Molecular details of a starch utilization pathway in the human gut symbiont Eubacterium rectale

Molecular Microbiology

Volumn 95, Issue 2, 2015, Pages 209-230

  Cockburn, Darrell W ^a   Orlovsky, Nicole I ^a   Foley, Matthew H ^a   Kwiatkowski, Kurt J ^a   Bahr, Constance M ^a   Maynard, Mallory ^a   Demeler, Borries ^b   Koropatkin, Nicole M ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 ALPHA GLUCAN BRANCHING ENZYME; ABC TRANSPORTER; AMYLOPECTIN; AMYLOSE; BETA CYCLODEXTRIN; GLUCOSE; GLYCOGEN; GLYCOGEN PHOSPHORYLASE; GLYCOGEN SYNTHASE; GLYCOSIDASE; MALTOOLIGOSACCHARIDE; MALTOSE; MALTOTRIOSE; OLIGOSACCHARIDE; STARCH; UNCLASSIFIED DRUG; GLUCAN 1,4-ALPHA-MALTOHYDROLASE; MALTOOLIGOSACCHARIDES; MALTOTETRAOSE; TRISACCHARIDE;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL CELL WALL; BACTERIAL MEMBRANE; BINDING AFFINITY; BINDING SITE; CARBOHYDRATE METABOLISM; CARBOXY TERMINAL SEQUENCE; CELL GROWTH; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOPLASM; ENZYME ACTIVITY; EUBACTERIUM; EUBACTERIUM RECTALE; GENETIC TRANSCRIPTION; MOLECULAR BIOLOGY; NONHUMAN; OPERON; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN HYDROLYSIS; PROTEIN PURIFICATION; PROTEOMICS; QUANTITATIVE ANALYSIS; SEQUENCE HOMOLOGY; UPREGULATION; ANALOGS AND DERIVATIVES; CELL MEMBRANE; CELL WALL; GENETICS; GROWTH, DEVELOPMENT AND AGING; MASS SPECTROMETRY; METABOLISM; MICROARRAY ANALYSIS; THIN LAYER CHROMATOGRAPHY;

BACTERIA (MICROORGANISMS); CLOSTRIDIUM; EUBACTERIUM RECTALE;

ATP-BINDING CASSETTE TRANSPORTERS; CARBOHYDRATE METABOLISM; CELL MEMBRANE; CELL WALL; CHROMATOGRAPHY, THIN LAYER; EUBACTERIUM; GLYCOSIDE HYDROLASES; MALTOSE; MASS SPECTROMETRY; MICROARRAY ANALYSIS; OLIGOSACCHARIDES; PROTEOMICS; STARCH; TRISACCHARIDES;

EID: 84920703276     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12859     Document Type: Article

References (90)

1. Abbott, D.W., Higgins, M.A., Hyrnuik, S., Pluvinage, B., Lammerts van Bueren, A., and Boraston, A.B. (2010) The molecular basis of glycogen breakdown and transport in Streptococcus pneumoniae. Mol Microbiol 77: 183-199.
2. Abell, G.C., Cooke, C.M., Bennett, C.N., Conlon, M.A., and McOrist, A.L. (2008) Phylotypes related to Ruminococcus bromii are abundant in the large bowel of humans and increase in response to a diet high in resistant starch. FEMS Microbiol Ecol 66: 505-515.
3. Adams, P.D., Grosse-Kunstleve, R.W., Hung, L.W., Ioerger, T.R., McCoy, A.J., Moriarty, N.W., etal. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr 58: 1948-1954.
4. Akiyama, N., Takeda, K., and Miki, K. (2009) Crystal structure of a periplasmic substrate-binding protein in complex with calcium lactate. J Mol Biol 392: 559-565.
5. Arumugam, M., Raes, J., Pelletier, E., Le Paslier, D., Yamada, T., Mende, D.R., etal. (2011) Enterotypes of the human gut microbiome. Nature 473: 174-180.
