Polysaccharides utilization in human gut bacterium Bacteroides thetaiotaomicron: Comparative genomics reconstruction of metabolic and regulatory networks

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Ravcheev, Dmitry A ^a,b   Godzik, Adam ^a   Osterman, Andrei L ^a   Rodionov, Dmitry A ^a,b  

^a BURNHAM INSTITUTE   (United States)

^b INSTITUTE FOR INFORMATION TRANSMISSION PROBLEMS   (Russian Federation)

Author keywords

BACTEROIDES; Carbohydrate utilization; Regulatory network; Regulon; Transcription factor

Indexed keywords

BACTERIAL POLYSACCHARIDE; CARBOHYDRATE; CYTARABINE; ENZYME; GLYCAN; MONOSACCHARIDE; TRANSCRIPTION FACTOR;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTEROIDES; BACTEROIDES THETAIOTAOMICRON; BIOINFORMATICS; CARBOHYDRATE METABOLISM; CARBOHYDRATE TRANSPORT; COMPARATIVE GENOMIC HYBRIDIZATION; COMPARATIVE STUDY; DNA BINDING MOTIF; DNA FOOTPRINTING; DNA STRUCTURE; ENZYME ACTIVITY; FUNCTIONAL GENOMICS; GENE REGULATORY NETWORK; GENE SEQUENCE; GENE STRUCTURE; GENETIC CONSERVATION; GENETIC LINE; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; HUMAN; INTESTINE; MOLECULAR GENETICS; NONHUMAN; NUCLEOTIDE REPEAT; PROMOTER REGION; PROTEIN FUNCTION; REGULATOR GENE; REGULON; TRANSCRIPTION REGULATION; TWO HYBRID SYSTEM;

BACTERIA (MICROORGANISMS); BACTEROIDES; BACTEROIDES THETAIOTAOMICRON;

BACTERIAL PROTEINS; BACTEROIDES; BASE SEQUENCE; BINDING SITES; GASTROINTESTINAL TRACT; GENE EXPRESSION REGULATION, BACTERIAL; GENE REGULATORY NETWORKS; GENOMICS; HUMANS; METABOLIC NETWORKS AND PATHWAYS; NUCLEOTIDE MOTIFS; PHYLOGENY; POLYSACCHARIDES; POSITION-SPECIFIC SCORING MATRICES; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

EID: 84889976808     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-873     Document Type: Article

References (67)

