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Cellular and Molecular Life Sciences

, Volume 76, Issue 21, pp 4319–4340 | Cite as

Surface glycan-binding proteins are essential for cereal beta-glucan utilization by the human gut symbiont Bacteroides ovatus

  • Kazune Tamura
  • Matthew H. Foley
  • Bernd R. Gardill
  • Guillaume Dejean
  • Matthew Schnizlein
  • Constance M. E. Bahr
  • A. Louise Creagh
  • Filip van Petegem
  • Nicole M. KoropatkinEmail author
  • Harry BrumerEmail author
Original Article

Abstract

The human gut microbiota, which underpins nutrition and systemic health, is compositionally sensitive to the availability of complex carbohydrates in the diet. The Bacteroidetes comprise a dominant phylum in the human gut microbiota whose members thrive on dietary and endogenous glycans by employing a diversity of highly specific, multi-gene polysaccharide utilization loci (PUL), which encode a variety of carbohydrases, transporters, and sensor/regulators. PULs invariably also encode surface glycan-binding proteins (SGBPs) that play a central role in saccharide capture at the outer membrane. Here, we present combined biophysical, structural, and in vivo characterization of the two SGBPs encoded by the Bacteroides ovatus mixed-linkage β-glucan utilization locus (MLGUL), thereby elucidating their key roles in the metabolism of this ubiquitous dietary cereal polysaccharide. In particular, molecular insight gained through several crystallographic complexes of SGBP-A and SGBP-B with oligosaccharides reveals that unique shape complementarity of binding platforms underpins specificity for the kinked MLG backbone vis-à-vis linear β-glucans. Reverse-genetic analysis revealed that both the presence and binding ability of the SusD homolog BoSGBPMLG-A are essential for growth on MLG, whereas the divergent, multi-domain BoSGBPMLG-B is dispensable but may assist in oligosaccharide scavenging from the environment. The synthesis of these data illuminates the critical role SGBPs play in concert with other MLGUL components, reveals new structure–function relationships among SGBPs, and provides fundamental knowledge to inform future (meta)genomic, biochemical, and microbiological analyses of the human gut microbiota.

Keywords

Microbiota Microbiome Dietary fiber Bacteroidetes Beta-glucan Cereal 

Notes

Acknowledgements

We thank Associate Professor Russ Algar (Dept. Chemistry, University of British Columbia) for use of a fluorescence microplate reader. We thank Associate Professor Eric Martens and his laboratory for the use of a microplate reader in the anaerobic chamber and qPCR thermal cycler. We thank Prof. Charles Haynes (Michael Smith Laboratories, UBC) for access to ITC equipment and invaluable technical advice. We thank the Canadian Macromolecular Crystallography Facility for access to beamline 08B1-1 at the Canadian Light Source, which is supported by the Canada Foundation for Innovation, Natural Sciences and Engineering Research Council of Canada, the University of Saskatchewan, the Government of Saskatchewan, Western Economic Diversification Canada, the National Research Council Canada, and the Canadian Institutes of Health Research. We thank the Life Sciences Collaborative Access Team for access to beamline 21-ID-F and 21-ID-G at the Advanced Photon Source, a U.S. Department of Energy (DOE) Office of Science User Facility operated for the DOE Office of Science by Argonne National Laboratory (Argonne, IL, USA) under Contract No. DE-AC02-06CH11357. We thank the Stanford Synchrotron Radiation Lightsource at the SLAC National Accelerator Laboratory (Menlo Park, CA, USA) for access to beamline 9-2, the use of which is supported by the U.S. DOE, Office of Science, Office of Basic Energy Sciences under Contract No. DE-AC02-76SF00515. The SSRL Structural Molecular Biology Program is supported by the DOE Office of Biological and Environmental Research, and by the National Institutes of Health, National Institute of General Medical Sciences (including P41GM103393). The contents of this publication are solely the responsibility of the authors and do not necessarily represent the official views of NIGMS or NIH.

