Salmonella utilizes D-glucosaminate via a mannose family phosphotransferase system permease and associated enzymes

Journal of Bacteriology

Volumn 195, Issue 18, 2013, Pages 4057-4066

  Miller, Katherine A ^a   Phillips, Robert S ^a   Mrázek, Jan ^a   Hoover, Timothy R ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 KETO 3 DEOXYGLUCONATE 6 PHOSPHATE; FRUCTOSE BISPHOSPHATE ALDOLASE; GLUCONIC ACID; GLUCOSAMINATE; GLUCOSE; GLYCERALDEHYDE 3 PHOSPHATE; MANNOSE; NITROGEN; PERMEASE; PHOSPHATE; PHOSPHOTRANSFERASE; PYRUVIC ACID; SIGMA FACTOR RPON; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; CARBON SOURCE; CELL MEMBRANE; CITROBACTER; DNA BASE COMPOSITION; ENTEROBACTER; ESCHERICHIA; ESCHERICHIA COLI; GAMMAPROTEOBACTERIA; GENETIC TRANSCRIPTION; HAFNIA; KLEBSIELLA; LACTOBACILLUS RHAMNOSUS; NONHUMAN; OPERON; PHYLOGENY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PHOSPHORYLATION; PROTEOBACTERIA; SALMONELLA; SALMONELLA TYPHIMURIUM; WILD TYPE;

BACTERIAL PROTEINS; CULTURE MEDIA; GENE EXPRESSION REGULATION, BACTERIAL; GLUCONATES; GLUCOSAMINE; MANNOSE; MEMBRANE TRANSPORT PROTEINS; OPERON; PHOSPHOENOLPYRUVATE SUGAR PHOSPHOTRANSFERASE SYSTEM; PHOSPHORYLATION; SALMONELLA TYPHIMURIUM;

EID: 84883275966     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00290-13     Document Type: Article

References (69)