6. Brookes, E., Cao, W., and Demeler, B. (2010) A two-dimensional spectrum analysis for sedimentation velocity experiments of mixtures with heterogeneity in molecular weight and shape. Eur Biophys J 39: 405-414.
7. Chassard, C., Delmas, E., Robert, C., Lawson, P.A., and Bernalier-Donadille, A. (2012) Ruminococcus champanellensis sp. nov., a cellulose-degrading bacterium from human gut microbiota. Int J Syst Evol Microbiol 62: 138-143.
8. Clarke, J.M., Topping, D.L., Bird, A.R., Young, G.P., and Cobiac, L. (2008) Effects of high-amylose maize starch and butyrylated high-amylose maize starch on azoxymethane-induced intestinal cancer in rats. Carcinogenesis 29: 2190-2194.
9. Cockburn, D.W., and Svensson, B. (2013) Surface binding sites in carbohydrate active enzymes: and emerging picture of structural and functional diversity. In Carbohydrate Chemistry: Chemical and Biological Approaches. Lindhorst, T.K., and Rauter, A.P. (eds). Cambridge: Royal Society of Chemistry, pp. 204-221.
10. Colinge, J., Chiappe, D., Lagache, S., Moniatte, M., and Bougueleret, L. (2005) Differential proteomics via probabilistic peptide identification scores. Anal Chem 77: 596-606.
11. Comfort, D., and Clubb, R.T. (2004) A comparative genome analysis identifies distinct sorting pathways in gram-positive bacteria. Infect Immun 72: 2710-2722.
12. Conlon, M.A., Kerr, C.A., McSweeney, C.S., Dunne, R.A., Shaw, J.M., Kang, S., etal. (2012) Resistant starches protect against colonic DNA damage and alter microbiota and gene expression in rats fed a Western diet. J Nutr 142: 832-840.
13. Demeler, B. (2010) Methods for the design and analysis of sedimentation velocity and sedimentation equilibrium experiments with proteins. In Current Protocols in Protein Science. John Wiley & sons, Ltd, pp. 7.13.11-17.13.24. DOI: 10.1002/0471140864.ps0713s60
14. Demeler, B., and van Holde, K.E. (2004) Sedimentation velocity analysis of highly heterogeneous systems. Anal Biochem 335: 279-288.
15. Demeler, B., Gorbet, G., Zollars, D., Dubbs, B., Brookes, E., and Cao, W.D. (2014) UltraScan-III version 3.1: a comprehensive data analysis software package for analytical ultracentrifugation experiments.
16. Duncan, S.H., and Flint, H.J. (2008) Proposal of a neotype strain (A1-86) for Eubacterium rectale. Request for an opinion. Int J Syst Evol Microbiol 58: 1735-1736.
17. Duncan, S.H., Belenguer, A., Holtrop, G., Johnstone, A.M., Flint, H.J., and Lobley, G.E. (2007) Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Appl Environ Microbiol 73: 1073-1078.
18. Eckburg, P.B., Bik, E.M., Bernstein, C.N., Purdom, E., Dethlefsen, L., Sargent, M., etal. (2005) Diversity of the human intestinal microbial flora. Science 308: 1635-1638.
19. El Kaoutari, A., Armougom, F., Gordon, J.I., Raoult, D., and Henrissat, B. (2013) The abundance and variety of carbohydrate-active enzymes in the human gut microbiota. Nat Rev Microbiol 11: 497-504.
20. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
21. Foresti, M.L., Williams Mdel, P., Martinez-Garcia, R., and Vazquez, A. (2014) Analysis of a preferential action of alpha-amylase from B. licheniformis towards amorphous regions of waxy maize starch. Carbohydr Polym 102: 80-87.
22. Frank, D.N., St Amand, A.L., Feldman, R.A., Boedeker, E.C., Harpaz, N., and Pace, N.R. (2007) Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA 104: 13780-13785.