Author contributions

KT cloned, expressed and purified recombinant SGBPs, GFP-fusions, and site-directed mutants, conducted AGE and pull-down depletion isotherm analyses, produced and purified MLG partial digest oligosaccharides, solved crystal structures of BoSGBPMLG-A, BoSGBPMLG-A_MLG7 and BoSGBPMLG-B_MLG7 with BRG, and co-wrote the article. MHF conducted reverse genetics and growth phenotype analyses, and co-wrote the article. BRG solved crystal structures of BoSGBPMLG-A, BoSGBPMLG-A_MLG7 and BoSGBPMLG-B_MLG7 with KT. GD conducted ITC experiments. MS expressed, purified and crystallized SeMet BoSGBPMLG-B_cellohexaose. CMEB crystallized BoSGBPMLG-A_cellohexaose and native BoSGBPMLG-B_cellohexaose. ALC assisted with ITC data collection and analysis. FVP, NMK, and HB designed and directed research, and co-wrote the article with input from all authors.

Funding

Work in the Brumer group was supported by operating grants from the Canadian Institutes of Health Research (MOP-137134 and MOP-142472) and infrastructure support from the Canadian Foundation for Innovation (Project #30663) and the British Columbia Knowledge Development Fund. Work in the Koropatkin group was funded by the National Institutes of Health (NIH R01 GM118475). Work in the van Petegem group was supported by the Canadian Institutes of Health Research (MOP-119404). K.T. was partially supported by a four-year doctoral fellowship from the University of British Columbia. M.H.F. was partially supported by a predoctoral fellowship from the Cellular Biotechnology Training Program (T32GM008353).

Supplementary material

18_2019_3115_MOESM1_ESM.pdf (2 mb)
Supplementary material 1 (PDF 2054 kb)

