In Salmonella enterica, the sirtuin-dependent protein acylation/deacylation system (SDPADS) maintains energy homeostasis during growth on low concentrations of acetate

Molecular Microbiology

Volumn 80, Issue 1, 2011, Pages 168-183

  Chan, Chi Ho ^a   Garrity, Jane ^a,b   Crosby, Heidi A ^a   Escalante Semerena, Jorge C ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; ACETYL COENZYME A SYNTHETASE; ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; SIRTUIN;

ACYLATION; ARTICLE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL STRAIN; CONTROLLED STUDY; DEACYLATION; ENERGY BALANCE; ENZYME ACTIVITY; GROWTH INHIBITION; NONHUMAN; NUTRIENT LIMITATION; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN INDUCTION; PROTEIN SYNTHESIS INHIBITION; SALMONELLA ENTERICA;

ACETATE-COA LIGASE; ACETATES; ADENOSINE TRIPHOSPHATE; ENERGY METABOLISM; ISOCITRATE DEHYDROGENASE; MUTAGENESIS, SITE-DIRECTED; SALMONELLA ENTERICA; SIRTUINS;

SALMONELLA ENTERICA;

EID: 79953058855     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07566.x     Document Type: Article

References (76)

1. Altschul, S.F., Gish, W., Miller, W., and Myers, E.W. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
2. Atkinson, D.E. (1968) The energy charge of the adenylate pool as a regulatory parameter. Interaction with feedback modifiers. Biochemistry 7: 4030-4034.
3. Atlas, R. (1995) Handbook of Media for Environmental Microbiology. Boca Raton: CRC Press.
4. Balch, W.E., and Wolfe, R.S. (1976) New approach to the cultivation of methanogenic bacteria: 2-mercaptoethanesulfonic acid (HS-CoM)-dependent growth of Methanobacterium ruminantium in a pressurized atmosphere. Appl Environ Microbiol 32: 781-791.
5. Beatty, C.M., Browning, D.F., Busby, S.J., and Wolfe, A.J. (2003) Cyclic AMP receptor protein-dependent activation of the Escherichia coli acsP2 promoter by a synergistic class III mechanism. J Bacteriol 185: 5148-5157.
6. Bennett, B.D., Kimball, E.H., Gao, M., Osterhout, R., Van Dien, S.J., and Rabinowitz, J.D. (2009) Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat Chem Biol 5: 593-599.
7. Berg, P. (1956) Acyl adenylates: the synthesis and properties of adenylate acetate. J Biol Chem 222: 1015-1023.
8. Berkowitz, D., Hushon, J.M., Whitfield, H.J., Jr, Roth, J., and Ames, B.N. (1968) Procedure for identifying nonsense mutations. J Bacteriol 96: 215-220.
9. Bertani, G. (1951) Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol 62: 293-300.
10. Bertani, G. (2004) Lysogeny at mid-twentieth century: P1, P2, and other experimental systems. J Bacteriol 186: 595-600.
11. Blander, G., and Guarente, L. (2004) The sir2 family of protein deacetylases. Annu Rev Biochem 73: 417-435.
12. Bochner, B.R., and Ames, B.N. (1982) Complete analysis of cellular nucleotides by two-dimensional thin layer chromatography. J Biol Chem 257: 9759-9769.
13. Brinsmade, S.R., and Escalante-Semerena, J.C. (2007) In vivo and in vitro analyses of single-amino acid variants of the Salmonella enterica phosphotransacetylase enzyme provide insights into the function of its N-terminal domain. J Biol Chem 282: 12629-12640.
14. Brown, T.D., Jones-Mortimer, M.C., and Kornberg, H.L. (1977) The enzymic interconversion of acetate and acetyl-coenzyme A in Escherichia coli. J Gen Microbiol 102: 327-336.
15. Browning, D.F., Beatty, C.M., Wolfe, A.J., Cole, J.A., and Busby, S.J. (2002) Independent regulation of the divergent Escherichia coli nrfA and acsP1 promoters by a nucleoprotein assembly at a shared regulatory region. Mol Microbiol 43: 687-701.
16. Browning, D.F., Beatty, C.M., Sanstad, E.A., Gunn, K.E., Busby, S.J., and Wolfe, A.J. (2004) Modulation of CRP-dependent transcription at the Escherichia coli acsP2 promoter by nucleoprotein complexes: anti-activation by the nucleoid proteins FIS and IHF. Mol Microbiol 51: 241-254.
