Structural genomics analysis of uncharacterized protein families overrepresented in human gut bacteria identifies a novel glycoside hydrolase

BMC Bioinformatics

Volumn 15, Issue 1, 2014, Pages

  Sheydina, Anna ^a,b   Eberhardt, Ruth Y ^c,d   Rigden, Daniel J ^e   Chang, Yuanyuan ^a,b   Li, Zhanwen ^b   Zmasek, Christian C ^b   Axelrod, Herbert L ^a,f   Godzik, Adam ^a,b,g  

^a Joint Center for Structural Genomics   (United States)

^b BURNHAM INSTITUTE   (United States)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^d WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^e UNIVERSITY OF LIVERPOOL   (United Kingdom)

^f SLAC NATIONAL ACCELERATOR LABORATORY   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

3D structure; Carbohydrate metabolism; Domain of unknown function; DUF; Glycoside hydrolase; Protein family; Protein function prediction

Indexed keywords

COPOLYMERIZATION; HYDROLASES; METABOLISM; PHYSIOLOGY; PLANTS (BOTANY); ENZYMES; PROTEINS; STRUCTURAL ANALYSIS; SUGARS;

3D STRUCTURE; CARBOHYDRATE METABOLISM; DUF; GLYCOSIDE HYDROLASES; PROTEIN FAMILY; PROTEIN FUNCTION PREDICTION;

PROTEINS; HYDROLASES;

BACTEROIDES; BACTEROIDES SP.; BACTEROIDES THETAIOTAOMICRON; BACTEROIDES THETAIOTAOMICRON VPI-5482;

BACTERIAL PROTEIN; GLYCOSIDASE;

AMINO ACID SEQUENCE; ARTICLE; BACTEROIDES; BIOLOGY; CHEMISTRY; ENZYMOLOGY; GASTROINTESTINAL TRACT; GENETICS; GENOMICS; HUMAN; MICROBIOLOGY; PROTEIN TERTIARY STRUCTURE;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BACTEROIDES; COMPUTATIONAL BIOLOGY; GASTROINTESTINAL TRACT; GENOMICS; GLYCOSIDE HYDROLASES; HUMANS; PROTEIN STRUCTURE, TERTIARY;

EID: 84901423167     PISSN: None     EISSN: 14712105     Source Type: Journal    
DOI: 10.1186/1471-2105-15-112     Document Type: Article

References (44)