References

  1. 1.
    Sender R, Fuchs S, Milo R (2016) Revised estimates for the number of human and bacteria cells in the body. Plos Biol.  https://doi.org/10.1371/journal.pbio.1002533 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Thomas S, Izard J, Walsh E, Batich K, Chongsathidkiet P, Clarke G, Sela DA, Muller AJ, Mullin JM, Albert K, Gilligan JP, DiGuilio K, Dilbarova R, Alexander W, Prendergast GC (2017) The host microbiome regulates and maintains human health: a primer and perspective for non-microbiologists. Can Res 77(8):1783–1812.  https://doi.org/10.1158/0008-5472.can-16-2929 CrossRefGoogle Scholar
  3. 3.
    Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444(7122):1027–1031.  https://doi.org/10.1038/nature05414 CrossRefPubMedGoogle Scholar
  4. 4.
    Ridaura VK, Faith JJ, Rey FE, Cheng JY, Duncan AE, Kau AL, Griffin NW, Lombard V, Henrissat B, Bain JR, Muehlbauer MJ, Ilkayeva O, Semenkovich CF, Funai K, Hayashi DK, Lyle BJ, Martini MC, Ursell LK, Clemente JC, Van Treuren W, Walters WA, Knight R, Newgard CB, Heath AC, Gordon JI (2013) Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 341(6150):1079.  https://doi.org/10.1126/science.1241214 CrossRefGoogle Scholar
  5. 5.
    Arrieta MC, Stiemsma LT, Dimitriu PA, Thorson L, Russell S, Yurist-Doutsch S, Kuzeljevic B, Gold MJ, Britton HM, Lefebvre DL, Subbarao P, Mandhane P, Becker A, McNagny KM, Sears MR, Kollmann T, Mohn WW, Turvey SE, Finlay BB, Investigators CS (2015) Early infancy microbial and metabolic alterations affect risk of childhood asthma. Sci Transl Med 7(307):14.  https://doi.org/10.1126/scitranslmed.aab2271 CrossRefGoogle Scholar
  6. 6.
    Fujimura KE, Lynch SV (2015) Microbiota in allergy and asthma and the emerging relationship with the gut microbiome. Cell Host Microbe 17(5):592–602.  https://doi.org/10.1016/j.chom.2015.04.007 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Schwabe RF, Jobin C (2013) The microbiome and cancer. Nat Rev Cancer 13(11):800–812.  https://doi.org/10.1038/nrc3610 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Claesson MJ, Jeffery IB, Conde S, Power SE, O’Connor EM, Cusack S, Harris HMB, Coakley M, Lakshminarayanan B, O’Sullivan O, Fitzgerald GF, Deane J, O’Connor M, Harnedy N, O’Connor K, O’Mahony D, van Sinderen D, Wallace M, Brennan L, Stanton C, Marchesi JR, Fitzgerald AP, Shanahan F, Hill C, Ross RP, O’Toole PW (2012) Gut microbiota composition correlates with diet and health in the elderly. Nature 488(7410):178–184.  https://doi.org/10.1038/nature11319 CrossRefPubMedGoogle Scholar
  9. 9.
    Fujimura KE, Slusher NA, Cabana MD, Lynch SV (2010) Role of the gut microbiota in defining human health. Expert Rev Anti Infect Ther 8(4):435–454.  https://doi.org/10.1586/eri.10.14 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, Biddinger SB, Dutton RJ, Turnbaugh PJ (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505(7484):559–563.  https://doi.org/10.1038/nature12820 CrossRefGoogle Scholar
  11. 11.
    Koropatkin NM, Cameron EA, Martens EC (2012) How glycan metabolism shapes the human gut microbiota. Nat Rev Microbiol 10(5):323–335.  https://doi.org/10.1038/nrmicro2746 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Gorham JB, Kang S, Williams BA, Grant LJ, McSweeney CS, Gidley MJ, Mikkelsen D (2017) Addition of arabinoxylan and mixed linkage glucans in porcine diets affects the large intestinal bacterial populations. Eur J Nutr 56(6):2193–2206.  https://doi.org/10.1007/s00394-016-1263-4 CrossRefPubMedGoogle Scholar
  13. 13.
