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The Sus operon: a model system for starch uptake by the human gut Bacteroidetes

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Abstract

Resident bacteria in the densely populated human intestinal tract must efficiently compete for carbohydrate nutrition. The Bacteroidetes, a dominant bacterial phylum in the mammalian gut, encode a plethora of discrete polysaccharide utilization loci (PULs) that are selectively activated to facilitate glycan capture at the cell surface. The most well-studied PUL-encoded glycan-uptake system is the starch utilization system (Sus) of Bacteroides thetaiotaomicron. The Sus includes the requisite proteins for binding and degrading starch at the surface of the cell preceding oligosaccharide transport across the outer membrane for further depolymerization to glucose in the periplasm. All mammalian gut Bacteroidetes possess analogous Sus-like systems that target numerous diverse glycans. In this review, we discuss what is known about the eight Sus proteins of B. thetaiotaomicron that define the Sus-like paradigm of nutrient acquisition that is exclusive to the Gram-negative Bacteroidetes. We emphasize the well-characterized outer membrane proteins SusDEF and the α-amylase SusG, each of which have unique structural features that allow them to interact with starch on the cell surface. Despite the apparent redundancy in starch-binding sites among these proteins, each has a distinct role during starch catabolism. Additionally, we consider what is known about how these proteins dynamically interact and cooperate in the membrane and propose a model for the formation of the Sus outer membrane complex.

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References

  1. Round JL, Mazmanian SK (2009) The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 9(5):313–323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Flint HJ, Bayer EA, Rincon MT, Lamed R, White BA (2008) Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat Rev Microbiol 6(2):121–131

    Article  CAS  PubMed  Google Scholar 

  3. Wardwell LH, Huttenhower C, Garrett WS (2011) Current concepts of the intestinal microbiota and the pathogenesis of infection. Curr Infect Dis Rep 13(1):28–34

    Article  PubMed  PubMed Central  Google Scholar 

  4. Stappenbeck TS, Hooper LV, Gordon JI (2002) Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc Natl Acad Sci USA 99(24):15451–15455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Natarajan N, Pluznick JL (2014) From microbe to man: the role of microbial short chain fatty acid metabolites in host cell biology. Am J Physiol Cell Physiol 307(11):C979–C985. doi:10.1152/ajpcell.00228.2014

    Article  CAS  PubMed  Google Scholar 

  6. Koropatkin NM, Cameron EA, Martens EC (2012) How glycan metabolism shapes the human gut microbiota. Nat Rev Microbiol 10(5):323–335. doi:10.1038/nrmicro2746

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Ze X, Le Mougen F, Duncan SH, Louis P, Flint HJ (2013) Some are more equal than others: the role of “keystone” species in the degradation of recalcitrant substrates. Gut Microbes 4(3):236–240. doi:10.4161/gmic.23998

    Article  PubMed  PubMed Central  Google Scholar 

  8. 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. doi:10.1038/nature12820

    Article  CAS  PubMed  Google Scholar 

  9. Carmody RN, Gerber GK, Luevano JM Jr, Gatti DM, Somes L, Svenson KL, Turnbaugh PJ (2015) Diet dominates host genotype in shaping the murine gut microbiota. Cell Host Microbe 17(1):72–84. doi:10.1016/j.chom.2014.11.010

    Article  CAS  PubMed  Google Scholar 

  10. Zeeman SC, Kossmann J, Smith AM (2010) Starch: its metabolism, evolution, and biotechnological modification in plants. Annu Rev Plant Biol 61:209–234. doi:10.1146/annurev-arplant-042809-112301

    Article  CAS  PubMed  Google Scholar 

  11. 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. doi:10.1038/nrmicro3050

    Article  PubMed  Google Scholar 

  12. Birt DF, Boylston T, Hendrich S, Jane JL, Hollis J, Li L, McClelland J, Moore S, Phillips GJ, Rowling M, Schalinske K, Scott MP, Whitley EM (2013) Resistant starch: promise for improving human health. Adv Nutr 4(6):587–601. doi:10.3945/an.113.004325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Hii SL, Tan JS, Ling TC, Ariff AB (2012) Pullulanase: role in starch hydrolysis and potential industrial applications. Enzyme Res 2012:921362. doi:10.1155/2012/921362

