Reversible Nε-lysine acetylation regulates the activity of acyl-CoA synthetases involved in anaerobic benzoate catabolism in Rhodopseudomonas palustris

Molecular Microbiology

Volumn 76, Issue 4, 2010, Pages 874-888

  Crosby, Heidi A ^a   Heiniger, Erin K ^b   Harwood, Caroline S ^b   Escalante Semerena, Jorge C ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 HYDROXYBENZOYL COENZYME A SYNTHETASE; ACYL COENZYME A; ACYLTRANSFERASE; BENZOIC ACID; BENZOYL COENZYME A; CYCLOHEXANECARBOXYL COENZYME A SYNTHETASE; LIGNIN; LONG CHAIN FATTY ACID COENZYME A LIGASE; LYSINE; NICOTINAMIDE ADENINE DINUCLEOTIDE; SIRTUIN; UNCLASSIFIED DRUG; BENZOIC ACID DERIVATIVE;

ACETYLATION; ANAEROBIC METABOLISM; AQUATIC ENVIRONMENT; ARTICLE; BACTERIAL GROWTH; CONTROLLED STUDY; DEACETYLATION; DEGRADATION KINETICS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME REGULATION; GENETIC TRANSCRIPTION; MASS SPECTROMETRY; MUTATIONAL ANALYSIS; NONHUMAN; PHOTOHETEROTROPH; PRIORITY JOURNAL; RHODOPSEUDOMONAS PALUSTRIS; SALMONELLA ENTERICA; SEQUENCE HOMOLOGY; AMINO ACID SEQUENCE; ANAEROBIC GROWTH; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN PROCESSING; RHODOPSEUDOMONAS;

BACTERIA (MICROORGANISMS); RHODOPSEUDOMONAS PALUSTRIS; SALMONELLA ENTERICA;

ACETYLATION; AMINO ACID SEQUENCE; ANAEROBIOSIS; BENZOATES; COENZYME A LIGASES; LYSINE; MOLECULAR SEQUENCE DATA; PROTEIN PROCESSING, POST-TRANSLATIONAL; RHODOPSEUDOMONAS;

EID: 77952222270     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07127.x     Document Type: Article

References (59)

