Hydrogen-stimulated carbon acquisition and conservation in Salmonella enterica serovar typhimurium

Journal of Bacteriology

Volumn 193, Issue 20, 2011, Pages 5824-5832

  Lamichhane Khadka, Reena ^a   Frye, Jonathan G ^b   Porwollik, Steffen ^c   McClelland, Michael ^c   Maier, Robert J ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b RUSSELL RESEARCH CENTER   (United States)

^c Vaccine Research Institute of San Diego   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARAGINASE; GALACTOSE; GLUTAMATE AMMONIA LIGASE; GLYCERIC ACID; GLYCEROPHOSPHATE; GLYCINE HYDROXYMETHYLTRANSFERASE; GLYOXYLIC ACID; HISTIDINE AMMONIALYASE; HYDROGEN; IRON; ISOCITRATE LYASE; MALATE SYNTHASE; MANGANESE; MANNOSE; PHOSPHOGLYCERATE MUTASE; RIBOSE; SACCHARIC ACID; URIDINE TRIPHOSPHATE GLUCOSE 1 PHOSPHATE URIDYLYLTRANSFERASE;

AMINO ACID TRANSPORT; ANAEROBIC GROWTH; ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL STRAIN; CARBOHYDRATE TRANSPORT; CARBON FIXATION; CARBON METABOLISM; CONTROLLED STUDY; DELETION MUTANT; DNA SYNTHESIS; ENERGY METABOLISM; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC CONSERVATION; GROWTH RATE; NONHUMAN; PRIORITY JOURNAL; SALMONELLA ENTERICA; UPREGULATION;

BACTERIAL PROTEINS; CARBON; ENERGY METABOLISM; GENE EXPRESSION REGULATION, BACTERIAL; HYDROGEN; SALMONELLA TYPHIMURIUM;

PUFFINUS AURICULARIS; SALMONELLA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

EID: 80053593606     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.05456-11     Document Type: Article

References (58)