1. Kinross JM, Darzi AW, Nicholson JK. Gut microbiome-host interactions in health and disease. Genome Med 2011, 3(3):14.
2. Koropatkin NM, Cameron EA, Martens EC. How glycan metabolism shapes the human gut microbiota. Nat Rev Microbiol 2012, 10(5):323-335.
3. Round JL, Mazmanian SK. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 2009, 9(5):313-323.
4. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA. Diversity of the human intestinal microbial flora. Science 2005, 308(5728):1635-1638.
5. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, Fernandes GR, Tap J, Bruls T, Batto JM, et al. Enterotypes of the human gut microbiome. Nature 2011, 473(7346):174-180.
6. Kurokawa K, Itoh T, Kuwahara T, Oshima K, Toh H, Toyoda A, Takami H, Morita H, Sharma VK, Srivastava TP, et al. Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes. DNA Res 2007, 14(4):169-181.
7. Hooper LV, Midtvedt T, Gordon JI. How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr 2002, 22:283-307.
8. 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.
9. Sonnenburg ED, Zheng H, Joglekar P, Higginbottom SK, Firbank SJ, Bolam DN, Sonnenburg JL. Specificity of polysaccharide use in intestinal bacteroides species determines diet-induced microbiota alterations. Cell 2010, 141(7):1241-1252.
10. Heinken A, Sahoo S, Fleming RM, Thiele I. Systems-level characterization of a host-microbe metabolic symbiosis in the mammalian gut. Gut Microbes 2013, 4(1):28-40.
11. 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.
12. D'Elia JN, Salyers AA. Effect of regulatory protein levels on utilization of starch by Bacteroides thetaiotaomicron. J Bacteriol 1996, 178(24):7180-7186.
13. Bolam DN, Koropatkin NM. Glycan recognition by the bacteroidetes Sus-like systems. Curr Opin Struct Biol 2012, 22(5):563-569.
14. Martens EC, Roth R, Heuser JE, Gordon JI. Coordinate regulation of glycan degradation and polysaccharide capsule biosynthesis by a prominent human gut symbiont. J Biol Chem 2009, 284(27):18445-18457.
15. Lowe EC, Basle A, Czjzek M, Firbank SJ, Bolam DN. A scissor blade-like closing mechanism implicated in transmembrane signaling in a Bacteroides hybrid two-component system. Proc Natl Acad Sci USA 2012, 109(19):7298-7303.
16. Martens EC, Koropatkin NM, Smith TJ, Gordon JI. Complex glycan catabolism by the human gut microbiota: the Bacteroidetes Sus-like paradigm. J Biol Chem 2009, 284(37):24673-24677.
17. Xu J, Chiang HC, Bjursell MK, Gordon JI. Message from a human gut symbiont: sensitivity is a prerequisite for sharing. Trends Microbiol 2004, 12(1):21-28.
18. Martens EC, Chiang HC, Gordon JI. Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe 2008, 4(5):447-457.
19. Fischbach MA, Sonnenburg JL. Eating for two: how metabolism establishes interspecies interactions in the gut. Cell Host Microbe 2011, 10(4):336-347.
20. Leyn SA, Kazanov MD, Sernova NV, Ermakova EO, Novichkov PS, Rodionov DA. Genomic reconstruction of the transcriptional regulatory network in Bacillus subtilis. J Bacteriol 2013, 195(11):2463-2473.
21. Ravcheev DA, Best AA, Sernova NV, Kazanov MD, Novichkov PS, Rodionov DA. Genomic reconstruction of transcriptional regulatory networks in lactic acid bacteria. BMC Genomics 2013, 14(1):94.
22. Ravcheev DA, Best AA, Tintle N, Dejongh M, Osterman AL, Novichkov PS, Rodionov DA. Inference of the transcriptional regulatory network in Staphylococcus aureus by integration of experimental and genomics-based evidence. J Bacteriol 2011, 193(13):3228-3240.
23. Rodionov DA, Novichkov PS, Stavrovskaya ED, Rodionova IA, Li X, Kazanov MD, Ravcheev DA, Gerasimova AV, Kazakov AE, Kovaleva GY, et al. Comparative genomic reconstruction of transcriptional networks controlling central metabolism in the Shewanella genus. BMC Genomics 2011, 12(Suppl 1):S3.
24. Rodionov DA, Rodionova IA, Li X, Ravcheev DA, Tarasova Y, Portnoy VA, Zengler K, Osterman AL. Transcriptional regulation of the carbohydrate utilization network in Thermotoga maritima. Front Microbiol 2013, 4:244.