    Article  PubMed  PubMed Central  Google Scholar 

  14. Cockburn DW, Orlovsky NI, Foley MH, Kwiatkowski KJ, Bahr CM, Maynard M, Demeler B, Koropatkin NM (2015) Molecular details of a starch utilization pathway in the human gut symbiont Eubacterium rectale. Mol Microbiol 95(2):209–230. doi:10.1111/mmi.12859

    Article  CAS  PubMed  Google Scholar 

  15. Martens EC, Koropatkin NM, Smith TJ, Gordon JI (2009) Complex glycan catabolism by the human gut microbiota: the Bacteroidetes Sus-like paradigm. J Biol Chem 284(37):24673–24677

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Ze X, Ben David Y, Laverde-Gomez JA, Dassa B, Sheridan PO, Duncan SH, Louis P, Henrissat B, Juge N, Koropatkin NM, Bayer EA, Flint HJ (2015) Unique organization of extracellular amylases into amylosomes in the resistant starch-utilizing human colonic firmicutes bacterium Ruminococcus bromii. MBio. doi:10.1128/mBio.01058-15

    PubMed  PubMed Central  Google Scholar 

  17. Duranti S, Turroni F, Lugli GA, Milani C, Viappiani A, Mangifesta M, Gioiosa L, Palanza P, van Sinderen D, Ventura M (2014) Genomic characterization and transcriptional studies of the starch-utilizing strain Bifidobacterium adolescentis 22L. Appl Environ Microbiol 80(19):6080–6090. doi:10.1128/AEM.01993-14

    Article  PubMed  PubMed Central  Google Scholar 

  18. Mahowald MA, Rey FE, Seedorf H, Turnbaugh PJ, Fulton RS, Wollam A, Shah N, Wang C, Magrini V, Wilson RK, Cantarel BL, Coutinho PM, Henrissat B, Crock LW, Russell A, Verberkmoes NC, Hettich RL, Gordon JI (2009) Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla. Proc Natl Acad Sci USA 106(14):5859–5864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Gu Y, Ding Y, Ren C, Sun Z, Rodionov DA, Zhang W, Yang S, Yang C, Jiang W (2010) Reconstruction of xylose utilization pathway and regulons in Firmicutes. BMC Genom 11:255. doi:10.1186/1471-2164-11-255

    Article  Google Scholar 

  20. Scott KP, Martin JC, Chassard C, Clerget M, Potrykus J, Campbell G, Mayer CD, Young P, Rucklidge G, Ramsay AG, Flint HJ (2011) Substrate-driven gene expression in Roseburia inulinivorans: importance of inducible enzymes in the utilization of inulin and starch. Proc Natl Acad Sci USA 108(Suppl 1):4672–4679. doi:10.1073/pnas.1000091107

    Article  CAS  PubMed  Google Scholar 

  21. Xu J, Mahowald MA, Ley RE, Lozupone CA, Hamady M, Martens EC, Henrissat B, Coutinho PM, Minx P, Latreille P, Cordum H, Van Brunt A, Kim K, Fulton RS, Fulton LA, Clifton SW, Wilson RK, Knight RD, Gordon JI (2007) Evolution of symbiotic bacteria in the distal human intestine. PLoS Biol 5(7):e156

    Article  PubMed  PubMed Central  Google Scholar 

  22. Salyers AA, Vercellotti JR, West SE, Wilkins TD (1977) Fermentation of mucin and plant polysaccharides by strains of Bacteroides from the human colon. Appl Environ Microbiol 33(2):319–322

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Anderson KL, Salyers AA (1989) Biochemical evidence that starch breakdown by Bacteroides thetaiotaomicron involves outer membrane starch-binding sites and periplasmic starch-degrading enzymes. J Bacteriol 171(6):3192–3198

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Tancula E, Feldhaus MJ, Bedzyk LA, Salyers AA (1992) Location and characterization of genes involved in binding of starch to the surface of Bacteroides thetaiotaomicron. J Bacteriol 174(17):5609–5616

    CAS  PubMed  PubMed Central  Google Scholar 

  25. D’Elia JN, Salyers AA (1996) Effect of regulatory protein levels on utilization of starch by Bacteroides thetaiotaomicron. J Bacteriol 178(24):7180–7186