    Desai MS, Seekatz AM, Koropatkin NM, Kamada N, Hickey CA, Wolter M, Pudlo NA, Kitamoto S, Terrapon N, Muller A, Young VB, Henrissat B, Wilmes P, Stappenbeck TS, Nunez G, Martens EC (2016) A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility. Cell 167(5):1339–1353.  https://doi.org/10.1016/j.cell.2016.10.043 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Sonnenburg ED, Sonnenburg JL (2014) Starving our microbial self: the deleterious consequences of a diet deficient in microbiota-accessible carbohydrates. Cell Metab 20(5):779–786.  https://doi.org/10.1016/j.cmet.2014.07.003 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Williams BA, Grant LJ, Gidley MJ, Mikkelsen D (2017) Gut fermentation of dietary fibres: physico-chemistry of plant cell walls and implications for health. Int J Mol Sci.  https://doi.org/10.3390/ijms18102203 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    El Kaoutari A, Armougom F, Gordon JI, Raoult D, Henrissat B (2013) The abundance and variety of carbohydrate-active enzymes in the human gut microbiota. Nat Rev Microbiol 11(7):497–504.  https://doi.org/10.1038/nrmicro3050 CrossRefPubMedGoogle Scholar
  17. 17.
    Ding T, Schloss PD (2014) Dynamics and associations of microbial community types across the human body. Nature 509(7500):357–360.  https://doi.org/10.1038/nature13178 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Grondin JM, Tamura K, Dejean G, Abbott DW, Brumer H (2017) Polysaccharide utilization loci: fueling microbial communities. J Bacteriol 199(15):1–15.  https://doi.org/10.1128/jb.00860-16 CrossRefGoogle Scholar
  19. 19.
    Martens EC, Lowe EC, Chiang H, Pudlo NA, Wu M, McNulty NP, Abbott DW, Henrissat B, Gilbert HJ, Bolam DN, Gordon JI (2011) Recognition and degradation of plant cell wall polysaccharides by two human gut symbionts. PLoS Biol 9(12):1–16.  https://doi.org/10.1371/journal.pbio.1001221 CrossRefGoogle Scholar
  20. 20.
    Othman RA, Moghadasian MH, Jones PJH (2011) Cholesterol-lowering effects of oat beta-glucan. Nutr Rev 69(6):299–309.  https://doi.org/10.1111/j.1753-4887.2011.00401.x CrossRefPubMedGoogle Scholar
  21. 21.
    El Khoury D, Cuda C, Luhovyy BL, Anderson GH (2012) Beta glucan: health benefits in obesity and metabolic syndrome. J Nutr Metab 2012:851362.  https://doi.org/10.1155/2012/851362 CrossRefPubMedGoogle Scholar
  22. 22.
    Gunness P, Michiels J, Vanhaecke L, De Smet S, Kravchuk O, Van de Meene A, Gidley MJ (2016) Reduction in circulating bile acid and restricted diffusion across the intestinal epithelium are associated with a decrease in blood cholesterol in the presence of oat β-glucan. FASEB J 30(12):4227–4238.  https://doi.org/10.1096/fj.201600465R CrossRefPubMedGoogle Scholar
  23. 23.
    Fehlbaum S, Prudence K, Kieboom J, Heerikhuisen M, van den Broek T, Schuren FHJ, Steinert RE, Raederstorff D (2018) In vitro fermentation of selected prebiotics and their effects on the composition and activity of the adult gut microbiota. Int J Mol Sci.  https://doi.org/10.3390/ijms19103097 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Nilsson U, Johansson M, Nilsson A, Björck I, Nyman M (2008) Dietary supplementation with beta-glucan enriched oat bran increases faecal concentration of carboxylic acids in healthy subjects. Eur J Clin Nutr 62(8):978–984.  https://doi.org/10.1038/sj.ejcn.1602816 CrossRefPubMedGoogle Scholar
  25. 25.
    Tamura K, Hemsworth GR, DeJean G, Rogers TE, Pudlo NA, Urs K, Jain N, Davies GJ, Martens EC, Brumer H (2017) Molecular mechanism by which prominent human gut Bacteroidetes utilize mixed-linkage beta-glucans. Major health-promoting cereal polysaccharides. Cell Rep 21(2):417–430.  https://doi.org/10.1016/j.celrep.2017.09.049 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Bolam DN, Koropatkin NM (2012) Glycan recognition by the bacteroidetes Sus-like systems. Curr Opin Struct Biol 22(5):563–569.  https://doi.org/10.1016/j.sbi.2012.06.006 CrossRefPubMedGoogle Scholar
  27. 27.
    Koropatkin NM, Martens EC, Gordon JI, Smith TJ (2008) Starch catabolism by a prominent human gut symbiont is directed by the recognition of amylose helices. Structure 16(7):1105–1115.  https://doi.org/10.1016/j.str.2008.03.017 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Cameron EA, Maynard MA, Smith CJ, Smith TJ, Koropatkin NM, Martens EC (2012) Multidomain carbohydrate-binding proteins involved in bacteroides thetaiotaomicron starch metabolism. J Biol Chem 287(41):34614–34625.  https://doi.org/10.1074/jbc.M112.397380 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Tauzin AS, Kwiatkowski KJ, Orlovsky NI, Smith CJ, Creagh AL, Haynes CA, Wawrzak Z, Brumer H, Koropatkin NM (2016) Molecular dissection of xyloglucan recognition in a prominent human gut symbiont. Mbio 7(2):15.  https://doi.org/10.1128/mBio.02134-15 CrossRefGoogle Scholar