1. Jones TF, Ingram LA, Cieslak PR, Vugia DJ, Tobin-D'Angelo M, Hurd S, Medus C, Cronquist A, Angulo FJ. 2008. Salmonellosis outcomes differ substantially by serotype. J. Infect. Dis. 198:109-114.
2. Figueira R, Holden DW. 2012. Functions of the Salmonella pathogenicity island 2 (SPI-2) type III secretion system effectors. Microbiology 158: 1147-1161.
3. Marcus SL, Brumell JH, Pfeifer CG, Finlay BB. 2000. Salmonella pathogenicity islands: big virulence in small packages. Microbes Infect. 2:145-156.
4. Que F, Wu S, Huang R. 2013. Salmonella pathogenicity island 1 (SPI-1) at work. Curr. Microbiol. 66:582-587.
5. Wagner C, Hensel M. 2011. Adhesive mechanisms of Salmonella enterica. Adv. Exp. Med. Biol. 715:17-34.
6. van Asten AJ, van Dijk JE. 2005. Distribution of "classic" virulence factors among Salmonella spp. FEMS Immunol. Med. Microbiol. 44:251-259.
7. Bumann D. 2009. System-level analysis of Salmonella metabolism during infection. Curr. Opin. Microbiol. 12:559-567.
8. Poncet S, Milohanic E, Maze A, Nait Abdallah J, Ake F, Larribe M, Deghmane AE, Taha MK, Dozot M, De Bolle X, Letesson JJ, Deutscher J. 2009. Correlations between carbon metabolism and virulence in bacteria. Contrib. Microbiol. 16:88-102.
9. AbuOun M, Suthers PF, Jones GI, Carter BR, Saunders MP, Maranas CD, Woodward MJ, Anjum MF. 2009. Genome scale reconstruction of a Salmonella metabolic model: comparison of similarity and differences with a commensal Escherichia coli strain. J. Biol. Chem. 284:29480-29488.
10. Adkins JN, Mottaz HM, Norbeck AD, Gustin JK, Rue J, Clauss TR, Purvine SO, Rodland KD, Heffron F, Smith RD. 2006. Analysis of the Salmonella typhimurium proteome through environmental response toward infectious conditions. Mol. Cell. Proteomics 5:1450-1461.
11. Holzer SU, Hensel M. 2012. Divergent roles of Salmonella pathogenicity island 2 and metabolic traits during interaction of S. enterica serovar Typhimurium with host cells. PLoS One 7:e33220.
12. Kim YM, Schmidt BJ, Kidwai AS, Jones MB, Deatherage Kaiser BL, Brewer HM, Mitchell HD, Palsson BO, McDermott JE, Heffron F, Smith RD, Peterson SN, Ansong C, Hyduke DR, Metz TO, Adkins JN. 2013. Salmonella modulates metabolism during growth under conditions that induce expression of virulence genes. Mol. Biosyst. 9:1522-1534.
13. Raghunathan A, Reed J, Shin S, Palsson B, Daefler S. 2009. Constraintbased analysis of metabolic capacity of Salmonella typhimurium during host-pathogen interaction. BMC Syst. Biol. 3:38.
14. Gutnick D, Calvo JM, Klopotowski T, Ames BN. 1969. Compounds which serve as the sole source of carbon or nitrogen for Salmonella typhimurium LT-2. J. Bacteriol. 100:215-219.
15. Jarvik T, Smillie C, Groisman EA, Ochman H. 2010. Short-term signatures of evolutionary change in the Salmonella enterica serovar Typhimurium 14028 genome. J. Bacteriol. 192:560-567.
16. Shakeri-Garakani A, Brinkkotter A, Schmid K, Turgut S, Lengeler JW. 2004. The genes and enzymes for the catabolism of galactitol, D-tagatose, and related carbohydrates in Klebsiella oxytoca M5a1 and other enteric bacteria display convergent evolution. Mol. Genet. Genomics 271:717-728.
17. Deutscher J, Francke C, Postma PW. 2006. How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol. Mol. Biol. Rev. 70:939-1031.
18. Erni B, Zanolari B, Graff P, Kocher HP. 1989. Mannose permease of Escherichia coli. Domain structure and function of the phosphorylating subunit. J. Biol. Chem. 264:18733-18741.
19. Erni B, Zanolari B, Kocher HP. 1987. The mannose permease of Escherichia coli consists of three different proteins. Amino acid sequence and function in sugar transport, sugar phosphorylation, and penetration of phage lambda DNA. J. Biol. Chem. 262:5238-5247.
20. Postma PW, Lengeler JW, Jacobson GR. 1993. Phosphoenolpyruvate: carbohydrate phosphotransferase systems of bacteria. Microbiol. Rev. 57: 543-594.
21. Erni B, Zanolari B. 1985. The mannose-permease of the bacterial phosphotransferase system. Gene cloning and purification of the enzyme IIMan/IIIMan complex of Escherichia coli. J. Biol. Chem. 260: 15495-15503.
22. Studholme DJ. 2002. Enhancer-dependent transcription in Salmonella enterica Typhimurium: new members of the sigmaN regulon inferred from protein sequence homology and predicted promoter sites. J. Mol. Microbiol. Biotechnol. 4:367-374.