25. Rodionov DA, Li X, Rodionova IA, Yang C, Sorci L, Dervyn E, Martynowski D, Zhang H, Gelfand MS, Osterman AL. Transcriptional regulation of NAD metabolism in bacteria: genomic reconstruction of NiaR (YrxA) regulon. Nucleic Acids Res 2008, 36(6):2032-2046.
26. Rodionov DA, Mironov AA, Rakhmaninova AB, Gelfand MS. Transcriptional regulation of transport and utilization systems for hexuronides, hexuronates and hexonates in gamma purple bacteria. Mol Microbiol 2000, 38(4):673-683.
27. Rodionov DA. Comparative genomic reconstruction of transcriptional regulatory networks in bacteria. Chem Rev 2007, 107(8):3467-3497.
28. Martens EC, Lowe EC, Chiang H, Pudlo NA, Wu M, McNulty NP, Abbott DW, Henrissat B, Gilbert HJ, Bolam DN, et al. Recognition and degradation of plant cell wall polysaccharides by two human gut symbionts. PLoS Biol 2011, 9(12):e1001221.
29. Rogers TE, Pudlo NA, Koropatkin NM, Bell JS, Moya Balasch M, Jasker K, Martens EC. Dynamic responses of Bacteroides thetaiotaomicron during growth on glycan mixtures. Mol Microbiol 2013, 88(5):876-890.
30. Sonnenburg ED, Sonnenburg JL, Manchester JK, Hansen EE, Chiang HC, Gordon JI. A hybrid two-component system protein of a prominent human gut symbiont couples glycan sensing in vivo to carbohydrate metabolism. Proc Natl Acad Sci USA 2006, 103(23):8834-8839.
31. Kazanov MD, Li X, Gelfand MS, Osterman AL, Rodionov DA. Functional diversification of ROK-family transcriptional regulators of sugar catabolism in the Thermotogae phylum. Nucleic Acids Res 2013, 41(2):790-803.
32. Leyn SA, Li X, Zheng Q, Novichkov PS, Reed S, Romine MF, Fredrickson JK, Yang C, Osterman AL, Rodionov DA. Control of Proteobacterial central carbon metabolism by the HexR transcriptional regulator: a case study in Shewanella oneidensis. J Biol Chem 2011, 286(41):35782-35794.
33. Ravcheev DA, Li X, Latif H, Zengler K, Leyn SA, Korostelev YD, Kazakov AE, Novichkov PS, Osterman AL, Rodionov DA. Transcriptional regulation of central carbon and energy metabolism in bacteria by redox responsive repressor Rex. J Bacteriol 2012, 194(5):1145-1157.
34. Novichkov PS, Kazakov AE, Ravcheev DA, Leyn SA, Kovaleva GY, Sutormin RA, Kazanov MD, Riehl W, Arkin AP, Dubchak I, et al. RegPrecise 3.0-a resource for genome-scale exploration of transcriptional regulation in Bacteria. BMC Genomics 2013, 14:745.
35. 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(7):e156.
36. Kleene R, Schachner M. Glycans and neural cell interactions. Nat Rev Neurosci 2004, 5(3):195-208.
37. Abbott DW, Boraston AB. Structural biology of pectin degradation by Enterobacteriaceae. Microbiol Mol Biol Rev 2008, 72(2):301-316. table of contents.
38. Willats WG, McCartney L, Mackie W, Knox JP. Pectin: cell biology and prospects for functional analysis. Plant Mol Biol 2001, 47(1-2):9-27.
39. Patel EH, Paul LV, Casanueva AI, Patrick S, Abratt VR. Overexpression of the rhamnose catabolism regulatory protein, RhaR: a novel mechanism for metronidazole resistance in Bacteroides thetaiotaomicron. J Antimicrob Chemother 2009, 64(2):267-273.
40. Patel EH, Paul LV, Patrick S, Abratt VR. Rhamnose catabolism in Bacteroides thetaiotaomicron is controlled by the positive transcriptional regulator RhaR. Res Microbiol 2008, 159(9-10):678-684.
41. Hooper LV, Xu J, Falk PG, Midtvedt T, Gordon JI. A molecular sensor that allows a gut commensal to control its nutrient foundation in a competitive ecosystem. Proc Natl Acad Sci USA 1999, 96(17):9833-9838.
42. Disz T, Akhter S, Cuevas D, Olson R, Overbeek R, Vonstein V, Stevens R, Edwards RA. Accessing the SEED genome databases via Web services API: tools for programmers. BMC Bioinforma 2010, 11:319.
43. Overbeek R, Begley T, Butler RM, Choudhuri JV, Chuang HY, Cohoon M, de Crecy-Lagard V, Diaz N, Disz T, Edwards R, et al. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res 2005, 33(17):5691-5702.
44. Kanehisa M, Goto S, Hattori M, Aoki-Kinoshita KF, Itoh M, Kawashima S, Katayama T, Araki M, Hirakawa M. From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res 2006, 34:D354-D357.