1. Bains, J. Boulanger, M.J. (2007) Biochemical and structural characterization of the paralogous benzoate CoA ligases from Burkholderia xenovorans LB400: defining the entry point into the novel benzoate oxidation (box) pathway. J Mol Biol 373 : 965 977.
2. Balch, W.E. 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.
3. Barragan, M.J., Blazquez, B., Zamarro, M.T., Mancheno, J.M., Garcia, J.L., Diaz, E. Carmona, M. (2005) BzdR, a repressor that controls the anaerobic catabolism of benzoate in Azoarcus sp. CIB, is the first member of a new subfamily of transcriptional regulators. J Biol Chem 280 : 10683 10694.
4. Bertani, G. (1951) Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol 62 : 293 300.
5. Bertani, G. (2004) Lysogeny at mid-twentieth century: P1, P2, and other experimental systems. J Bacteriol 186 : 595 600.
6. Blommel, P.G. Fox, B.G. (2007) A combined approach to improving large-scale production of tobacco etch virus protease. Protein Expr Purif 55 : 53 68.
7. Boll, M. Fuchs, G. (1995) Benzoyl-coenzyme A reductase (dearomatizing), a key enzyme of anaerobic aromatic metabolism. ATP dependence of the reaction, purification and some properties of the enzyme from Thauera aromatica strain K172. Eur J Biochem 234 : 921 933.
8. Boll, M., Albracht, S.S. Fuchs, G. (1997) Benzoyl-CoA reductase (dearomatizing), a key enzyme of anaerobic aromatic metabolism. A study of adenosinetriphosphatase activity, ATP stoichiometry of the reaction and EPR properties of the enzyme. Eur J Biochem 244 : 840 851.
9. Carmona, M., Zamarro, M.T., Blazquez, B., Durante-Rodriguez, G., Juarez, J.F., Valderrama, J.A., et al. (2009) Anaerobic catabolism of aromatic compounds: a genetic and genomic view. Microbiol Mol Biol Rev 73 : 71 133.
10. Conti, E., Stachelhaus, T., Marahiel, M.A. Brick, P. (1997) Structural basis for the activation of phenylalanine in the non-ribosomal biosynthesis of gramicidin S. EMBO J 16 : 4174 4183.
11. Dagley, S. (1981) New perspectives in aromatic catabolism. In Microbial Degradation of Xenobiotics and Recalcitrant Compounds. Leisinger, T., Cook, A.M., Hutter, R. Nuesch, J. (eds).
12. Denu, J.M. (2005) Vitamin B(3) and sirtuin function. Trends Biochem Sci 30 : 479 483.
13. Diaz, E. (2004) Bacterial degradation of aromatic pollutants: a paradigm of metabolic versatility. Int Microbiol 7 : 173 180.
14. Dispensa, M., Thomas, C.T., Kim, M.K., Perrotta, J.A., Gibson, J. Harwood, C.S. (1992) Anaerobic growth of Rhodopseudomonas palustris on 4-hydroxybenzoate is dependent on AadR, a member of the cyclic AMP receptor protein family of transcriptional regulators. J Bacteriol 174 : 5803 5813.
15. Egland, P.G. Harwood, C.S. (1999) BadR, a new MarR family member, regulates anaerobic benzoate degradation by Rhodopseudomonas palustris in concert with AadR, an Fnr family member. J Bacteriol 181 : 2102 2109.
16. Egland, P.G., Gibson, J. Harwood, C.S. (1995) Benzoate-coenzyme A ligase, encoded by badA, is one of 3 ligases able to catalyze benzoyl-coenzyme A formation during anaerobic growth of Rhodopseudomonas palustris on benzoate. J Bacteriol 177 : 6545 6551.
17. Egland, P.G., Pelletier, D.A., Dispensa, M., Gibson, J. Harwood, C.S. (1997) A cluster of bacterial genes for anaerobic benzene ring biodegradation. Proc Natl Acad Sci USA 94 : 6484 6489.
18. Fuchs, G. (2008) Anaerobic metabolism of aromatic compounds. Ann NY Acad Sci 1125 : 82 99.
19. Gardner, J.G. Escalante-Semerena, J.C. (2008) Biochemical and mutational analyses of AcuA, the acetyltransferase enzyme that controls the activity of the acetyl coenzyme a synthetase (AcsA) in Bacillus subtilis. J Bacteriol 190 : 5132 5136.
20. Gardner, J.G. 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.
21. Gardner, J.G., Grundy, F.J., Henkin, T.M. 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.
22. Garrity, J., Gardner, J.G., Hawse, W., Wolberger, C. Escalante-Semerena, J.C. (2007) N-lysine propionylation controls the activity of propionyl-CoA synthetase. J Biol Chem 282 : 30239 30245.
23. Geissler, J.F., Harwood, C.S. Gibson, J. (1988) Purification and properties of benzoate-coenzyme A ligase, a Rhodopseudomonas palustris enzyme involved in the anaerobic degradation of benzoate. J Bacteriol 170 : 1709 1714.
24. Gibson, J. Harwood, C. (2002) Metabolic diversity in aromatic compound utilization by anaerobic microbes. Annu Rev Microbiol 56 : 345 369.
25. Gibson, J., Dispensa, M., Fogg, G.C., Evans, D.T. Harwood, C.S. (1994) 4-Hydroxybenzoate-coenzyme A ligase from Rhodopseudomonas palustris: purification, gene sequence, and role in anaerobic degradation. J Bacteriol 176 : 634 641.
26. Gouet, P., Courcelle, E., Stuart, D.I. Metoz, F. (1999) ESPript: multiple sequence alignments in PostScript. Bioinformatics 15 : 305 308.
27. Guzman, L.M., Belin, D., Carson, M.J. Beckwith, J. (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177 : 4121 4130.
28. Hallows, W.C., Lee, S. Denu, J.M. (2006) Sirtuins deacetylate and activate mammalian acetyl-CoA synthetases. Proc Natl Acad Sci USA 103 : 10230 10235.
29. Harrison, F.H. Harwood, C.S. (2005) The pimFABCDE operon from Rhodopseudomonas palustris mediates dicarboxylic acid degradation and participates in anaerobic benzoate degradation. Microbiology 151 : 727 736.