  30. 30.
    Cartmell A, Lowe EC, Basle A, Firbank SJ, Ndeh DA, Murray H, Terrapon N, Lombard V, Henrissat B, Turnbull JE, Czjzek M, Gilbert HJ, Bolam DN (2017) How members of the human gut microbiota overcome the sulfation problem posed by glycosaminoglycans. Proc Natl Acad Sci USA 114(27):7037–7042.  https://doi.org/10.1073/pnas.1704367114 CrossRefPubMedGoogle Scholar
  31. 31.
    Rogowski A, Briggs JA, Mortimer JC, Tryfona T, Terrapon N, Lowe EC, Basle A, Morland C, Day AM, Zheng HJ, Rogers TE, Thompson P, Hawkins AR, Yadav MP, Henrissat B, Martens EC, Dupree P, Gilbert HJ, Bolam DN (2015) Glycan complexity dictates microbial resource allocation in the large intestine. Nat Commun 6:15.  https://doi.org/10.1038/ncomms8481 CrossRefGoogle Scholar
  32. 32.
    Glenwright AJ, Pothula KR, Bhamidimarri SP, Chorev DS, Basle A, Firbank SJ, Zheng HJ, Robinson CV, Winterhalter M, Kleinekathofer U, Bolam DN, van den Berg B (2017) Structural basis for nutrient acquisition by dominant members of the human gut microbiota. Nature 541(7637):407–411.  https://doi.org/10.1038/nature20828 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Koropatkin N, Martens EC, Gordon JI, Smith TJ (2009) Structure of a SusD homologue, BT1043, involved in mucin O-glycan utilization in a prominent human gut symbiont. Biochemistry 48(7):1532–1542.  https://doi.org/10.1021/bi801942a CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Phansopa C, Roy S, Rafferty JB, Douglas CWI, Pandhal J, Wright PC, Kelly DJ, Stafford GP (2014) Structural and functional characterization of NanU, a novel high-affinity sialic acid-inducible binding protein of oral and gut-dwelling Bacteroidetes species. Biochem J 458:499–511.  https://doi.org/10.1042/bj20131415 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Mystkowska AA, Robb C, Vidal-Melgosa S, Vanni C, Fernandez-Guerra A, Hohne M, Hehemann JH (2018) Molecular recognition of the beta-glucans laminarin and pustulan by a SusD-like glycan-binding protein of a marine Bacteroidetes. FEBS J 285(23):4465–4481.  https://doi.org/10.1111/febs.14674 CrossRefPubMedGoogle Scholar
  36. 36.
    Larsbrink J, Zhu Y, Kharade SS, Kwiatkowski KJ, Eijsink VGH, Koropatkin NM, McBride MJ, Pope PB (2016) A polysaccharide utilization locus from Flavobacterium johnsoniae enables conversion of recalcitrant chitin. Biotechnol Biofuels 9:16.  https://doi.org/10.1186/s13068-016-0674-z CrossRefGoogle Scholar
  37. 37.
    Hudson KL, Bartlett GJ, Diehl RC, Agirre J, Gallagher T, Kiessling LL, Woolfson DN (2015) Carbohydrate–aromatic interactions in proteins. J Am Chem Soc 137(48):15152–15160.  https://doi.org/10.1021/jacs.5b08424 CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Asensio JL, Ardá A, Cañada FJ, Jiménez-Barbero J (2013) Carbohydrate–aromatic interactions. Acc Chem Res 46(4):946–954.  https://doi.org/10.1021/ar300024d CrossRefPubMedGoogle Scholar
  39. 39.
    Jeffrey GA (1997) An introduction to hydrogen bonding: topics in physical chemistry. Oxford University Press, New YorkGoogle Scholar
  40. 40.
    Holm L, Rosenstrom P (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res 38:W545–W549.  https://doi.org/10.1093/nar/gkq366 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Holm L, Laakso LM (2016) Dali server update. Nucleic Acids Res 44(W1):W351–W355.  https://doi.org/10.1093/nar/gkw357 CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Cameron EA, Kwiatkowski KJ, Lee BH, Hamaker BR, Koropatkin NM, Martens EC (2014) Multifunctional nutrient-binding proteins adapt human symbiotic bacteria for glycan competition in the gut by separately promoting enhanced sensing and catalysis. MBIO 5(5):1–12.  https://doi.org/10.1128/mBio.01441-14 CrossRefGoogle Scholar
  43. 43.
