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PMID: 19690172 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Genome scale reconstruction of a Salmonella metabolic model: comparison of similarity and differences with a commensal Escherichia coli strain.

The Journal of biological chemistry ·Vol. 284 ·No. 43 ·2009-10-23 ·Pages 29480-8

AbuOun M, Suthers PF, Jones GI, Carter BR, Saunders MP, Maranas CD, Woodward MJ, Anjum MF

Abstract

Salmonella are closely related to commensal Escherichia coli but have gained virulence factors enabling them to behave as enteric pathogens. Less well studied are the similarities and differences that exist between the metabolic properties of these organisms that may contribute toward niche adaptation of Salmonella pathogens. To address this, we have constructed a genome scale Salmonella metabolic model (iMA945). The model comprises 945 open reading frames or genes, 1964 reactions, and 1036 metabolites. There was significant overlap with genes present in E. coli MG1655 model iAF1260. In silico growth predictions were simulated using the model on different carbon, nitrogen, phosphorous, and sulfur sources. These were compared with substrate utilization data gathered from high throughput phenotyping microarrays revealing good agreement. Of the compounds tested, the majority were utilizable by both Salmonella and E. coli. Nevertheless a number of differences were identified both between Salmonella and E. coli and also within the Salmonella strains included. These differences provide valuable insight into differences between a commensal and a closely related pathogen and within different pathogenic strains opening new avenues for future explorations.

MeSH Terms
Escherichia coli/genetics,metabolism Genome, Bacterial/physiology Models, Biological Oligonucleotide Array Sequence Analysis Open Reading Frames/physiology Salmonella enteritidis/genetics,metabolism Salmonella typhimurium/genetics,metabolism Species Specificity
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
AbuOun Manal
Department of Food and Environmental Safety, Veterinary Laboratories Agency (Weybridge), Addlestone, Surrey KT153NB, United Kingdom. m.abuoun@vla.defra.gsi.gov.uk
Suthers Patrick F
Jones Gareth I
Carter Ben R
Saunders Mark P
Maranas Costas D
Woodward Martin J
Anjum Muna F
References (73)
73 references, click to expand
  1. Determining divergence times of the major kingdoms of living organisms with a protein clock.
    Science. 1996 Jan 26;271(5248):470-7 PMID: 8560259
  2. Systems approach to refining genome annotation.
    Proc Natl Acad Sci U S A. 2006 Nov 14;103(46):17480-4 PMID: 17088549
  3. The growing scope of applications of genome-scale metabolic reconstructions using Escherichia coli.
    Nat Biotechnol. 2008 Jun;26(6):659-67 PMID: 18536691
  4. Metabolic flux distributions in Corynebacterium glutamicum during growth and lysine overproduction.
    Biotechnol Bioeng. 1993 Mar 15;41(6):633-46 PMID: 18609599
  5. Constraint-based analysis of metabolic capacity of Salmonella typhimurium during host-pathogen interaction.
    BMC Syst Biol. 2009 Apr 08;3:38 PMID: 19356237
  6. The alternative electron acceptor tetrathionate supports B12-dependent anaerobic growth of Salmonella enterica serovar typhimurium on ethanolamine or 1,2-propanediol.
    J Bacteriol. 2001 Apr;183(8):2463-75 PMID: 11274105
  7. Infection of laying hens with Salmonella enteritidis PT4 by conjunctival challenge.
    Vet Rec. 1992 Oct 24;131(17):386-8 PMID: 1455584
  8. Characterization of the multiple catalytic activities of tartrate dehydrogenase.
    Biochemistry. 1990 Feb 20;29(7):1749-56 PMID: 2184888
  9. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2.
    Nature. 2001 Oct 25;413(6858):852-6 PMID: 11677609
  10. Hexose/Pentose and Hexitol/Pentitol Metabolism.
    EcoSal Plus. 2005 Nov;1(2): PMID: 26443516
  11. Physiological and genetic regulation of the aldohexuronate transport system in Escherichia coli.
    J Bacteriol. 1976 Aug;127(2):706-18 PMID: 783117
  12. Genome-scale reconstruction and analysis of the Pseudomonas putida KT2440 metabolic network facilitates applications in biotechnology.