1. Rosenstiel P. Stories of love and hate: innate immunity and host-microbe crosstalk in the intestine. Curr Opin Gastroenterol 2013, 29(2):125-132. 10.1097/MOG.0b013e32835da2c7, 23337934.
2. Tasse L, Bercovici J, Pizzut-Serin S, Robe P, Tap J, Klopp C, Cantarel BL, Coutinho PM, Henrissat B, Leclerc M, Doré J, Monsan P, Remaud-Simeon M, Potocki-Veronese G. Functional metagenomics to mine the human gut microbiome for dietary fiber catabolic enzymes. Genome Res 2010, 20(11):1605-1612. 10.1101/gr.108332.110, 2963823, 20841432.
3. Quiocho FA. Carbohydrate-binding proteins: tertiary structures and protein-sugar interactions. Annu Rev Biochem 1986, 55:287-315. 10.1146/annurev.bi.55.070186.001443, 3527044.
4. Xu J, Bjursell MK, Himrod J, Deng S, Carmichael LK, Chiang HC, Hooper LV, Gordon JI. A genomic view of the human-bacteroides thetaiotaomicron symbiosis. Science 2003, 299(5615):2074-2076. 10.1126/science.1080029, 12663928.
5. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 2009, 37(Database issue):D233-D238. 2686590, 18838391.
6. Henrissat B, Davies G. Structural and sequence-based classification of glycoside hydrolases. Curr Opin Struct Biol 1997, 7(5):637-644. 10.1016/S0959-440X(97)80072-3, 9345621.
7. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer EL, Eddy SR, Bateman A, Finn RD. The Pfam protein families database. Nucleic Acids Res 2012, 40(Database issue):D290-D301. 3245129, 22127870.
8. Bateman A, Coggill P, Finn RD. DUFs: families in search of function. Acta Crystallogr Sect F Struct Biol Cryst Commun 2010, 66(Pt 10):1148-1152. 2954198, 20944204.
9. Jaroszewski L, Li Z, Krishna SS, Bakolitsa C, Wooley J, Deacon AM, Wilson IA, Godzik A. Exploration of uncharted regions of the protein universe. PLoS Biol 2009, 7(9):e1000205. 10.1371/journal.pbio.1000205, 2744874, 19787035.
10. Chen VB, Arendall WB, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 2010, 66(Pt 1):12-21. 2803126, 20057044.
11. UniProt C. Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic acids research 2012, 40(Database issue):D71-75. 3245120, 22102590.
12. Dusko Ehrlich S. Meta HITc: [Metagenomics of the intestinal microbiota: potential applications]. Gastroenterol Clin Biol 2010, 34(Suppl 1):S23-S28.
13. Boraston AB, Bolam DN, Gilbert HJ, Davies GJ. Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 2004, 382(Pt 3):769-781. 1133952, 15214846.
14. Holm L, Sander C. Dali: a network tool for protein structure comparison. Trends Biochem Sci 1995, 20(11):478-480. 10.1016/S0968-0004(00)89105-7, 8578593.
15. Ye Y, Godzik A. Multiple flexible structure alignment using partial order graphs. Bioinformatics 2005, 21(10):2362-2369. 10.1093/bioinformatics/bti353, 15746292.
16. Jaroszewski L, Rychlewski L, Li Z, Li W, Godzik A. FFAS03: a server for profile--profile sequence alignments. Nucleic Acids Res 2005, 33(Web Server issue):W284-288. 1160179, 15980471.
17. Shallom D, Shoham Y. Microbial hemicellulases. Curr Opin Microbiol 2003, 6(3):219-228. 10.1016/S1369-5274(03)00056-0, 12831897.
18. Maksimainen M, Paavilainen S, Hakulinen N, Rouvinen J. Structural analysis, enzymatic characterization, and catalytic mechanisms of beta-galactosidase from Bacillus circulans sp. alkalophilus. FEBS J 2012, 279(10):1788-1798. 10.1111/j.1742-4658.2012.08555.x, 22385475.
19. Correia MA, Mazumder K, Bras JL, Firbank SJ, Zhu Y, Lewis RJ, York WS, Fontes CM, Gilbert HJ. Structure and function of an arabinoxylan-specific xylanase. J Biol Chem 2011, 286(25):22510-22520. 10.1074/jbc.M110.217315, 3121396, 21378160.
20. Santos CR, Polo CC, Correa JM, Simao Rde C, Seixas FA, Murakami MT. The accessory domain changes the accessibility and molecular topography of the catalytic interface in monomeric GH39 beta-xylosidases. Acta Crystallogr D Biol Crystallogr 2012, 68(Pt 10):1339-1345.