17. Castilho, B.A., Olfson, P., and Casadaban, M.J. (1984) Plasmid insertion mutagenesis and lac gene fusion with mini-mu bacteriophage transposons. J Bacteriol 158: 488-495.
18. Chan, R.K., Botstein, D., Watanabe, T., and Ogata, Y. (1972) Specialized transduction of tetracycline resistance by phage P22 in Salmonella typhimurium. II. Properties of a high-frequency-transducing lysate. Virology 50: 883-898.
19. Chapman, A.G., Fall, L., and Atkinson, D.E. (1971) Adenylate energy charge in Escherichia coli during growth and starvation. J Bacteriol 108: 1072-1086.
20. Chohnan, S., Furukawa, H., Fujio, T., Nishihara, H., and Takamura, Y. (1997) Changes in the size and composition of intracellular pools of nonesterified coenzyme A and coenzyme A thioesters in aerobic and facultatively anaerobic bacteria. Appl Environ Microbiol 63: 553-560.
21. Chohnan, S., Izawa, H., Nishihara, H., and Takamura, Y. (1998) Changes in size of intracellular pools of coenzyme A and its thioesters in Escherichia coli K-12 cells to various carbon sources and stresses. Biosci Biotechnol Biochem 62: 1122-1128.
22. Crosby, H.A., Heiniger, E.K., Harwood, C.S., and Escalante-Semerena, J.C. (2010) Reversible N(epsilon)-lysine acetylation regulates the activity of acyl-CoA synthetases involved in anaerobic benzoate catabolism in Rhodopseudomonas palustris. Mol Microbiol 76: 874-888.
23. Davis, R.W., Botstein, D., and Roth, J.R. (1980) A Manual for Genetic Engineering: Advanced Bacterial Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
24. Frey, P.A., and Arabshahi, A. (1995) Standard free energy change for the hydrolysis of the alpha, beta-phosphoanhydride bridge in ATP. Biochemistry 34: 11307-11310.
25. Gardner, J.G., and Escalante-Semerena, J.C. (2009) In Bacillus subtilis, the sirtuin protein deacetylase encoded by the srtN gene (formerly yhdZ), and functions encoded by the acuABC genes control the activity of acetyl-CoA synthetase. J Bacteriol 191: 1749-1755.
26. Gardner, J.G., Grundy, F.J., Henkin, T.M., and Escalante-Semerena, J.C. (2006) Control of acetyl-coenzyme A synthetase (AcsA) activity by acetylation/deacetylation without NAD(+) involvement in Bacillus subtilis. J Bacteriol 188: 5460-5468.
27. Garrity, J., Gardner, J.G., Hawse, W., Wolberger, C., and Escalante-Semerena, J.C. (2007) N-lysine propionylation controls the activity of propionyl-CoA synthetase. J Biol Chem 282: 30239-30245.
28. Guzman, L.M., Belin, D., Carson, M.J., and Beckwith, J. (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177: 4121-4130.
29. Hallows, W.C., Lee, S., and Denu, J.M. (2006) Sirtuins deacetylate and activate mammalian acetyl-CoA synthetases. Proc Natl Acad Sci USA 103: 10230-10235.
30. Horswill, A.R., and Escalante-Semerena, J.C. (2002) Characterization of the propionyl-CoA synthetase (PrpE) enzyme of Salmonella enterica: residue Lys592 is required for propionyl-AMP synthesis. Biochemistry 41: 2379-2387.
31. Ikeuchi, Y., Kitahara, K., and Suzuki, T. (2008) The RNA acetyltransferase driven by ATP hydrolysis synthesizes N4-acetylcytidine of tRNA anticodon. EMBO J 27: 2194-2203.
32. Ingram-Smith, C., Martin, S.R., and Smith, K.S. (2006) Acetate kinase: not just a bacterial enzyme. Trends Microbiol 14: 249-253.
33. Inoue, H., Nojima, H., and Okayama, H. (1990) High efficiency transformation of Escherichia coli with plasmids. Gene 96: 23-28.
34. Iram, S.H., and Cronan, J.E. (2006) The beta-oxidation systems of Escherichia coli and Salmonella enterica are not functionally equivalent. J Bacteriol 188: 599-608.
35. Jackowski, S., and Rock, C.O. (1981) Regulation of coenzyme A biosynthesis. J Bacteriol 148: 926-932.
36. Kornberg, H.L. (1966) The role and control of the glyoxylate cycle in Escherichia coli. Biochem J 99: 1-11.
37. Kumari, S., Beatty, C.M., Browning, D.F., Busby, S.J., Simel, E.J., Hovel-Miner, G., and Wolfe, A.J. (2000a) Regulation of acetyl coenzyme A synthetase in Escherichia coli. J Bacteriol 182: 4173-4179.