45. Kanehisa M, Goto S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 2000, 28(1):27-30.
46. Conejo MS, Thompson SM, Miller BG. Evolutionary bases of carbohydrate recognition and substrate discrimination in the ROK protein family. J Mol Evol 2010, 70(6):545-556.
47. Hoskisson PA, Rigali S. Chapter 1: variation in form and function the helix-turn-helix regulators of the GntR superfamily. Adv Appl Microbiol 2009, 69:1-22.
48. Swint-Kruse L, Matthews KS. Allostery in the LacI/GalR family: variations on a theme. Curr Opin Microbiol 2009, 12(2):129-137.
49. Yang J, Tauschek M, Robins-Browne RM. Control of bacterial virulence by AraC-like regulators that respond to chemical signals. Trends Microbiol 2011, 19(3):128-135.
50. Rodionov DA, De Ingeniis J, Mancini C, Cimadamore F, Zhang H, Osterman AL, Raffaelli N. Transcriptional regulation of NAD metabolism in bacteria: NrtR family of Nudix-related regulators. Nucleic Acids Res 2008, 36(6):2047-2059.
51. Teramoto H, Suda M, Inui M, Yukawa H. Regulation of the expression of genes involved in NAD de novo biosynthesis in Corynebacterium glutamicum. Appl Environ Microbiol 2010, 76(16):5488-5495.
52. Grainger DC, Hurd D, Harrison M, Holdstock J, Busby SJ. Studies of the distribution of Escherichia coli cAMP-receptor protein and RNA polymerase along the E. coli chromosome. Proc Natl Acad Sci USA 2005, 102(49):17693-17698.
53. Devoid S, Overbeek R, DeJongh M, Vonstein V, Best AA, Henry C. Automated genome annotation and metabolic model reconstruction in the SEED and Model SEED. Methods Mol Biol 2013, 985:17-45. PubMed PMID: 23417797.
54. Dehal PS, Joachimiak MP, Price MN, Bates JT, Baumohl JK, Chivian D, Friedland GD, Huang KH, Keller K, Novichkov PS, et al. MicrobesOnline: an integrated portal for comparative and functional genomics. Nucleic Acids Res 2010, 38:D396-D400.
55. Kazakov AE, Rodionov DA, Alm E, Arkin AP, Dubchak I, Gelfand MS. Comparative genomics of regulation of fatty acid and branched-chain amino acid utilization in proteobacteria. J Bacteriol 2009, 191(1):52-64.
56. McCue L, Thompson W, Carmack C, Ryan MP, Liu JS, Derbyshire V, Lawrence CE. Phylogenetic footprinting of transcription factor binding sites in proteobacterial genomes. Nucleic Acids Res 2001, 29(3):774-782.
57. Shelton DA, Stegman L, Hardison R, Miller W, Bock JH, Slightom JL, Goodman M, Gumucio DL. Phylogenetic footprinting of hypersensitive site 3 of the beta-globin locus control region. Blood 1997, 89(9):3457-3469.
58. Mironov AA, Vinokurova NP, Gel'fand MS. Software for analyzing bacterial genomes. Mol Biol (Mosk) 2000, 34(2):253-262.
59. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32(5):1792-1797.
60. Felsenstein J. Inferring phylogenies from protein sequences by parsimony, distance, and likelihood methods. Meth Enzymol 1996, 266:418-427.
61. Huson DH, Richter DC, Rausch C, Dezulian T, Franz M, Rupp R. Dendroscope: an interactive viewer for large phylogenetic trees. BMC Bioinforma 2007, 8:460.
62. Gupta S, Stamatoyannopoulos JA, Bailey TL, Noble WS. Quantifying similarity between motifs. Genome Biol 2007, 8(2):R24.
63. Seo J, Gordish-Dressman H. Exploratory data analysis with categorical variables: an improved rank-by-feature framework and a case study. Int J Hum-Comp Interact 2007, 23(3):287-314.
64. Novichkov PS, Rodionov DA, Stavrovskaya ED, Novichkova ES, Kazakov AE, Gelfand MS, Arkin AP, Mironov AA, Dubchak I. RegPredict: an integrated system for regulon inference in prokaryotes by comparative genomics approach. Nucleic Acids Res 2010, 38:W299-W307.
65. Crooks GE, Hon G, Chandonia JM, Brenner SE. WebLogo: a sequence logo generator. Genome Res 2004, 14(6):1188-1190.
66. Magrane M, Consortium U. UniProt knowledgebase: a hub of integrated protein data. Database (Oxford) 2011, 2011:bar009.
67. Magnus M, Pawlowski M, Bujnicki JM. MetaLocGramN: a meta-predictor of protein subcellular localization for Gram-negative bacteria. Biochim Biophys Acta 2012, 1824(12):1425-1433.