23. Frank, D.N., Robertson, C.E., Hamm, C.M., Kpadeh, Z., Zhang, T., Chen, H., etal. (2011) Disease phenotype and genotype are associated with shifts in intestinal-associated microbiota in inflammatory bowel diseases. Inflamm Bowel Dis 17: 179-184.
24. Gevers, D., Kugathasan, S., Denson, L.A., Vazquez-Baeza, Y., Van Treuren, W., Ren, B., etal. (2014) The treatment-naive microbiome in new-onset Crohn's disease. Cell Host Microbe 15: 382-392.
25. Gibbons, R.J., and Kapsimalis, B. (1963) Synthesis of intracellular iodophilic polysaccharide by Streptococcus mitis. Arch Oral Biol 8: 319-329.
26. Haider, S., and Pal, R. (2013) Integrated analysis of transcriptomic and proteomic data. Curr Genomics 14: 91-110.
27. Hamer, H.M., Jonkers, D., Venema, K., Vanhoutvin, S., Troost, F.J., and Brummer, R.J. (2008) Review article: the role of butyrate on colonic function. Aliment Pharmacol Ther 27: 104-119.
28. Han, Y., Agarwal, V., Dodd, D., Kim, J., Bae, B., Mackie, R.I., etal. (2012) Biochemical and structural insights into xylan utilization by the thermophilic bacterium Caldanaerobius polysaccharolyticus. J Biol Chem 287: 34946-34960.
29. Hold, G.L., Schwiertz, A., Aminov, R.I., Blaut, M., and Flint, H.J. (2003) Oligonucleotide probes that detect quantitatively significant groups of butyrate-producing bacteria in human feces. Appl Environ Microbiol 69: 4320-4324.
30. Holm, L., and Sander, C. (1995) Dali: a network tool for protein structure comparison. Trends Biochem Sci 20: 478-480.
31. Jiang, G., and Liu, Q. (2002) Characterization of residues from partially hydrolyzed potato and high amylose corn starches by pancreatic alpha-amylase. Starch 54: 527-533.
32. Kang, S., Denman, S.E., Morrison, M., Yu, Z., Dore, J., Leclerc, M., and McSweeney, C.S. (2010) Dysbiosis of fecal microbiota in Crohn's disease patients as revealed by a custom phylogenetic microarray. Inflamm Bowel Dis 16: 2034-2042.
33. Karlsson, F.H., Tremaroli, V., Nookaew, I., Bergstrom, G., Behre, C.J., Fagerberg, B., etal. (2013) Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature 498: 99-103.
34. Koropatkin, N.M., and Smith, T.J. (2010) SusG: a unique cell-membrane-associated alpha-amylase from a prominent human gut symbiont targets complex starch molecules. Structure 18: 200-215.
35. Koropatkin, N.M., Cameron, E.A., and Martens, E.C. (2012) How glycan metabolism shapes the human gut microbiota. Nat Rev Microbiol 10: 323-335.
36. Kraal, L., Abubucker, S., Kota, K., Fischbach, M.A., and Mitreva, M. (2014) The prevalence of species and strains in the human microbiome: a resource for experimental efforts. PLoS ONE 9: e97279.
37. Larsen, N., Vogensen, F.K., van den Berg, F.W., Nielsen, D.S., Andreasen, A.S., Pedersen, B.K., etal. (2010) Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS ONE 5: e9085.
38. Laue, T.M., Shah, B.D., Ridgeway, T.M., and Peltier, S.L. (1992) Computer-aided interpretation of analytical sedimentation data for proteins. In Analytical Ultracentrifugation in Biochemistry and Polymer Science. Harding, S.E., Rowe, A.J., and Horton, J.C. (eds). Cambridge: Royal Society of Chemistry, pp. 90-125.