21. Dehal PS, Joachimiak MP, Price MN, Bates JT, Baumohl JK, Chivian D, Friedland GD, Huang KH, Keller K, Novichkov PS, Dubchak IL, Alm EJ, Arkin AP. MicrobesOnline: an integrated portal for comparative and functional genomics. Nucleic Acids Res 2010, 38(Database issue):D396-400. 2808868, 19906701.
22. Gotō M. Fundamentals of bacterial plant pathology 1992, San Diego: Academic Press.
23. Yin Y, Mao X, Yang J, Chen X, Mao F, Xu Y. dbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 2012, 40(Web Server issue):W445-451. 3394287, 22645317.
24. Elsliger MA, Deacon AM, Godzik A, Lesley SA, Wooley J, Wuthrich K, Wilson IA. The JCSG high-throughput structural biology pipeline. Acta Crystallogr Sect F Struct Biol Cryst Commun 2010, 66(Pt 10):1137-1142. 2954196, 20944202.
25. McPhillips TM, McPhillips SE, Chiu HJ, Cohen AE, Deacon AM, Ellis PJ, Garman E, Gonzalez A, Sauter NK, Phizackerley RP, Soltis SM, Kuhn P. Blu-Ice and the distributed control system: software for data acquisition and instrument control at macromolecular crystallography beamlines. J Synchrotron Radiat 2002, 9(Pt 6):401-406.
26. Battye TG, Kontogiannis L, Johnson O, Powell HR, Leslie AG. iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr D Biol Crystallogr 2011, 67(Pt 4):271-281. 3069742, 21460445.
27. The CCP4 suite Programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 1994, 50(Pt 5):760-763. The CCP4 suite.
28. Sheldrick GM. A short history of SHELX. Acta Crystallogr A 2008, 64(Pt 1):112-122.
29. Vonrhein C, Blanc E, Roversi P, Bricogne G. Automated structure solution with autoSHARP. Methods Mol Biol 2007, 364:215-230.
30. Langer G, Cohen SX, Lamzin VS, Perrakis A. Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat Protoc 2008, 3(7):1171-1179. 10.1038/nprot.2008.91, 2582149, 18600222.
31. Winn MD, Murshudov GN, Papiz MZ. Macromolecular TLS refinement in REFMAC at moderate resolutions. Methods Enzymol 2003, 374:300-321.
32. Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 2004, 60(Pt 12 Pt 1):2126-2132.
33. Diederichs K, Karplus PA. Improved R-factors for diffraction data analysis in macromolecular crystallography. Nat Struct Biol 1997, 4(4):269-275. 10.1038/nsb0497-269, 9095194.
34. Weiss MS, Hilgenfeld R. On the use of the merging R factor as a quality indicator for X-ray data. J Appl Crystallogr 1997, 30(2):203-205.
35. Weiss MS, Metzner HJ, Hilgenfeld R. Two non-proline cis peptide bonds may be important for factor XIII function. FEBS Lett 1998, 423(3):291-296. 10.1016/S0014-5793(98)00098-2, 9515726.
36. Cruickshank DW. Remarks about protein structure precision. Acta Crystallogr D Biol Crystallogr 1999, 55(Pt 3):583-601.
37. Katoh K, Kuma K, Toh H, Miyata T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic acids research 2005, 33(2):511-518. 10.1093/nar/gki198, 548345, 15661851.
38. DeLano W. The PyMOL Molecular Graphics System, Version 1.2r3pre 2002, DeLano Scientific: San Carlos, CA.
39. Gouet P, Courcelle E, Stuart DI, Metoz F. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 1999, 15(4):305-308. 10.1093/bioinformatics/15.4.305, 10320398.
40. Joosten RP, te Beek TA, Krieger E, Hekkelman ML, Hooft RW, Schneider R, Sander C, Vriend G. A series of PDB related databases for everyday needs. Nucleic Acids Res 2011, 39(Database issue):D411-419. 3013697, 21071423.
41. Desper R, Gascuel O. Fast and accurate phylogeny reconstruction algorithms based on the minimum-evolution principle. J Comput Biol 2002, 9(5):687-705. 10.1089/106652702761034136, 12487758.
42. Felsenstein J. PHYLIP - Phylogeny Inference Package (Version 3.2). Cladistics 1989, 5:164-166.
43. Schmidt HA, Strimmer K, Vingron M, von Haeseler A. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 2002, 18(3):502-504. 10.1093/bioinformatics/18.3.502, 11934758.
44. Han MV, Zmasek CM. phyloXML: XML for evolutionary biology and comparative genomics. BMC Bioinformatics 2009, 10:356. 10.1186/1471-2105-10-356, 2774328, 19860910.