    PubMed  PubMed Central  Google Scholar 

  26. Shipman JA, Berleman JE, Salyers AA (2000) Characterization of four outer membrane proteins involved in binding starch to the cell surface of Bacteroides thetaiotaomicron. J Bacteriol 182(19):5365–5372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Cho KH, Salyers AA (2001) Biochemical analysis of interactions between outer membrane proteins that contribute to starch utilization by Bacteroides thetaiotaomicron. J Bacteriol 183(24):7224–7230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Shipman JA, Cho KH, Siegel HA, Salyers AA (1999) Physiological characterization of SusG, an outer membrane protein essential for starch utilization by Bacteroides thetaiotaomicron. J Bacteriol 181(23):7206–7211

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Reeves AR, D’Elia JN, Frias J, Salyers AA (1996) A Bacteroides thetaiotaomicron outer membrane protein that is essential for utilization of maltooligosaccharides and starch. J Bacteriol 178(3):823–830

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Smith KA, Salyers AA (1991) Characterization of a neopullulanase and an alpha-glucosidase from Bacteroides thetaiotaomicron 95-1. J Bacteriol 173(9):2962–2968

    CAS  PubMed  PubMed Central  Google Scholar 

  31. D’Elia JN, Salyers AA (1996) Contribution of a neopullulanase, a pullulanase, and an alpha-glucosidase to growth of Bacteroides thetaiotaomicron on starch. J Bacteriol 178(24):7173–7179

    PubMed  PubMed Central  Google Scholar 

  32. Sonnenburg JL, Xu J, Leip DD, Chen CH, Westover BP, Weatherford J, Buhler JD, Gordon JI (2005) Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 307(5717):1955–1959

    Article  CAS  PubMed  Google Scholar 

  33. 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. doi:10.1038/nature12907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Rogowski A, Briggs JA, Mortimer JC, Tryfona T, Terrapon N, Lowe EC, Basle A, Morland C, Day AM, Zheng H, 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 6:7481. doi:10.1038/ncomms8481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Cuskin F, Lowe EC, Temple MJ, Zhu Y, Cameron EA, Pudlo NA, Porter NT, Urs K, Thompson AJ, Cartmell A, Rogowski A, Hamilton BS, Chen R, Tolbert TJ, Piens K, Bracke D, Vervecken W, Hakki Z, Speciale G, Munoz-Munoz JL, Day A, Pena MJ, McLean R, Suits MD, Boraston AB, Atherly T, Ziemer CJ, Williams SJ, Davies GJ, Abbott DW, Martens EC, Gilbert HJ (2015) Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism. Nature 517(7533):165–169. doi:10.1038/nature13995

    Article  CAS  PubMed  Google Scholar 

  36. Sonnenburg ED, Zheng H, Joglekar P, Higginbottom SK, Firbank SJ, Bolam DN, Sonnenburg JL (2010) Specificity of polysaccharide use in intestinal Bacteroides species determines diet-induced microbiota alterations. Cell 141(7):1241–1252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Hehemann JH, Kelly AG, Pudlo NA, Martens EC, Boraston AB (2012) Bacteria of the human gut microbiome catabolize red seaweed glycans with carbohydrate-active enzyme updates from extrinsic microbes. Proc Natl Acad Sci USA 109(48):19786–19791. doi:10.1073/pnas.1211002109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Bjursell MK, Martens EC, Gordon JI (2006) Functional genomic and metabolic studies of the adaptations of a prominent adult human gut symbiont, Bacteroides thetaiotaomicron, to the suckling period. J Biol Chem 281(47):36269–36279

    Article  CAS  PubMed  Google Scholar 

  39. 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):e1001221. doi:10.1371/journal.pbio.1001221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. McNulty NP, Wu M, Erickson AR, Pan C, 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):e1001637. doi:10.1371/journal.pbio.1001637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Reeves AR, Wang GR, Salyers AA (1997) Characterization of four outer membrane proteins that play a role in utilization of starch by Bacteroides thetaiotaomicron. J Bacteriol 179(3):643–649

    CAS  PubMed  PubMed Central  Google Scholar 

  42. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Bolam DN, Koropatkin NM (2012) Glycan recognition by the Bacteroidetes Sus-like systems. Curr Opin Struct Biol 22(5):563–569. doi:10.1016/j.sbi.2012.06.006