39. Lee, H.S., Kim, M.S., Cho, H.S., Kim, J.I., Kim, T.J., Choi, J.H., etal. (2002) Cyclomaltodextrinase, neopullulanase, and maltogenic amylase are nearly indistinguishable from each other. J Biol Chem 277: 21891-21897.
40. Leitch, E.C., Walker, A.W., Duncan, S.H., Holtrop, G., and Flint, H.J. (2007) Selective colonization of insoluble substrates by human faecal bacteria. Environ Microbiol 9: 667-679.
41. Ley, R.E., Peterson, D.A., and Gordon, J.I. (2006a) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124: 837-848.
42. Ley, R.E., Turnbaugh, P.J., Klein, S., and Gordon, J.I. (2006b) Microbial ecology: human gut microbes associated with obesity. Nature 444: 1022-1023.
43. McCoy, A.J., Grosse-Kunstleve, R.W., Adams, P.D., Winn, M.D., Storoni, L.C., and Read, R.J. (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658-674.
44. Machiels, K., Joossens, M., Sabino, J., De Preter, V., Arijs, I., Eeckhaut, V., etal. (2014) A decrease of the butyrate-producing species Roseburia hominis and Faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut 63: 1275-1283.
45. Maeda, K., Nagata, H., Kuboniwa, M., Ojima, M., Osaki, T., Minamino, N., and Amano, A. (2013) Identification and characterization of Porphyromonas gingivalis client proteins that bind to Streptococcus oralis glyceraldehyde-3-phosphate dehydrogenase. Infect Immun 81: 753-763.
46. Mahowald, M.A., Rey, F.E., Seedorf, H., Turnbaugh, P.J., Fulton, R.S., Wollam, A., etal. (2009) Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla. Proc Natl Acad Sci USA 106: 5859-5864.
47. Martinez, I., Kim, J., Duffy, P.R., Schlegel, V.L., and Walter, J. (2010) Resistant starches types 2 and 4 have differential effects on the composition of the fecal microbiota in human subjects. PLoS ONE 5: e15046.
48. Matsumoto, N., Yamada, M., Kurakata, Y., Yoshida, H., Kamitori, S., Nishikawa, A., and Tonozuka, T. (2009) Crystal structures of open and closed forms of cyclo/maltodextrin-binding protein. FEBS J 276: 3008-3019.
49. Mazmanian, S.K., Liu, C.H., Tzianabos, A.O., and Kasper, D.L. (2005) An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122: 107-118.
50. Mazmanian, S.K., Round, J.L., and Kasper, D.L. (2008) A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 453: 620-625.
51. Morgan, X.C., Tickle, T.L., Sokol, H., Gevers, D., Devaney, K.L., Ward, D.V., etal. (2012) Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol 13: R79.
52. Mowbray, S.L., Smith, R.D., and Cole, L.B. (1990) Structure of the periplasmic glucose/galactose receptor of Salmonella typhimurium. Receptor 1: 41-53.
53. van Munster, I.P., Tangerman, A., and Nagengast, F.M. (1994) Effect of resistant starch on colonic fermentation, bile acid metabolism, and mucosal proliferation. Dig Dis Sci 39: 834-842.
54. Nemoto, H., Kataoka, K., Ishikawa, H., Ikata, K., Arimochi, H., Iwasaki, T., etal. (2012) Reduced diversity and imbalance of fecal microbiota in patients with ulcerative colitis. Dig Dis Sci 57: 2955-2964.
55. Nie, L., Wu, G., Culley, D.E., Scholten, J.C., and Zhang, W. (2007) Integrative analysis of transcriptomic and proteomic data: challenges, solutions and applications. Crit Rev Biotechnol 27: 63-75.
56. Nielsen, M.M., Bozonnet, S., Seo, E.S., Motyan, J.A., Andersen, J.M., Dilokpimol, A., etal. (2009) Two secondary carbohydrate binding sites on the surface of barley alpha-amylase 1 have distinct functions and display synergy in hydrolysis of starch granules. Biochemistry 48: 7686-7697.