    PLoS Comput Biol. 2008 Oct;4(10):e1000210 PMID: 18974823
  13. Comparison of the Escherichia coli K-12 genome with sampled genomes of a Klebsiella pneumoniae and three salmonella enterica serovars, Typhimurium, Typhi and Paratyphi.
    Nucleic Acids Res. 2000 Dec 15;28(24):4974-86 PMID: 11121489
  14. The COG database: an updated version includes eukaryotes.
    BMC Bioinformatics. 2003 Sep 11;4:41 PMID: 12969510
  15. The Tricarballylate utilization (tcuRABC) genes of Salmonella enterica serovar Typhimurium LT2.
    J Bacteriol. 2004 Mar;186(6):1629-37 PMID: 14996793
  16. Molecular characterization of the 4-hydroxyphenylacetate catabolic pathway of Escherichia coli W: engineering a mobile aromatic degradative cluster.
    J Bacteriol. 1996 Jan;178(1):111-20 PMID: 8550403
  17. Biodegradation of aromatic compounds by Escherichia coli.
    Microbiol Mol Biol Rev. 2001 Dec;65(4):523-69, table of contents PMID: 11729263
  18. The complete genome sequence of Escherichia coli K-12.
    Science. 1997 Sep 5;277(5331):1453-62 PMID: 9278503
  19. International increase in Salmonella enteritidis: a new pandemic?
    Epidemiol Infect. 1990 Aug;105(1):21-7 PMID: 2200698
  20. Complete nucleotide sequence of a 43-kilobase genomic island associated with the multidrug resistance region of Salmonella enterica serovar Typhimurium DT104 and its identification in phage type DT120 and serovar Agona.
    J Bacteriol. 2001 Oct;183(19):5725-32 PMID: 11544236
  21. Towards multidimensional genome annotation.
    Nat Rev Genet. 2006 Feb;7(2):130-41 PMID: 16418748
  22. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection.
    Mol Syst Biol. 2006;2:2006.0008 PMID: 16738554
  23. 2-Phenylethylamine catabolism by Escherichia coli K12.
    J Gen Microbiol. 1987 Feb;133(2):347-51 PMID: 3309152
  24. Genetic control of histidine degradation in Salmonella typhimurium, strain LT-2.
    J Biol Chem. 1969 Oct 10;244(19):5382-91 PMID: 4899017
  25. A genome-scale metabolic reconstruction for Escherichia coli K-12 MG1655 that accounts for 1260 ORFs and thermodynamic information.
    Mol Syst Biol. 2007;3:121 PMID: 17593909
  26. Evolution of a second gene for beta-galactosidase in Escherichia coli.
    Proc Natl Acad Sci U S A. 1973 Jun;70(6):1841-5 PMID: 4124306
  27. The D-allose operon of Escherichia coli K-12.
    J Bacteriol. 1997 Dec;179(24):7631-7 PMID: 9401019
  28. Identification of core and variable components of the Salmonella enterica subspecies I genome by microarray.
    Infect Immun. 2005 Dec;73(12):7894-905 PMID: 16299280
  29. Characterization of Salmonella enterica subspecies I genovars by use of microarrays.
    J Bacteriol. 2004 Sep;186(17):5883-98 PMID: 15317794
  30. The control region of the pdu/cob regulon in Salmonella typhimurium.
    J Bacteriol. 1994 Sep;176(17):5474-82 PMID: 8071226
  31. Regulation of newly evolved enzymes. IV. Directed evolution of the Ebg repressor.
    Genetics. 1978 Dec;90(4):673-81 PMID: 105963
  32. Identification of putative ancestors of the multidrug-resistant Salmonella enterica serovar typhimurium DT104 clone harboring the Salmonella genomic island 1.