    Article  CAS  PubMed  Google Scholar 

  44. D’Andrea LD, Regan L (2003) TPR proteins: the versatile helix. Trends Biochem Sci 28(12):655–662

    Article  PubMed  Google Scholar 

  45. Machovic M, Janecek S (2006) The evolution of putative starch-binding domains. FEBS Lett 580(27):6349–6356. doi:10.1016/j.febslet.2006.10.041

    Article  CAS  PubMed  Google Scholar 

  46. Machovic M, Janecek S (2006) Starch-binding domains in the post-genome era. Cell Molec Life Sci 63(23):2710–2724. doi:10.1007/s00018-006-6246-9

    Article  CAS  PubMed  Google Scholar 

  47. Cockburn D, Wilkens C, Ruzanski C, Andersen S, Nielsen J, Smith AM, Field RA, Willemoes M, Hachem MA, Svensson B (2014) Analysis of surface binding sites (SBSs) in carbohydrate active enzymes with focus on glycoside hydrolase families 13 and 77–a mini-review. Biologia 69(6):705–712

    Article  CAS  Google Scholar 

  48. Abbott DW, van Bueren AL (2014) Using structure to inform carbohydrate binding module function. Curr Opin Struct Biol 28:32–40. doi:10.1016/j.sbi.2014.07.004

    Article  CAS  PubMed  Google Scholar 

  49. Taylor ME, Drickamer K (2014) Convergent and divergent mechanisms of sugar recognition across kingdoms. Curr Opin Struct Biol 28:14–22. doi:10.1016/j.sbi.2014.07.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Boraston AB, Healey M, Klassen J, Ficko-Blean E, Lammerts van Bueren A, Law V (2006) A structural and functional analysis of alpha-glucan recognition by family 25 and 26 carbohydrate-binding modules reveals a conserved mode of starch recognition. J Biol Chem 281(1):587–598. doi:10.1074/jbc.M509958200

    Article  CAS  PubMed  Google Scholar 

  51. Chou WI, Pai TW, Liu SH, Hsiung BK, Chang MD (2006) The family 21 carbohydrate-binding module of glucoamylase from Rhizopus oryzae consists of two sites playing distinct roles in ligand binding. Biochem J396(3):469–477. doi:10.1042/BJ20051982

    Article  Google Scholar 

  52. Williamson MP, Le Gal-Coeffet MF, Sorimachi K, Furniss CS, Archer DB, Williamson G (1997) Function of conserved tryptophans in the Aspergillus niger glucoamylase 1 starch binding domain. Biochemistry 36(24):7535–7539. doi:10.1021/bi9702896

    Article  CAS  PubMed  Google Scholar 

  53. Robert X, Haser R, Mori H, Svensson B, Aghajari N (2005) Oligosaccharide binding to barley alpha-amylase 1. J Biol Chem 280(38):32968–32978

    Article  CAS  PubMed  Google Scholar 

  54. Glaring MA, Baumann MJ, Abou Hachem M, Nakai H, Nakai N, Santelia D, Sigurskjold BW, Zeeman SC, Blennow A, Svensson B (2011) Starch-binding domains in the CBM45 family-low-affinity domains from glucan, water dikinase and alpha-amylase involved in plastidial starch metabolism. FEBS J 278(7):1175–1185. doi:10.1111/j.1742-4658.2011.08043.x

    Article  CAS  PubMed  Google Scholar 

  55. Flint HJ, Scott KP, Duncan SH, Louis P, Forano E (2012) Microbial degradation of complex carbohydrates in the gut. Gut Microbes 3(4):289–306. doi:10.4161/gmic.19897

    Article  PubMed  PubMed Central  Google Scholar 

  56. Koropatkin NM, Smith TJ (2010) SusG: a unique cell-membrane-associated alpha-amylase from a prominent human gut symbiont targets complex starch molecules. Structure 18(2):200–215

    Article  CAS  PubMed  Google Scholar 

  57. Fritzsche HB, Schwede T, Schulz GE (2003) Covalent and three-dimensional structure of the cyclodextrinase from Flavobacterium sp. no. 92. Eur J Biochem 270(10):2332–2341

    Article  CAS  PubMed  Google Scholar 

  58. Hondoh H, Kuriki T, Matsuura Y (2003) Three-dimensional structure and substrate binding of Bacillus stearothermophilus neopullulanase. J Mol Biol 326(1):177–188