57. Old, W.M., Meyer-Arendt, K., Aveline-Wolf, L., Pierce, K.G., Mendoza, A., Sevinsky, J.R., etal. (2005) Comparison of label-free methods for quantifying human proteins by shotgun proteomics. Mol Cell Proteomics 4: 1487-1502.
58. Oldham, M.L., Chen, S., and Chen, J. (2013) Structural basis for substrate specificity in the Escherichia coli maltose transport system. Proc Natl Acad Sci USA 110: 18132-18137.
59. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. In Methods in Enzymology. Carter, C.W.J., and Sweet, R.M.R.M. (eds). New York: Academic Press, pp. 307-326.
60. Peng, J., Narasimhan, S., Marchesi, J.R., Benson, A., Wong, F.S., and Wen, L. (2014) Long term effect of gut microbiota transfer on diabetes development. J Autoimmun 53: 85-94.
61. Pryde, S.E., Duncan, S.H., Hold, G.L., Stewart, C.S., and Flint, H.J. (2002) The microbiology of butyrate formation in the human colon. FEMS Microbiol Lett 217: 133-139.
62. Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K.S., Manichanh, C., etal. (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464: 59-65.
63. Qin, J., Li, Y., Cai, Z., Li, S., Zhu, J., Zhang, F., etal. (2012) A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490: 55-60.
64. Ramsay, A.G., Scott, K.P., Martin, J.C., Rincon, M.T., and Flint, H.J. (2006) Cell-associated alpha-amylases of butyrate-producing Firmicute bacteria from the human colon. Microbiology 152: 3281-3290.
65. Rees, D.C., Johnson, E., and Lewinson, O. (2009) ABC transporters: the power to change. Nat Rev Mol Cell Biol 10: 218-227.
66. Robert, C., and Bernalier-Donadille, A. (2003) The cellulolytic microflora of the human colon: evidence of microcrystalline cellulose-degrading bacteria in methane-excreting subjects. FEMS Microbiol Ecol 46: 81-89.
67. Schafer, K., Magnusson, U., Scheffel, F., Schiefner, A., Sandgren, M.O., Diederichs, K., etal. (2004) X-ray structures of the maltose-maltodextrin-binding protein of the thermoacidophilic bacterium Alicyclobacillus acidocaldarius provide insight into acid stability of proteins. J Mol Biol 335: 261-274.
68. Schuck, P., and Demeler, B. (1999) Direct sedimentation boundary analysis of interference optical data in analytical ultracentrifugation. Biophys J 76: 2288-2296.
69. Scott, K.P., Martin, J.C., Chassard, C., Clerget, M., Potrykus, J., Campbell, G., etal. (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.
70. Segain, J.P., Raingeard de la Bletiere, D., Bourreille, A., Leray, V., Gervois, N., Rosales, C., etal. (2000) Butyrate inhibits inflammatory responses through NFkappaB inhibition: implications for Crohn's disease. Gut 47: 397-403.
71. Sivakumar, N., Li, N., Tang, J.W., Patel, B.K., and Swaminathan, K. (2006) Crystal structure of AmyA lacks acidic surface and provide insights into protein stability at poly-extreme condition. FEBS Lett 580: 2646-2652.
72. Stam, M.R., Danchin, E.G., Rancurel, C., Coutinho, P.M., and Henrissat, B. (2006) Dividing the large glycoside hydrolase family 13 into subfamilies: towards improved functional annotations of alpha-amylase-related proteins. Protein Eng Des Sel 19: 555-562.
73. Stappenbeck, T.S., Hooper, L.V., and Gordon, J.I. (2002) Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc Natl Acad Sci USA 99: 15451-15455.