    Arch Microbiol. 2007 May;187(5):415-24 PMID: 17180672
  33. Evidence for transcription antitermination control of tryptophanase operon expression in Escherichia coli K-12.
    J Bacteriol. 1985 Nov;164(2):731-40 PMID: 3902796
  34. Global phenotypic characterization of bacteria.
    FEMS Microbiol Rev. 2009 Jan;33(1):191-205 PMID: 19054113
  35. The Salmonella genomic island 1 is an integrative mobilizable element.
    Mol Microbiol. 2005 Mar;55(6):1911-24 PMID: 15752209
  36. Regulation of expression of the 2-deoxy-D-ribose utilization regulon, deoQKPX, from Salmonella enterica serovar typhimurium.
    J Bacteriol. 2003 Oct;185(20):6042-50 PMID: 14526015
  37. Optimization based automated curation of metabolic reconstructions.
    BMC Bioinformatics. 2007 Jun 20;8:212 PMID: 17584497
  38. Citrate utilization by Escherichia coli: plasmid- and chromosome-encoded systems.
    J Bacteriol. 1983 Dec;156(3):1019-24 PMID: 6358185
  39. Sulfonate-sulfur metabolism and its regulation in Escherichia coli.
    Arch Microbiol. 2001 Jul;176(1-2):1-8 PMID: 11479697
  40. A new gene, cbl, encoding a member of the LysR family of transcriptional regulators belongs to Escherichia coli cys regulon.
    Gene. 1995 Dec 1;166(1):11-7 PMID: 8529872
  41. Comparison of sample sequences of the Salmonella typhi genome to the sequence of the complete Escherichia coli K-12 genome.
    Infect Immun. 1998 Sep;66(9):4305-12 PMID: 9712782
  42. Experimental and computational assessment of conditionally essential genes in Escherichia coli.
    J Bacteriol. 2006 Dec;188(23):8259-71 PMID: 17012394
  43. Genetic and metabolic control of enzymes responsible for histidine degradation in Salmonella typhimurium. 4-imidazolone-5-propionate amidohydrolase and N-formimino-L-glutamate formiminohydrolase.
    J Biol Chem. 1971 May 25;246(10):3320-9 PMID: 4930059
  44. Genotypic exclusion: a novel relationship between the ribitol-arabitol and galactitol genes of E. coli.
    Mol Gen Genet. 1983;189(2):337-9 PMID: 6343795
  45. Genetics of the glutamine transport system in Escherichia coli.
    J Bacteriol. 1981 Sep;147(3):805-19 PMID: 6115851
  46. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18.
    Nature. 2001 Oct 25;413(6858):848-52 PMID: 11677608
  47. Polymorphism in Escherichia coli: rtl atl and gat regions behave as chromosomal alternatives.
    J Gen Microbiol. 1983 Jan;129(1):75-84 PMID: 6339679
  48. Genomic comparison of Salmonella enterica serovars and Salmonella bongori by use of an S. enterica serovar typhimurium DNA microarray.
    J Bacteriol. 2003 Jan;185(2):553-63 PMID: 12511502
  49. Molecular relationships among the Salmonelleae.
    J Bacteriol. 1973 Jul;115(1):307-15 PMID: 4717519
  50. Salmonella: a model for bacterial pathogenesis.
    Annu Rev Med. 2001;52:259-74 PMID: 11160778
  51. The MetaCyc Database of metabolic pathways and enzymes and the BioCyc collection of Pathway/Genome Databases.
    Nucleic Acids Res. 2008 Jan;36(Database issue):D623-31 PMID: 17965431
  52. Mutations affecting a regulated, membrane-associated esterase in Salmonella typhimurium LT2.
    Mol Gen Genet. 1994 Jun 15;243(6):674-80 PMID: 8028584
  53. Increasing incidence of resistance to trimethoprim and ciprofloxacin in epidemic Salmonella typhimurium DT104 in England and Wales.
    Euro Surveill. 1997 Nov;2(11):81-84 PMID: 12631789
  54. D-Allose catabolism of Escherichia coli: involvement of alsI and regulation of als regulon expression by allose and ribose.