    Article  CAS  PubMed  Google Scholar 

  59. Kamitori S, Kondo S, Okuyama K, Yokota T, Shimura Y, Tonozuka T, Sakano Y (1999) Crystal structure of Thermoactinomyces vulgaris R-47 alpha-amylase II (TVAII) hydrolyzing cyclodextrins and pullulan at 2.6 A resolution. J Molec Biol 287(5):907–921

    Article  CAS  PubMed  Google Scholar 

  60. Lee HS, Kim MS, Cho HS, Kim JI, Kim TJ, Choi JH, Park C, Lee HS, Oh BH, Park KH (2002) Cyclomaltodextrinase, neopullulanase, and maltogenic amylase are nearly indistinguishable from each other. J Biol Chem 277(24):21891–21897. doi:10.1074/jbc.M201623200

    Article  CAS  PubMed  Google Scholar 

  61. Cockburn D, Nielsen MM, Christiansen C, Andersen JM, Rannes JB, Blennow A, Svensson B (2015) Surface binding sites in amylase have distinct roles in recognition of starch structure motifs and degradation. Int J Biol Macromol 75:338–345. doi:10.1016/j.ijbiomac.2015.01.054

    Article  CAS  PubMed  Google Scholar 

  62. Boraston AB, Bolam DN, Gilbert HJ, Davies GJ (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 382(Pt 3):769–781. doi:10.1042/BJ20040892

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Ze X, Duncan SH, Louis P, Flint HJ (2012) Ruminococcus bromii is a keystone species for the degradation of resistant starch in the human colon. ISME J 6(8):1535–1543. doi:10.1038/ismej.2012.4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Flint HJ, Whitehead TR, Martin JC, Gasparic A (1997) Interrupted catalytic domain structures in xylanases from two distantly related strains of Prevotella ruminicola. Biochim Biophys Acta 1337(2):161–165

    Article  CAS  PubMed  Google Scholar 

  65. Zhang M, Chekan JR, Dodd D, Hong PY, Radlinski L, Revindran V, Nair SK, Mackie RI, Cann I (2014) Xylan utilization in human gut commensal bacteria is orchestrated by unique modular organization of polysaccharide-degrading enzymes. Proc Natl Acad Sci USA 111(35):E3708–E3717. doi:10.1073/pnas.1406156111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Sivakumar N, Li N, Tang JW, Patel BK, Swaminathan K (2006) Crystal structure of AmyA lacks acidic surface and provide insights into protein stability at poly-extreme condition. FEBS Lett 580(11):2646–2652

    Article  CAS  PubMed  Google Scholar 

  67. Janecek S, Svensson B, MacGregor EA (2014) Alpha-Amylase: an enzyme specificity found in various families of glycoside hydrolases. Cell Molec Life Sc 71(7):1149–1170. doi:10.1007/s00018-013-1388-z

    Article  CAS  Google Scholar 

  68. Qian M, Nahoum V, Bonicel J, Bischoff H, Henrissat B, Payan F (2001) Enzyme-catalyzed condensation reaction in a mammalian alpha-amylase. High-resolution structural analysis of an enzyme-inhibitor complex. Biochemistry 40(25):7700–7709

    Article  CAS  PubMed  Google Scholar 

  69. McCarter JD, Withers SG (1994) Mechanisms of enzymatic glycoside hydrolysis. Curr Opin Struct Biol 4(6):885–892

    Article  CAS  PubMed  Google Scholar 

  70. 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):e01441–01414. doi:10.1128/mBio.01441-14

    Article  Google Scholar 

  71. Raghavan V, Lowe EC, Townsend GE 2nd, Bolam DN, Groisman EA (2014) Tuning transcription of nutrient utilization genes to catabolic rate promotes growth in a gut bacterium. Mol Microbiol 93(5):1010–1025. doi:10.1111/mmi.12714

    Article  CAS  PubMed  Google Scholar 

  72. Smith KA, Salyers AA (1989) Cell-associated pullulanase from Bacteroides thetaiotaomicron: cloning, characterization, and insertional mutagenesis to determine role in pullulan utilization. J Bacteriol 171(4):2116–2123