23. Xu H, Hoover TR. 2001. Transcriptional regulation at a distance in bacteria. Curr. Opin. Microbiol. 4:138-144.
24. Zhang X, Chaney M, Wigneshweraraj SR, Schumacher J, Bordes P, Cannon W, Buck M. 2002. Mechanochemical ATPases and transcriptional activation. Mol. Microbiol. 45:895-903.
25. Neidhardt FC, Bloch PL, Smith DF. 1974. Culture medium for enterobacteria. J. Bacteriol. 119:736-747.
26. Maloy SR, Stewart VJ, Taylor RK. 1996. Genetic analysis of pathogenic bacteria: a laboratory manual. Cold Spring Harbor Laboratory Press, Plainview, NY.
27. Dalcanale E, Montanari F. 1986. Selective oxidation of aldehydes to carboxylic acids with sodium chlorite-hydrogen peroxide. J. Org. Chem. 51:567-569.
28. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
29. Warren JW, Walker JR, Roth JR, Altman E. 2000. Construction and characterization of a highly regulable expression vector, pLAC11, and its multipurpose derivatives, pLAC22 and pLAC33. Plasmid 44:138-151.
30. Studier FW, Rosenberg AH, Dunn JJ, Dubendorff JW. 1990. Use of T7 RNA polymerase to direct the expression of cloned genes. Methods Enzymol. 185:60-89.
31. Studier FW. 2005. Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif. 41:207-234.
32. Schmittgen TD, Livak KJ. 2008. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3:1101-1108.
33. Karlin S, Campbell AM, Mrazek J. 1998. Comparative DNA analysis across diverse genomes. Annu. Rev. Genet. 32:185-225.
34. Karlin S, Mrazek J, Campbell AM. 1997. Compositional biases of bacterial genomes and evolutionary implications. J. Bacteriol. 179:3899-3913.
35. Karlin S, Ladunga I, Blaisdell BE. 1994. Heterogeneity of genomes: measures and values. Proc. Natl. Acad. Sci. U. S. A. 91:12837-12841.
36. Campbell AM, Mrazek J, Karlin S. 1999. Genome signature comparisons among prokaryote, plasmid, and mitochondrial DNA. Proc. Natl. Acad. Sci. U. S. A. 96:9184-9189.
37. Karlin S, Burge C. 1995. Dinucleotide relative abundance extremes: a genomic signature. Trends Genet. 11:283-290.
38. Garcia E, Bancroft S, Rhee SG, Kustu S. 1977. The product of a newly identified gene, glnF, is required for synthesis of glutamine synthetase in Salmonella. Proc. Natl. Acad. Sci. U. S. A. 74:1662-1666.
39. Chin AM, Feldheim DA, Saier MH, Jr. 1989. Altered transcriptional patterns affecting several metabolic pathways in strains of Salmonella typhimurium which overexpress the fructose regulon. J. Bacteriol. 171: 2424-2434.
40. Sutrina SL, Chin AM, Esch F, Saier MH, Jr. 1988. Purification and characterization of the fructose-inducible HPr-like protein, FPr, and the fructose-specific enzyme III of the phosphoenolpyruvate:sugar phosphotransferase system of Salmonella typhimurium. J. Biol. Chem. 263:5061-5069.
41. Schneider G, Kack H, Lindqvist Y. 2000. The manifold of vitamin B6 dependent enzymes. Structure 8:R1-R6.
42. Deutscher J. 2008. The mechanisms of carbon catabolite repression in bacteria. Curr. Opin. Microbiol. 11:87-93.
43. 54- and phosphotransferase system-dependent regulators. Proc. Natl. Acad. Sci. U. S. A. 88:2212-2216.
44. Martin-Verstraete I, Charrier V, Stulke J, Galinier A, Erni B, Rapoport G, Deutscher J. 1998. Antagonistic effects of dual PTS-catalysed phosphorylation on the Bacillus subtilis transcriptional activator LevR. Mol. Microbiol. 28:293-303.
45. Curtis SJ, Epstein W. 1975. Phosphorylation of D-glucose in Escherichia coli mutants defective in glucosephosphotransferase, mannosephosphotransferase, and glucokinase. J. Bacteriol. 122:1189-1199.
46. Kornberg HL, Jones-Mortimer MC. 1975. PtsX: a gene involved in the uptake of glucose and fructose by Escherichia coli. FEBS Lett. 51:1-4.
47. Markowitz VM, Chen IM, Palaniappan K, Chu K, Szeto E, Grechkin Y, Ratner A, Anderson I, Lykidis A, Mavromatis K, Ivanova NN, Kyrpides NC. 2010. The integrated microbial genomes system: an expanding comparative analysis resource. Nucleic Acids Res. 38:D382-D390.
48. 54-dependent promoter sequences. Nucleic Acids Res. 27:4305-4313.
49. Iwamoto R, Imanaga Y, Sawada S, Soda K. 1983. Stereochemistry of an alpha, beta-elimination reaction by D-glucosaminate dehydratase. FEBS Lett. 156:33-36.