    Larsbrink J, Rogers TE, Hemsworth GR, McKee LS, Tauzin AS, Spadiut O, Klinter S, Pudlo NA, Urs K, Koropatkin NM, Creagh AL, Haynes CA, Kelly AG, Cederholm SN, Davies GJ, Martens EC, Brumer H (2014) A discrete genetic locus confers xyloglucan metabolism in select human gut Bacteroidetes. Nature 506(7489):498–502.  https://doi.org/10.1038/nature12907 CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Barsanti L, Passarelli V, Evangelista V, Frassanito AM, Gualtieri P (2011) Chemistry, physico-chemistry and applications linked to biological activities of beta-glucans. Nat Prod Rep 28(3):457–466.  https://doi.org/10.1039/c0np00018c CrossRefPubMedGoogle Scholar
  45. 45.
    Wood PJ, Weisz J, Blackwell BA (1994) Structural studies of (1-3), (1-4)-beta-d-glucans by C(13)-nuclear magnetic-resonance spectroscopy and by rapid analysis of cellulose-like regions using high-performance anion-exchange chromatography of oligosaccharides released by lichenase. Cereal Chem 71(3):301–307Google Scholar
  46. 46.
    Terrapon N, Lombard V, Drula E, Lapebie P, Al-Masaudi S, Gilbert HJ, Henrissat B (2018) PULDB: the expanded database of polysaccharide utilization loci. Nucleic Acids Res 46(D1):D677–D683.  https://doi.org/10.1093/nar/gkx1022 CrossRefPubMedGoogle Scholar
  47. 47.
    Foley MH, Martens EC, Koropatkin NM (2018) SusE facilitates starch uptake independent of starch binding in B. thetaiotaomicron. Mol Microbiol 108(5):551–566.  https://doi.org/10.1111/mmi.13949 CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Rakoff-Nahoum S, Coyne MJ, Comstock LE (2014) An ecological network of polysaccharide utilization among human intestinal symbionts. Curr Biol 24(1):40–49.  https://doi.org/10.1016/j.cub.2013.10.077 CrossRefPubMedGoogle Scholar
  49. 49.
    Luis AS, Briggs J, Zhang XY, Farnell B, Ndeh D, Labourel A, Basle A, Cartmell A, Terrapon N, Stott K, Lowe EC, McLean R, Shearer K, Schuckel J, Venditto I, Ralet MC, Henrissat B, Martens EC, Mosimann SC, Abbott DW, Gilbert HJ (2018) Dietary pectic glycans are degraded by coordinated enzyme pathways in human colonic Bacteroides. Nat Microbiol 3(2):210–219.  https://doi.org/10.1038/s41564-017-0079-1 CrossRefPubMedGoogle Scholar
  50. 50.
    Paetzel M, Karla A, Strynadka NCJ, Dalbey RE (2002) Signal peptidases. Chem Rev 102(12):4549–4579.  https://doi.org/10.1021/cr010166y CrossRefPubMedGoogle Scholar
  51. 51.
    Lazaridou A, Biliaderis CG, Micha-Screttas M, Steele BR (2004) A comparative study on structure-function relations of mixed-linkage (1 - > 3), (1 - > 4) linear beta-d-glucans. Food Hydrocolloids 18(5):837–855.  https://doi.org/10.1016/j.foodhyd.2004.01.002 CrossRefGoogle Scholar
  52. 52.
    Gilbert HJ, Knox JP, Boraston AB (2013) Advances in understanding the molecular basis of plant cell wall polysaccharide recognition by carbohydrate-binding modules. Curr Opin Struct Biol 23(5):669–677.  https://doi.org/10.1016/j.sbi.2013.05.005 CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Mackenzie AK, Pope PB, Pedersen HL, Gupta R, Morrison M, Willats WG, Eijsink VG (2012) Two SusD-like proteins encoded within a polysaccharide utilization locus of an uncultured ruminant Bacteroidetes phylotype bind strongly to cellulose. Appl Environ Microbiol 78(16):5935–5937.  https://doi.org/10.1128/AEM.01164-12 CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Mackenzie AK, Naas AE, Kracun SK, Schückel J, Fangel JU, Agger JW, Willats WG, Eijsink VG, Pope PB (2015) A polysaccharide utilization locus from an uncultured Bacteroidetes phylotype suggests ecological adaptation and substrate versatility. Appl Environ Microbiol 81(1):187–195.  https://doi.org/10.1128/AEM.02858-14 CrossRefPubMedGoogle Scholar
  55. 55.
    Naas AE, Mackenzie AK, Mravec J, Schückel J, Willats WG, Eijsink VG, Pope PB (2014) Do rumen Bacteroidetes utilize an alternative mechanism for cellulose degradation? MBio 5(4):e01401–e01414.  https://doi.org/10.1128/mBio.01401-14 CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Kiemle SN, Zhang X, Esker AR, Toriz G, Gatenholm P, Cosgrove DJ (2014) Role of (1,3)(1,4)-beta-glucan in cell walls: interaction with cellulose. Biomacromol 15(5):1727–1736.  https://doi.org/10.1021/bm5001247 CrossRefGoogle Scholar
  57. 57.