    J Bacteriol. 1999 Nov;181(22):7126-30 PMID: 10559180
  55. Catabolism of 3- and 4-hydroxyphenylacetate by the 3,4-dihydroxyphenylacetate pathway in Escherichia coli.
    J Bacteriol. 1980 Jul;143(1):302-6 PMID: 6995433
  56. GrowMatch: an automated method for reconciling in silico/in vivo growth predictions.
    PLoS Comput Biol. 2009 Mar;5(3):e1000308 PMID: 19282964
  57. Phenotype microarray analysis of Escherichia coli K-12 mutants with deletions of all two-component systems.
    J Bacteriol. 2003 Aug;185(16):4956-72 PMID: 12897016
  58. KEGG for linking genomes to life and the environment.
    Nucleic Acids Res. 2008 Jan;36(Database issue):D480-4 PMID: 18077471
  59. The apeE gene of Salmonella typhimurium encodes an outer membrane esterase not present in Escherichia coli.
    J Bacteriol. 1998 Jul;180(14):3517-21 PMID: 9657991
  60. An expanded genome-scale model of Escherichia coli K-12 (iJR904 GSM/GPR).
    Genome Biol. 2003;4(9):R54 PMID: 12952533
  61. Phenotype microarrays for high-throughput phenotypic testing and assay of gene function.
    Genome Res. 2001 Jul;11(7):1246-55 PMID: 11435407
  62. The Escherichia coli ssuEADCB gene cluster is required for the utilization of sulfur from aliphatic sulfonates and is regulated by the transcriptional activator Cbl.
    J Biol Chem. 1999 Oct 8;274(41):29358-65 PMID: 10506196
  63. maoB, a gene that encodes a positive regulator of the monoamine oxidase gene (maoA) in Escherichia coli.
    J Bacteriol. 1996 May;178(10):2941-7 PMID: 8631685
  64. Convergent pathways for utilization of the amino sugars N-acetylglucosamine, N-acetylmannosamine, and N-acetylneuraminic acid by Escherichia coli.
    J Bacteriol. 1999 Jan;181(1):47-54 PMID: 9864311
  65. Identification of sulfate starvation-regulated genes in Escherichia coli: a gene cluster involved in the utilization of taurine as a sulfur source.
    J Bacteriol. 1996 Sep;178(18):5438-46 PMID: 8808933
  66. Efflux of choline and glycine betaine from osmoregulating cells of Escherichia coli.
    FEMS Microbiol Lett. 1992 Sep 15;75(2-3):149-54 PMID: 1398030
  67. The nac (nitrogen assimilation control) gene from Escherichia coli.
    J Bacteriol. 1998 Mar;180(5):1166-73 PMID: 9495755
  68. Characterization of alpha-ketoglutarate-dependent taurine dioxygenase from Escherichia coli.
    J Biol Chem. 1997 Sep 12;272(37):23031-6 PMID: 9287300
  69. A genome-scale metabolic reconstruction of Mycoplasma genitalium, iPS189.
    PLoS Comput Biol. 2009 Feb;5(2):e1000285 PMID: 19214212
  70. Modelling strategies for the industrial exploitation of lactic acid bacteria.
    Nat Rev Microbiol. 2006 Jan;4(1):46-56 PMID: 16357860
  71. Regulation of the ansB gene of Salmonella enterica.
    Mol Microbiol. 1993 Jul;9(1):165-72 PMID: 8412661
  72. Integrating high-throughput and computational data elucidates bacterial networks.
    Nature. 2004 May 6;429(6987):92-6 PMID: 15129285
  73. Lateral gene transfer and the nature of bacterial innovation.
    Nature. 2000 May 18;405(6784):299-304 PMID: 10830951
Article Info
Journal
The Journal of biological chemistry
Abbr.
J Biol Chem
ISSN
1083-351X
Published
2009-10-23
Epub
2009-00-18
Pages
29480-8
Language
English
Region
United States
NLM ID
2985121R
PMCID
PMC2785581
Subset
IM
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