74. Vahedi-Faridi, A., Licht, A., Bulut, H., Scheffel, F., Keller, S., Wehmeier, U.F., etal. (2010) Crystal structures of the solute receptor GacH of Streptomyces glaucescens in complex with acarbose and an acarbose homolog: comparison with the acarbose-loaded maltose-binding protein of Salmonella typhimurium. J Mol Biol 397: 709-723.
75. Van Duyne, G.D., Standaert, R.F., Karplus, P.A., Schreiber, S.L., and Clardy, J. (1993) Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin. J Mol Biol 229: 105-124.
76. Van Immerseel, F., Ducatelle, R., De Vos, M., Boon, N., Van De Wiele, T., Verbeke, K., etal. (2010) Butyric acid-producing anaerobic bacteria as a novel probiotic treatment approach for inflammatory bowel disease. J Med Microbiol 59: 141-143.
77. Vonk, R.J., Hagedoorn, R.E., de Graaff, R., Elzinga, H., Tabak, S., Yang, Y.X., and Stellaard, F. (2000) Digestion of so-called resistant starch sources in the human small intestine. Am J Clin Nutr 72: 432-438.
78. Waffenschmidt, S., and Jaenicke, L. (1987) Assay of reducing sugars in the nanomole range with 2, 2′-bicinchoninate. Anal Biochem 165: 337-340.
79. Walker, A.W., Duncan, S.H., Harmsen, H.J., Holtrop, G., Welling, G.W., and Flint, H.J. (2008) The species composition of the human intestinal microbiota differs between particle-associated and liquid phase communities. Environ Microbiol 10: 3275-3283.
80. Walker, A.W., Ince, J., Duncan, S.H., Webster, L.M., Holtrop, G., Ze, X., etal. (2011) Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J 5: 220-230.
81. Wang, J.F., Zhu, Y.H., Li, D.F., Wang, Z., and Jensen, B.B. (2004) In vitro fermentation of various fiber and starch sources by pig fecal inocula. J Anim Sci 82: 2615-2622.
82. Willing, B.P., Dicksved, J., Halfvarson, J., Andersson, A.F., Lucio, M., Zheng, Z., etal. (2010) A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology 139: 1844-1854.e1.
83. Wilson, W.A., Roach, P.J., Montero, M., Baroja-Fernandez, E., Munoz, F.J., Eydallin, G., etal. (2010) Regulation of glycogen metabolism in yeast and bacteria. FEMS Microbiol Rev 34: 952-985.
84. Wu, N., Yang, X., Zhang, R., Li, J., Xiao, X., Hu, Y., etal. (2013) Dysbiosis signature of fecal microbiota in colorectal cancer patients. Microb Ecol 66: 462-470.
85. Yoshioka, Y., Hasegawa, K., Matsuura, Y., Katsube, Y., and Kubota, M. (1997) Crystal structures of a mutant maltotetraose-forming exo-amylase cocrystallized with maltopentaose. J Mol Biol 271: 619-628.
86. Yu, N.Y., Wagner, J.R., Laird, M.R., Melli, G., Rey, S., Lo, R., etal. (2010) PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics 26: 1608-1615.
87. Yu, T., Xu, X., Peng, Y., Luo, Y., and Yang, K. (2012) Cell wall proteome of Clostridium thermocellum and detection of glycoproteins. Microbiol Res 167: 364-371.
88. Ze, X., Duncan, S.H., Louis, P., and Flint, H.J. (2012) Ruminococcus bromii is a keystone species for the degradation of resistant starch in the human colon. ISME J 6: 1535-1543.
89. Zukin, R.S., Strange, P.G., Heavey, R., and Koshland, D.E. (1977) Properties of the galactose binding protein of Salmonella typhimurium and Escherichia coli. Biochemistry 16: 381-386.
90. Zwart, P.H., Afonine, P.V., Grosse-Kunstleve, R.W., Hung, L.W., Ioerger, T.R., McCoy, A.J., etal. (2008) Automated structure solution with the PHENIX suite. Methods Mol Biol 426: 419-435.