    McNulty NP, Wu M, Erickson AR, Pan CL, Erickson BK, Martens EC, Pudlo NA, Muegge BD, Henrissat B, Hettich RL, Gordon JI (2013) Effects of diet on resource utilization by a model human gut microbiota containing Bacteroides cellulosilyticus WH2, a symbiont with an extensive glycobiome. PLoS Biol 11(8):20.  https://doi.org/10.1371/journal.pbio.1001637 CrossRefGoogle Scholar
  58. 58.
    Cann I, Bernardi RC, Mackie RI (2016) Cellulose degradation in the human gut: Ruminococcus champanellensis expands the cellulosome paradigm. Environ Microbiol 18(2):307–310.  https://doi.org/10.1111/1462-2920.13152 CrossRefPubMedGoogle Scholar
  59. 59.
    Haskey N, Gibson DL (2017) An examination of diet for the maintenance of remission in inflammatory bowel disease. Nutrients.  https://doi.org/10.3390/nu9030259 CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Armstrong Z, Mewis K, Liu F, Morgan-Lang C, Scofield M, Durno E, Chen HM, Mehr K, Withers SG, Hallam SJ (2018) Metagenomics reveals functional synergy and novel polysaccharide utilization loci in the Castor canadensis fecal microbiome. ISME J 12(11):2757–2769.  https://doi.org/10.1038/s41396-018-0215-9 CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Shepherd ES, DeLoache WC, Pruss KM, Whitaker WR, Sonnenburg JL (2018) An exclusive metabolic niche enables strain engraftment in the gut microbiota. Nature 557(7705):434–438.  https://doi.org/10.1038/s41586-018-0092-4 CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Joglekar P, Sonnenburg ED, Higginbottom SK, Earle KA, Morland C, Shapiro-Ward S, Bolam DN, Sonnenburg JL (2018) Genetic variation of the SusC/SusD homologs from a polysaccharide utilization locus underlies divergent fructan specificities and functional adaptation in Bacteroides thetaiotaomicron strains. mSphere 3(3):5.  https://doi.org/10.1128/mspheredirect.00185-18 CrossRefGoogle Scholar
  63. 63.
    Farrar MD, Whitehead TR, Lan J, Dilger P, Thorpe R, Holland KT, Carding SR (2005) Engineering of the gut commensal bacterium Bacteroides ovatus to produce and secrete biologically active murine interleukin-2 in response to xylan. J Appl Microbiol 98(5):1191–1197.  https://doi.org/10.1111/j.1365-2672.2005.02565.x CrossRefPubMedGoogle Scholar
  64. 64.
    McGregor N, Morar M, Fenger TH, Stogios P, Lenfant N, Yin V, Xu XH, Evdokimova E, Cui H, Henrissat B, Savchenko A, Brumer H (2016) Structure-function analysis of a mixed-linkage beta-glucanase/xyloglucanase from the key ruminal Bacteroidetes Prevotella bryantii B(1)4. J Biol Chem 291(3):1175–1197.  https://doi.org/10.1074/jbc.M115.691659 CrossRefPubMedGoogle Scholar
  65. 65.
    Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nature Methods 8(10):785–786.  https://doi.org/10.1038/nmeth.1701 CrossRefPubMedGoogle Scholar
  66. 66.
    Nielsen H (2017) Predicting secretory proteins with signalP. Methods Mol Biol 1611:59–73.  https://doi.org/10.1007/978-1-4939-7015-5_6 CrossRefPubMedGoogle Scholar
  67. 67.
    Juncker AS, Willenbrock H, Von Heijne G, Brunak S, Nielsen H, Krogh A (2003) Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci 12(8):1652–1662.  https://doi.org/10.1110/ps.0303703 CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Sundqvist G, Stenvall M, Berglund H, Ottosson J, Brumer H (2007) A general, robust method for the quality control of intact proteins using LC–ESI–MS. J Chromatogr B Anal Technol Biomed Life Sci 852(1–2):188–194.  https://doi.org/10.1016/j.jchromb.2007.01.011 CrossRefGoogle Scholar
  69. 69.
    Doublié S (2007) Production of selenomethionyl proteins in prokaryotic and eukaryotic expression systems. Methods Mol Biol 363:91–108.  https://doi.org/10.1007/978-1-59745-209-0_5 CrossRefPubMedGoogle Scholar
  70. 70.
    Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol Macromol Crystallogr Pt A 276:307–326.  https://doi.org/10.1016/s0076-6879(97)76066-x CrossRefGoogle Scholar
  71. 71.
    Terwilliger TC, Adams PD, Read RJ, McCoy AJ, Moriarty NW, Grosse-Kunstleve RW, Afonine PV, Zwart PH, Hung LW (2009) Decision-making in structure solution using Bayesian estimates of map quality: the PHENIX AutoSol wizard. Acta Crystallogr Sect D Biol Crystallogr 65:582–601.  https://doi.org/10.1107/s0907444909012098 CrossRefGoogle Scholar
