V, Fontana E, Amoretti L. Microbiota-derived lantibiotic restores resistance against vancomycin-resistant Enterococcus. Nature. 2019;572:665–669.
  • Charlet R, Pruvost Y, Tumba G, Istel F, Poulain D, Kuchler K, Sendid B, Jawhara S. Remodeling of the Candida glabrata cell wall in the gastrointestinal tract affects the gut microbiota and the immune response. Sci Rep. 2018;8:3316.
  • Cherry P, O’Hara C, Magee PJ, McSorley EM, Allsopp PJ. Risks and benefits of consuming edible seaweeds. Nutr Rev. 2019;77:307–329.
  • Singh RP. Glycan utilisation system in Bacteroides and Bifidobacteria and their roles in gut stability and health. Appl Microbiol Biotechnol. 2019;103:7287–7315.