38. Kumari, S., Simel, E.J., and Wolfe, A.J. (2000b) Sigma(70) is the principal sigma factor responsible for transcription of acs, which encodes acetyl coenzyme A synthetase in Escherichia coli. J Bacteriol 182: 551-554.
39. Kunitz, M. (1952) Crystalline inorganic pyrophosphatase isolated from baker's yeast. J Gen Physiol 35: 423-450.
40. LaPorte, D.C. (1993) The isocitrate dehydrogenase phosphorylation cycle: regulation and enzymology. J Cell Biochem 51: 14-18.
41. LaPorte, D.C., Thorsness, P.E., and Koshland, D.E., Jr (1985) Compensatory phosphorylation of isocitrate dehydrogenase. A mechanism for adaptation to the intracellular environment. J Biol Chem 260: 10563-10568.
42. Miller, S.P., Chen, R., Karschnia, E.J., Romfo, C., Dean, A., and LaPorte, D.C. (2000) Locations of the regulatory sites for isocitrate dehydrogenase kinase/phosphatase. J Biol Chem 275: 833-839.
43. Morgan-Kiss, R.M., Wadler, C., and Cronan, J.E., Jr (2002) Long-term and homogeneous regulation of the Escherichia coli araBAD promoter by use of a lactose transporter of relaxed specificity. Proc Natl Acad Sci USA 99: 7373-7377.
44. Neidhardt, F.C., Bloch, P.L., and Smith, D.F. (1974) Culture medium for enterobacteria. J Bacteriol 119: 736-747.
45. Nimmo, G.A., and Nimmo, H.G. (1984) The regulatory properties of isocitrate dehydrogenase kinase and isocitrate dehydrogenase phosphatase from Escherichia coli ML308 and the roles of these activities in the control of isocitrate dehydrogenase. Eur J Biochem 141: 409-414.
46. North, B.J., and Verdin, E. (2004) Sirtuins: sir2-related NAD-dependent protein deacetylases. Genome Biol 5: 224.
47. Reger, A.S., Carney, J.M., and Gulick, A.M. (2007) Biochemical and crystallographic analysis of substrate binding and conformational changes in acetyl-CoA synthetase. Biochemistry 46: 6536-6546.
48. Rock, C.O., Park, H.W., and Jackowski, S. (2003) Role of feedback regulation of pantothenate kinase (CoaA) in control of coenzyme A levels in Escherichia coli. J Bacteriol 185: 3410-3415.
49. Sánchez, L.B., and Muller, M. (1996) Purification and characterization of the acetate forming enzyme, acetyl-CoA synthetase (ADP-forming) from the amitochondriate protist, Giardia lamblia. FEBS Lett 378: 240-244.
50. Sánchez, L.B., Morrison, H.G., Sogin, M.L., and Muller, M. (1999) Cloning and sequencing of an acetyl-CoA synthetase (ADP-forming) gene from the amitochondriate protist, Giardia lamblia. Gene 233: 225-231.
51. Sánchez, L.B., Galperin, M.Y., and Muller, M. (2000) Acetyl-CoA synthetase from the amitochondriate eukaryote Giardia lamblia belongs to the newly recognized superfamily of acyl-CoA synthetases (Nucleoside diphosphate-forming). J Biol Chem 275: 5794-5803.
52. Sasse, J. (1991) Detection of proteins. In Current Protocols in Molecular Biology. Ausubel, F.A., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., and Struhl, K. (eds). New York: Wiley Interscience, pp. 10.16.11-10.16.18.
53. Schmieger, H. (1971) The fate of the bacterial chromosome in P22-infected cells of Salmonella typhimurium. Mol Gen Genet 110: 238-244.
54. Schmieger, H., and Backhaus, H. (1973) The origin of DNA in transducing particles in P22-mutants with increased transduction-frequencies (HT-mutants). Mol Gen Genet 120: 181-190.
55. Schwer, B., Bunkenborg, J., Verdin, R.O., Andersen, J.S., and Verdin, E. (2006) Reversible lysine acetylation controls the activity of the mitochondrial enzyme acetyl-CoA synthetase 2. Proc Natl Acad Sci USA 103: 10224-10229.
56. Shin, S., Song, S.G., Lee, D.S., Pan, J.G., and Park, C. (1997) Involvement of iclR and rpoS in the induction of acs, the gene for acetyl coenzyme A synthetase of Escherichia coli K-12. FEMS Microbiol Lett 146: 103-108.
57. Starai, V.J., and Escalante-Semerena, J.C. (2004a) Acetyl-coenzyme A synthetase (AMP forming). Cell Mol Life Sci 61: 2020-2030.