50. Iwamoto R, Imanaga Y, Soda K. 1979. Purification and properties of D-glucosaminate dehydratase from Agrobacterium radiobacter. FEBS Lett. 104:131-134.
51. Iwamoto R, Imanaga Y, Soda K. 1982. D-Glucosaminate dehydratase from Agrobacterium radiobacter. Physicochemical and enzymological properties. J. Biochem. 91:283-289.
52. Iwamoto R, Imanaga Y, Soda K. 1984. D-Glucosaminate dehydratase: spectrometric properties of the enzyme-bound pyridoxal 5=-phosphate. J. Biochem. 95:13-18.
53. Arrach N, Zhao M, Porwollik S, Hoffman RM, McClelland M. 2008. Salmonella promoters preferentially activated inside tumors. Cancer Res. 68:4827-4832.
54. Bourret TJ, Porwollik S, McClelland M, Zhao R, Greco T, Ischiropoulos H, Vazquez-Torres A. 2008. Nitric oxide antagonizes the acid tolerance response that protects Salmonella against innate gastric defenses. PLoS One 3:e1833.
55. Eriksson S, Lucchini S, Thompson A, Rhen M, Hinton JC. 2003. Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol. Microbiol. 47:103-118.
56. Ge S, Danino V, He Q, Hinton JC, Granfors K. 2010. Microarray analysis of response of Salmonella during infection of HLA-B27-transfected human macrophage-like U937 cells. BMC Genomics 11:456.
57. Harvey PC, Watson M, Hulme S, Jones MA, Lovell M, Berchieri A, Jr, Young J, Bumstead N, Barrow P. 2011. Salmonella enterica serovar Typhimurium colonizing the lumen of the chicken intestine grows slowly and upregulates a unique set of virulence and metabolism genes. Infect. Immun. 79:4105-4121.
58. Hautefort I, Thompson A, Eriksson-Ygberg S, Parker ML, Lucchini S, Danino V, Bongaerts RJ, Ahmad N, Rhen M, Hinton JC. 2008. During infection of epithelial cells Salmonella enterica serovar Typhimurium undergoes a time-dependent transcriptional adaptation that results in simultaneous expression of three type 3 secretion systems. Cell. Microbiol. 10: 958-984.
59. Lamichhane-Khadka R, Frye JG, Porwollik S, McClelland M, Maier RJ. 2011. Hydrogen-stimulated carbon acquisition and conservation in Salmonella enterica serovar Typhimurium. J. Bacteriol. 193:5824-5832.
60. Prouty AM, Brodsky IE, Manos J, Belas R, Falkow S, Gunn JS. 2004. Transcriptional regulation of Salmonella enterica serovar Typhimurium genes by bile. FEMS Immunol. Med. Microbiol. 41:177-185.
61. Yoon H, McDermott JE, Porwollik S, McClelland M, Heffron F. 2009. Coordinated regulation of virulence during systemic infection of Salmonella enterica serovar Typhimurium. PLoS Pathog. 5:e1000306.
62. Fink RC, Evans MR, Porwollik S, Vazquez-Torres A, Jones-Carson J, Troxell B, Libby SJ, McClelland M, Hassan HM. 2007. FNR is a global regulator of virulence and anaerobic metabolism in Salmonella enterica serovar Typhimurium (ATCC 14028s). J. Bacteriol. 189:2262-2273.
63. Lawhon SD, Frye JG, Suyemoto M, Porwollik S, McClelland M, Altier C. 2003. Global regulation by CsrA in Salmonella typhimurium. Mol. Microbiol. 48:1633-1645.
64. Troxell B, Fink RC, Porwollik S, McClelland M, Hassan HM. 2011. The Fur regulon in anaerobically grown Salmonella enterica sv. Typhimurium: identification of new Fur targets. BMC Microbiol. 11:236.
65. Steeb B, Claudi B, Burton NA, Tienz P, Schmidt A, Farhan H, Maze A, Bumann D. 2013. Parallel exploitation of diverse host nutrients enhances Salmonella virulence. PLoS Pathog. 9:e1003301.
66. Bhat UR, Forsberg LS, Carlson RW. 1994. Structure of lipid A component of Rhizobium leguminosarum bv. phaseoli lipopolysaccharide. Unique nonphosphorylated lipid A containing 2-amino-2-deoxygluconate, galacturonate, and glucosamine. J. Biol. Chem. 269: 14402-14410.
67. Cozier GE, Salleh RA, Anthony C. 1999. Characterization of the membrane quinoprotein glucose dehydrogenase from Escherichia coli and characterization of a site-directed mutant in which histidine-262 has been changed to tyrosine. Biochem. J. 340:639-647.
68. Erni B, Zanolari B. 1986. Glucose-permease of the bacterial phosphotransferase system. Gene cloning, overproduction, and amino acid sequence of enzyme IIGlc. J. Biol. Chem. 261:16398-16403.
69. Matsushita K, Arents JC, Bader R, Yamada M, Adachi O, Postma PW. 1997. Escherichia coli is unable to produce pyrroloquinoline quinone (PQQ). Microbiology 143:3149-3156.