1. Ajl, S. J. 1956. Conversion of acetate and glyoxylate to malate. J. Am. Chem. Soc. 78:3230-3231.
2. Ballantine, S. P., and D. H. Boxer. 1985. Nickel-containing hydrogenase isoenzymes from anaerobically grown Escherichia coli K-12. J. Bacteriol. 163:454-459.
3. Blumenthal, H. J., and D. C. Fish. 1963. Bacterial conversion of D-glucarate to glycerate and pyruvate. Biochem. Biophys. Res. Commun. 11:239-243.
4. Blumenthal, H. J., V. L. Lucuta, and D. C. Blumenthal. 1990. Specific enzymatic assay for D-glucarate in human serum. Anal. Biochem. 185:286-293.
5. Boyer, E., I. Bergevin, D. Malo, P. Gros, and M. F. Cellier. 2002. Acquisition of Mn(II) in addition to Fe(II) is required for full virulence of Salmonella enterica serovar Typhimurium. Infect. Immun. 70:6032-6042.
6. Cohen, G. N., and H. V. Rickenberg. 1956. Concentration specifique reversible des amino acides chez Escherichia coli. Ann. Inst. Pasteur (Paris) 91: 693-720.
7. Compan, I., and D. Touati. 1993. Interaction of six global transcription regulators in expression of manganese superoxide dismutase in Escherichia coli K-12. J. Bacteriol. 175:1687-1696.
8. Cotruvo, J. A., Jr., and J. Stubbe. 2008. NrdI, a flavodoxin involved in maintenance of the diferric-tyrosyl radical cofactor in Escherichia coli class Ib ribonucleotide reductase. Proc. Natl. Acad. Sci. U. S. A. 105: 14383-14388.
9. Creaghan, I. T., and J. R. Guest. 1977. Suppression of the succinate requirement of lipoamide dehydrogenase mutants of Escherichia coli by mutations affecting succinate dehydrogenase activity. J. Gen. Microbiol. 103:183-194.
10. Cronan, J. E., Jr., and D. LaPorte. 9 November 2006, posting date. Tricarboxylic acid cycle and glyoxylate bypass. In A. Böck (ed.), EcoSal-Escherichia coli and Salmonella: cellular and molecular biology (http://www.ecosal.org). ASM Press, Washington, DC. doi:10.1128/EcoSal.3.5.2.
11. Datsenko, K. A., and B. L. Wanner. 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.
12. Difco Laboratories, Division of Becton Dickinson and Company. 1998. Difco manual, 11th ed., p. 383-385. Difco Laboratories, Sparks, MD.
13. Dubnau, E., N. P. Fonta, R. Manganelli, S. Soares-Appel, and I. Smith. 2002. Mycobacterium tuberculosis genes induced during infection of human macrophages. Infect. Immun. 70:2787-2795.
14. Dunn, M. F., J. A. Ramírez-Trujillo, and I. Hernandez-Lucas. 2009. Major roles of isocitrate lyase and malate synthase in bacterial and fungal pathogenesis. Microbiology 155:3166-3175.
15. Dutton, G. J. 1980. Glucuronidation of drugs and other compounds, p. 83-89. CRC Press, Boca Raton, FL.
16. Eriksson, S., S. Lucchini, A. Thompson, M. Rhen, and J. C. Hinton. 2003. Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol. Microbiol. 47:103-118.
17. Evans, M. R., et al. 2011. Analysis of the ArcA regulon in anaerobically grown Salmonella enterica sv. Typhimurium. BMC Microbiol. 11:58.
18. Fang, F. C., S. J. Libby, M. F. Castor, and A. M. Fung. 2005. Isocitrate lyase (AceA) is required for Salmonella persistence but not for acute lethal infection in mice. Infect. Immun. 73:2547-2549.
19. Foster, J. W., and M. P. Spector. 1995. How Salmonella survive against the odds. Annu. Rev. Microbiol. 49:145-174.
20. Graham, J. E., and J. E. Clark-Curtiss. 1999. Identification of Mycobacterium tuberculosis RNAs synthesized in response to phagocytosis by human macrophages by selective capture of transcribed sequences (SCOTS). Proc. Natl. Acad. Sci. U. S. A. 96:11554-11559.
21. Hansen, R. W., and J. A. Hayashi. 1962. Glycolate metabolism in Escherichia coli. J. Bacteriol. 83:679-687.
22. Janakiraman, A., and J. M. Slauch. 2000. The putative iron transport system SitABCD encoded on SPI1 is required for full virulence of Salmonella typhimurium. Mol. Microbiol. 35:1146-1155.
23. Kauko, T., et al. 2010. Phenotype MicroArray in the metabolic characterisation of Salmonella serotypes Agona, Enteritidis, Give, Hvittingfoss, Infantis, Newport and Typhimurium. Eur. J. Clin. Microbiol. Infect. Dis. 29:311-317.
24. 2+ transporter of Salmonella enterica serovar Typhimurium. J. Bacteriol. 184:3159-3166.
25. Kehres, D. G., and M. E. Maguire. 2003. Emerging themes in manganese transport, biochemistry and pathogenesis in bacteria. FEMS Microbiol. Rev. 27:263-290.
26. Kinhikar, A. G., et al. 2006. Mycobacterium tuberculosis malate synthase is a laminin-binding adhesin. Mol. Microbiol. 60:999-1013.
27. Kornberg, H. L. 1966. Anaplerotic sequences and their role in metabolism. Essays Biochem. 2:1-31.
28. Kornberg, H. L. 1966. The role and control of the glyoxylate cycle in Escherichia coli. Biochem. J. 99:1-11.
29. 2-units by a modified tricarboxylic acid cycle. Nature 179:988-991.
30. Kwon, Y. M., and S. C. Ricke. 1998. Survival of a Salmonella typhimurium poultry isolate in the presence of propionic acid under aerobic and anaerobic conditions. Anaerobe 4:251-256.