58. Starai, V.J., and Escalante-Semerena, J.C. (2004b) Identification of the protein acetyltransferase (Pat) enzyme that acetylates acetyl-CoA synthetase in Salmonella enterica. J Mol Biol 340: 1005-1012.
59. Starai, V.J., Celic, I., Cole, R.N., Boeke, J.D., and Escalante-Semerena, J.C. (2002) Sir2-dependent activation of acetyl-CoA synthetase by deacetylation of active lysine. Science 298: 2390-2392.
60. Starai, V.J., Takahashi, H., Boeke, J.D., and Escalante-Semerena, J.C. (2003) Short-chain fatty acid activation by acyl-coenzyme A synthetases requires SIR2 protein function in Salmonella enterica and Saccharomyces cerevisiae. Genetics 163: 545-555.
61. Starai, V.J., Takahashi, H., Boeke, J.D., and Escalante-Semerena, J.C. (2004) A link between transcription and intermediary metabolism: a role for Sir2 in the control of acetyl-coenzyme A synthetase. Curr Opin Microbiol 7: 115-119.
62. Starai, V.J., Gardner, J.G., and Escalante-Semerena, J.C. (2005a) Residue Leu-641 of acetyl-CoA synthetase is critical for the acetylation of residue Lys-609 by the Protein acetyltransferase enzyme of Salmonella enterica. J Biol Chem 280: 26200-26205.
63. Starai, V.J., Garrity, J., and Escalante-Semerena, J.C. (2005b) Acetate excretion during growth of Salmonella enterica on ethanolamine requires phosphotransacetylase (EutD) activity, and acetate recapture requires acetyl-CoA synthetase (Acs) and phosphotransacetylase (Pta) activities. Microbiology 151: 3793-3801.
64. Studer, S.V., Mandel, M.J., and Ruby, E.G. (2008) AinS quorum sensing regulates the Vibrio fischeri acetate switch. J Bacteriol 190: 5915-5923.
65. Thao, S., Chen, S.-S., Zhu, H., and Escalante-Semerena, J.C. (2010) Nε-Lysine acetylation of a bacterial transcription factor inhibits its DNA-binding activity. PLoS ONE 5: e15123.
66. Thauer, R.K., Jungermann, K., and Decker, K. (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 41: 100-180.
67. Vallari, D.S., Jackowski, S., and Rock, C.O. (1987) Regulation of pantothenate kinase by coenzyme A and its thioesters. J Biol Chem 262: 2468-2471.
68. Vetting, M.W., Magnet, S., Nieves, E., Roderick, S.L., and Blanchard, J.S. (2004) A bacterial acetyltransferase capable of regioselective N-acetylation of antibiotics and histones. Chem Biol 11: 565-573.
69. Vetting, M.W., de Carvalho, L.P., Roderick, S.L., and Blanchard, J.S. (2005) A novel dimeric structure of the RimL Nalpha-acetyltransferase from Salmonella typhimurium. J Biol Chem 280: 22108-22114.
70. Wadler, C., and Cronan, J.E. (2007) Dephospho-CoA kinase provides a rapid and sensitive radiochemical assay for coenzyme A and its thioesters. Anal Biochem 368: 17-23.
71. Wang, Q., Zhang, Y., Yang, C., Xiong, H., Lin, Y., Yao, J., etal. (2010) Acetylation of metabolic enzymes coordinates carbon source utilization and metabolic flux. Science 327: 1004-1007.
72. Way, J.C., Davis, M.A., Morisato, D., Roberts, D.E., and Kleckner, N. (1984) New Tn10 derivatives for transposon mutagenesis and for construction of lacZ operon fusions by transposition. Gene 32: 369-379.
73. Williamson, J.R., and Corkey, B.E. (1969) Assays of intermediates of the citric acid cycle and related compounds by fluorometric enzyme methods. In Methods in Enzymology. Lowenstein, J.M. (ed.). New York: Academic Press, pp. 494-497.
74. Winston, S.E., Fuller, S.A., and Hurrell, J.G.R. (1990) Western blotting. In Current Protocols in Molecular Biology. Ausubel, F.A., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., and Struhl, K. (eds). New York: Wiley Interscience, pp. 10.18.11-10.18.16.
75. Zhao, K., Chai, X., and Marmorstein, R. (2004) Structure and substrate binding properties of CobB, a Sir2 homolog protein deacetylase from Escherichia coli. J Mol Biol 337: 731-741.
76. Zheng, J., and Jia, Z. (2010) Structure of the bifunctional isocitrate dehydrogenase kinase/phosphatase. Nature 465: 961-965.