30. Harwood, C.S., Burchhardt, G., Herrmann, H. Fuchs, G. (1999) Anaerobic metabolism of aromatic compounds via the benzoyl-CoA pathway. FEMS Microbiol Rev 22 : 439 458.
31. + and acetylated peptide. Structure 14 : 1231 1240.
32. Horswill, A.R. 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.
33. Horton, R.M., Ho, S.N., Pullen, J.K., Hunt, H.D., Cai, Z. Pease, L.R. (1993) Gene splicing by overlap extension. Methods Enzymol 217 : 270 279.
34. Kim, M.-K. Harwood, C.S. (1991) Regulation of benzoate-CoA ligase in Rhodopseudomonas palustris. FEMS Microbiol Lett 83 : 199 203.
35. Kovach, M.E., Elzer, P.H., Hill, D.S., Robertson, G.T., Farris, M.A., Roop, R.M., 2nd. Peterson, K.M. (1995) Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166 : 175 176.
36. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 : 680 685.
37. Larimer, F.W., Chain, P., Hauser, L., Lamerdin, J., Malfatti, S., Do, L., et al. (2004) Complete genome sequence of the metabolically versatile photosynthetic bacterium Rhodopseudomonas palustris. Nat Biotechnol 22 : 55 61.
38. May, J.J., Kessler, N., Marahiel, M.A. Stubbs, M.T. (2002) Crystal structure of DhbE, an archetype for aryl acid activating domains of modular nonribosomal peptide synthetases. Proc Natl Acad Sci USA 99 : 12120 121205.
39. Miroux, B. Walker, J.E. (1996) Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J Mol Biol 260 : 289 298.
40. Moore, D.D. (2001) Commonly used reagents and equipment. In Current Protocols in Molecular Biology, A.2.1-A.2.8. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A. Struhl, K. (eds).
41. Nakatsu, T., Ichiyama, S., Hiratake, J., Saldanha, A., Kobashi, N., Sakata, K. Kato, H. (2006) Structural basis for the spectral difference in luciferase bioluminescence. Nature 440 : 372 376.
42. Nielsen, T.K., Hildmann, C., Dickmanns, A., Schwienhorst, A. Ficner, R. (2005) Crystal structure of a bacterial class 2 histone deacetylase homologue. J Mol Biol 354 : 107 120.
43. Peres, C.M. Harwood, C.S. (2006) BadM is a transcriptional repressor and one of three regulators that control benzoyl coenzyme A reductase gene expression in Rhodopseudomonas palustris. J Bacteriol 188 : 8662 8665.
44. Quandt, J. Hynes, M.F. (1993) Versatile suicide vectors which allow direct selection for gene replacement in Gram-negative bacteria. Gene 127 : 15 21.
45. Reger, A.S., Carney, J.M. Gulick, A.M. (2007) Biochemical and crystallographic analysis of substrate binding and conformational changes in acetyl-CoA synthetase. Biochemistry 46 : 6536 6546.
46. Rocco, C.J., Dennison, K.L., Klenchin, V.A., Rayment, I. Escalante-Semerena, J.C. (2008) Construction and use of new cloning vectors for the rapid isolation of recombinant proteins from Escherichia coli. Plasmid 59 : 231 237.
47. Samanta, S.K. Harwood, C.S. (2005) Use of the Rhodopseudomonas palustris genome sequence to identify a single amino acid that contributes to the activity of a coenzyme A ligase with chlorinated substrates. Mol Microbiol 55 : 1151 1159.
48. Sasse, J. (1991) Detection of proteins Current Protocols in Molecular Biology. Ausubel, F.A., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A. Struhl, K. (eds).
49. Schafer, A., Tauch, A., Jager, W., Kalinowski, J., Thierbach, G. Puhler, A. (1994) Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145 : 69 73.
50. Schwer, B., Bunkenborg, J., Verdin, R.O., Andersen, J.S. 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.
51. Starai, V.J. Escalante-Semerena, J.C. (2004) Identification of the protein acetyltransferase (Pat) enzyme that acetylates acetyl-CoA synthetase in Salmonella enterica. J Mol Biol 340 : 1005 1012.
52. Starai, V.J., Celic, I., Cole, R.N., Boeke, J.D. Escalante-Semerena, J.C. (2002) Sir2-dependent activation of acetyl-CoA synthetase by deacetylation of active lysine. Science 298 : 2390 2392.
53. Starai, V.J., Takahashi, H., Boeke, J.D. 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. Genet 163 : 545 555.
54. Thompson, J.D., Higgins, D.G. Gibson, T.J. (1994) CLUSTAL W:improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acid Res 22 : 4673 4680.
55. Tsang, A.W. Escalante-Semerena, J.C. (1998) CobB, a new member of the SIR2 family of eucaryotic regulatory proteins, is required to compensate for the lack of nicotinate mononucleotide:5,6-dimethylbenzimidazole phosphoribosyltransferase activity in cobT mutants during cobalamin biosynthesis in Salmonella typhimurium LT2. J Biol Chem 273 : 31788 31794.
56. Vaillancourt, F.H., Bolin, J.T. Eltis, L.D. (2006) The ins and outs of ring-cleaving dioxygenases. Crit Rev Biochem Mol Biol 41 : 241 267.
57. Vetting, M.W., Carvalho, L.P.S., Yu, M., Hegde, S.S., Magnet, S., Roderick, S.L. Blanchard, J.S. (2005) Structure and functions of the GNAT superfamily of acetyltransferases. Arch Biochem Biophys 433 : 212 226.
58. Zaar, A., Eisenreich, W., Bacher, A. Fuchs, G. (2001) A novel pathway of aerobic benzoate catabolism in the bacteria Azoarcus evansii and Bacillus stearothermophilus. J Biol Chem 276 : 24997 25004.
59. Zaar, A., Gescher, J., Eisenreich, W., Bacher, A. Fuchs, G. (2004) New enzymes involved in aerobic benzoate metabolism in Azoarcus evansii. Mol Microbiol 54 : 223 238.