31. Lajolo, C., et al. 2010. Calcium glucarate inhibits DMBA-induced oral carcinogenesis in the hamster: histomorphometric evaluation. Anticancer Res. 30:843-849.
32. Lamichhane-Khadka, R., A. Kwiatkowski, and R. J. Maier. 2010. The Hyb hydrogenase permits hydrogen-dependent respiratory growth of Salmonella enterica serovar Typhimurium. mBio 1(5):e00284-10.
33. Lawhon, S. D., et al. 2003. Global regulation by CsrA in Salmonella typhimurium. Mol. Microbiol. 48:1633-1645.
34. -ΔΔCt method. Methods 25(4):402-408.
35. Lorenz, M. C., J. A. Bender, and G. R. Fink. 2004. Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot. Cell 3:1076-1087.
36. Maier, R. J. 2005. Use of molecular hydrogen as an energy substrate by human pathogenic bacteria. Biochem. Soc. Trans. 33:83-85.
37. Maier, R. J., A. Olczak, S. S. Maier, S. Soni, and J. Gunn. 2004. Respiratory hydrogen use by Salmonella enterica serovar Typhimurium is essential for virulence. Infect. Immun. 72:6294-6299.
38. Marsh, C. A. 1963. Metabolism of D-glucuronolactone in mammalian systems. II. Conversion of D-glucuronolactone into D-glucaric acid by tissue preparation. Biochem. J. 87:82-90.
39. Martin, J. E., and J. A. J. A. Imlay. 2011. The alternative aerobic ribonucleotide reductase of Escherichia coli, NrdEF, is a manganese-dependent enzyme that enables cell replication during periods of iron starvation. Mol. Microbiol. 80:319-334.
40. Matsui, M., A. Fukuo, Y. Watanabe, T. Wanibe, and M. Okada. 1977. Studies on the glucaric acid pathway in the metabolism of D-glucuronic acid in mammals. IV. Fluorometric method for the determination of glucaric acid in serum. Chem. Pharm. Bull. 20:845-848.
41. Maurer, J. J., T. A. Doggett, L. Burns-Keliher, and R. Curtis, 3rd. 2000. Expression of the rfa, LPS biosynthesis promoter in Salmonella typhimurium during invasion of intestinal epithelial cells. Curr. Microbiol. 41:172-176.
42. Mehta, N., S. S. Benoit, J. V. Mysore, R. S. Sousa, and R. J. Maier. 2005. Helicobacter hepaticus hydrogenase mutants are deficient in hydrogen-supported amino acid uptake and in causing liver lesions in A/J. mice. Infect. Immun. 73:5311-5318.
43. Monterrubio, R., L. Baldoma, N. Obradors, J. Aguilar, and J. Badia. 2000. A common regulator for the operons encoding the enzymes involved in D-galactarate, D-glucarate, and D-glycerate utilization in Escherichia coli. J. Bacteriol. 182:2672-2674.
44. Ollis, A. A., M. Manning, K. G. Held, and K. Postle. 2009. Cytoplasmic membrane protonmotive force energizes periplasmic interactions between ExbD and TonB. Mol. Microbiol. 73:466-481.
45. Postle, K. 1993. TonB protein and energy transduction between membranes. J. Bioenerg. Biomembr. 25:591-601.
46. Roberton, A. M., P. A. Sullivan, M. C. Jones-Mortimer, and H. L. Kornberg. 1980. Two genes affecting glucarate utilization in Escherichia coli K12. J. Gen. Microbiol. 117:311-382.
47. Rodrigue, D. C., R. V. Tauxe, and B. Rowe. 1990. International increase in Salmonella enteritidis: a new pandemic? Epidemiol. Infect. 105:21-27.
48. Schauer, K., D. A. Rodionov, and H. de Reuse. 2008. New substrates for TonB-dependent transport: do we only see the 'tip of the iceberg'? Trends Biochem. Sci. 33:330-338.
49. Skare, J. T., M. M. Ahmer, C. L. Seachord, R. P. Darveau, and K. Postle. 1993. Energy transduction between membranes: TonB, a cytoplasmic membrane protein, can be chemically crosslinked in vivo to the outer membrane receptor FepA. J. Biol. Chem. 268:16302-16308.
50. Smith, R. A., and I. C. Gunsalus. 1954. Isocitritase: a new tricarboxylic acid cleavage system. J. Am. Chem. Soc. 76:5002-5003.
51. Sunnarborg, A., D. Klumpp, T. Chung, and D. C. LaPorte. 1990. Regulation of the glyoxylate bypass operon: cloning and characterization of iclR. J. Bacteriol. 172:2642-2649.
52. Tchawa Yimga, M., et al. 2006. Role of gluconeogenesis and the tricarboxylic acid cycle in the virulence of Salmonella enterica serovar Typhimurium in BALB/c mice. Infect. Immun. 74:1130-1140.
53. +-reduction in primary energy conservation. Results Probl. Cell Differ. 45:223-244.
54. Vignais, P. M., and A. Colbeau. 2004. Molecular biology of microbial hydrogenases. Curr. Issues Mol. Biol. 6:159-188.
55. Webb, T. E., H. Abou-Issa, P. C. Stromberg, R. C. Curley, Jr., and M. H. Nguyen. 1993. Mechanism of growth inhibition of mammary carcinomas by glucarate and the glucarate: retinoid combination. Anticancer Res. 13(6A): 2095-2099.
56. Xia, X., M. McClelland, and Y. Wang. 2005. WebArray: an online platform for microarray data analysis. BMC Bioinformatics 6:306.
57. 2 in Salmonella enterica serovar Typhimurium. Appl. Environ. Microbiol. 75:1456-1459.
58. Zbell, A. L., S. L. Benoit, and R. J. Maier. 2007. Differential expression of NiFe uptake-type hydrogenase genes in Salmonella enterica serovar Typhimurium. Microbiology 153:3508-3516.