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Gloster TM, Turkenburg JP, Potts JR, Henrissat B, Davies GJ (2008) Divergence of catalytic mechanism within a glycosidase family provides insight into evolution of carbohydrate metabolism by human gut flora. Chem Biol 15(10):1058–1067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Ellrott K, Jaroszewski L, Li W, Wooley JC, Godzik A (2010) Expansion of the protein repertoire in newly explored environments: human gut microbiome specific protein families. PLoS Comput Biol 6(6):e1000798

    Article  PubMed  PubMed Central  Google Scholar 

  75. 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. doi:10.1074/jbc.M112.397380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Turkenburg JP, Brzozowski AM, Svendsen A, Borchert TV, Davies GJ, Wilson KS (2009) Structure of a pullulanase from Bacillus acidopullulyticus. Proteins 76(2):516–519

    Article  CAS  PubMed  Google Scholar 

  77. Bayer EA, Lamed R, White BA, Flint HJ (2008) From cellulosomes to cellulosomics. Chem Rec 8(6):364–377

    Article  CAS  PubMed  Google Scholar 

  78. White BA, Lamed R, Bayer EA, Flint HJ (2014) Biomass utilization by gut microbiomes. Annu Rev Microbiol 68:279–296. doi:10.1146/annurev-micro-092412-155618

    Article  CAS  PubMed  Google Scholar 

  79. Renzi F, Manfredi P, Mally M, Moes S, Jeno P, Cornelis GR (2011) The N-glycan glycoprotein deglycosylation complex (Gpd) from Capnocytophaga canimorsus deglycosylates human IgG. PLoS Pathog 7(6):e1002118. doi:10.1371/journal.ppat.1002118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Karunatilaka KS, Cameron EA, Martens EC, Koropatkin NM, Biteen JS (2014) Superresolution imaging captures carbohydrate utilization dynamics in human gut symbionts. MBio 5(6):e02172. doi:10.1128/mBio.02172-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Martens EC, Roth R, Heuser JE, Gordon JI (2009) Coordinate regulation of glycan degradation and polysaccharide capsule biosynthesis by a prominent human gut symbiont. J Biol Chem 284(27):18445–18457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Los GV, Encell LP, McDougall MG, Hartzell DD, Karassina N, Zimprich C, Wood MG, Learish R, Ohana RF, Urh M, Simpson D, Mendez J, Zimmerman K, Otto P, Vidugiris G, Zhu J, Darzins A, Klaubert DH, Bulleit RF, Wood KV (2008) HaloTag: a novel protein labeling technology for cell imaging and protein analysis. ACS Chem Biol 3(6):373–382. doi:10.1021/cb800025k

    Article  CAS  PubMed  Google Scholar 

  83. Los GV, Wood K (2007) The HaloTag: a novel technology for cell imaging and protein analysis. Methods Mol Biol 356:195–208

    CAS  PubMed  Google Scholar 

  84. Martens EC, Chiang HC, Gordon JI (2008) Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe 4(5):447–457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Zhang Y (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9:40. doi:10.1186/1471-2105-9-40

    Article  PubMed  PubMed Central  Google Scholar 

  86. Roy A, Kucukural A, Zhang Y (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5(4):725–738. doi:10.1038/nprot.2010.5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Pieper U, Webb B, Dong GQ, Schneidman-Duhovny D, Fan H, Kim SJ, Khuri N, Spill Y, Weinkam P, Hammel M, Tainer J, Nilges M, Sali A (2014) ModBase, a database of annotated comparative protein structure models, and associated resources. Nucleic Acids Res 42:336–346

    Article  Google Scholar 

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Acknowledgments

This work was supported by funds from a pilot/feasibility Grant from the University of Michigan Gastrointestinal Peptides Research Center (DK 034933) awarded to N.M.K., as well as the Host Microbiome Initiative at the University of Michigan Medical School (N.M.K.). M.H.F. was partially supported by a predoctoral fellowship from the Cellular Biotechnology Training Program (T32GM008353).

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Foley, M.H., Cockburn, D.W. & Koropatkin, N.M. The Sus operon: a model system for starch uptake by the human gut Bacteroidetes. Cell. Mol. Life Sci. 73, 2603–2617 (2016). https://doi.org/10.1007/s00018-016-2242-x

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  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-016-2242-x

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