  72. 72.
    Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr Sect D Biol Crystallogr 66:213–221.  https://doi.org/10.1107/s0907444909052925 CrossRefGoogle Scholar
  73. 73.
    Afonine PV, Grosse-Kunstleve RW, Echols N, Headd JJ, Moriarty NW, Mustyakimov M, Terwilliger TC, Urzhumtsev A, Zwart PH, Adams PD (2012) Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr Sect D Struct Biol 68:352–367.  https://doi.org/10.1107/s0907444912001308 CrossRefGoogle Scholar
  74. 74.
    Winter G, Waterman DG, Parkhurst JM, Brewster AS, Gildea RJ, Gerstel M, Fuentes-Montero L, Vollmar M, Michels-Clark T, Young ID, Sauter NK, Evans G (2018) DIALS: implementation and evaluation of a new integration package. Acta Crystallogr Sect D Struct Biol 74:85–97.  https://doi.org/10.1107/s2059798317017235 CrossRefGoogle Scholar
  75. 75.
    Winter G (2010) xia2: an expert system for macromolecular crystallography data reduction. J Appl Crystallogr 43:186–190.  https://doi.org/10.1107/s0021889809045701 CrossRefGoogle Scholar
  76. 76.
    McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ (2007) Phaser crystallographic software. J Appl Crystallogr 40:658–674.  https://doi.org/10.1107/s0021889807021206 CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Murshudov GN, Skubak P, Lebedev AA, Pannu NS, Steiner RA, Nicholls RA, Winn MD, Long F, Vagin AA (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr Sect D Biol Crystallogr 67:355–367.  https://doi.org/10.1107/s0907444911001314 CrossRefGoogle Scholar
  78. 78.
    Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr Sect D Biol Crystallogr 60:2126–2132.  https://doi.org/10.1107/s0907444904019158 CrossRefGoogle Scholar
  79. 79.
    Agirre J, Iglesias-Fernandez J, Rovira C, Davies GJ, Wilson KS, Cowtan KD (2015) Privateer: software for the conformational validation of carbohydrate structures. Nat Struct Mol Biol 22(11):833–834.  https://doi.org/10.1038/nsmb.3115 CrossRefPubMedGoogle Scholar
  80. 80.
    Kabsch W (2010) XDS. Acta Crystallogr Sect D Biol Crystallogr 66:125–132.  https://doi.org/10.1107/s0907444909047337 CrossRefGoogle Scholar
  81. 81.
    Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AGW, McCoy A, McNicholas SJ, Murshudov GN, Pannu NS, Potterton EA, Powell HR, Read RJ, Vagin A, Wilson KS (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr Sect D Biol Crystallogr 67:235–242.  https://doi.org/10.1107/s0907444910045749 CrossRefGoogle Scholar
  82. 82.
    Potterton L, Agirre J, Ballard C, Cowtan K, Dodson E, Evans PR, Jenkins HT, Keegan R, Krissinel E, Stevenson K, Lebedev A, McNicholas SJ, Nicholls RA, Noble M, Pannu NS, Roth C, Sheldrick G, Skubak P, Turkenburg J, Uski V, von Delft F, Waterman D, Wilson K, Winn M, Wojdyr M (2018) CCP4i2: the new graphical user interface to the CCP4 program suite. Acta Crystallogr Sect D Struct Biol 74:68–84.  https://doi.org/10.1107/s2059798317016035 CrossRefGoogle Scholar
  83. 83.
    Vagin A, Teplyakov A (2010) Molecular replacement with MOLREP. Acta Crystallogr Sect D Biol Crystallogr 66:22–25.  https://doi.org/10.1107/s0907444909042589 CrossRefGoogle Scholar
  84. 84.
    Blanc E, Roversi P, Vonrhein C, Flensburg C, Lea SM, Bricogne G (2004) Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr Sect D Struct Biol 60:2210–2221.  https://doi.org/10.1107/s0907444904016427 CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Michael Smith LaboratoriesUniversity of British ColumbiaVancouverCanada
  2. 2.Department of Biochemistry and Molecular BiologyUniversity of British ColumbiaVancouverCanada
  3. 3.Department of Microbiology and ImmunologyUniversity of Michigan Medical SchoolAnn ArborUSA
  4. 4.Department of Chemical and Biological EngineeringUniversity of British ColumbiaVancouverCanada
  5. 5.Department of ChemistryUniversity of British ColumbiaVancouverCanada
  6. 6.Department of BotanyUniversity of British ColumbiaVancouverCanada

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