Changes in the acetylome and succinylome of Bacillus subtilis in response to carbon source

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Kosono, Saori ^a,b   Tamura, Masaru ^a,c   Suzuki, Shota ^a   Kawamura, Yumi ^b   Yoshida, Ayako ^a   Nishiyama, Makoto ^a   Yoshida, Minoru ^b  

^a UNIVERSITY OF TOKYO   (Japan)

^b Elements Chemistry Laboratory   (Japan)

^c NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACETATE KINASE; CITRIC ACID; GLUCOSE; RNA POLYMERASE; ACETYL COENZYME A; ACYL COENZYME A; BRANCHED CHAIN AMINO ACID; CARBON; LYSINE; PURINE; PURINE DERIVATIVE; SUCCINIC ACID; SUCCINYL-COENZYME A;

ACETYLATION; AMINO ACID SYNTHESIS; ARTICLE; BACILLUS SUBTILIS; BACTERIAL GROWTH; BIOTRANSFORMATION; CARBON METABOLISM; CARBON SOURCE; CITRIC ACID CYCLE; CONTROLLED STUDY; ESCHERICHIA COLI; ISOTOPE LABELING; NONHUMAN; NUTRIENT AVAILABILITY; PROTEOMICS; PURINE METABOLISM; RIBOSOME; SUCCINYLATION; GENE EXPRESSION REGULATION; MASS SPECTROMETRY; METABOLISM; PHYSIOLOGY; WESTERN BLOTTING;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA; POSIBACTERIA;

ACETYL COENZYME A; ACETYLATION; ACYL COENZYME A; AMINO ACIDS, BRANCHED-CHAIN; BACILLUS SUBTILIS; BLOTTING, WESTERN; CARBON; CITRIC ACID; GENE EXPRESSION REGULATION, BACTERIAL; LYSINE; MASS SPECTROMETRY; METABOLIC NETWORKS AND PATHWAYS; PROTEOMICS; PURINES; SUCCINIC ACID;

EID: 84939213871     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0131169     Document Type: Article

References (70)

1. Ramakrishnan R, Schuster M, Bourret ARB. Acetylation at Lys-92 enhances signaling by the chemotaxis response regulator protein CheY. Proc Natl Acad Sci USA 1998; 95: 4918-4923. PMID: 9560203
2. Starai VJ, Celic I, Cole RN, Boeke JD, Escalante-Semerena JC. Sir2-dependent activation of acetyl-CoA synthetase by deacetylation of active lysine. Science 2002; 298: 2390-2392. doi: 10.1126/science.1077650 PMID: 12493915
3. Yu BJ, Kim JA, Moon JH, Ryu SE, Pan J-G. The diversity of lysine-acetylated proteins in Escherichia coli. J Microbiol Biotechnol. 2008; 18: 1529-1536. PMID: 18852508
4. Zhang J, Sprung R, Pei J, Tan X, Kim S, Zhu H, et al. Lysine acetylation is a highly abundant and evolutionarily conserved modification in Escherichia coli. Mol Cell Proteomics 2008; 8: 215-225. doi: 10. 1074/mcp.M800187-MCP200 PMID: 18723842
5. Wang Q, Zhang Y, Yang C, Xiong H, Lin Y, Yao J, et al. Acetylation of metabolic enzymes coordinates carbon source utilization and metabolic flux. Science 2010; 327: 1004-1007. doi: 10.1126/science. 1179687 PMID: 20167787
6. Lee DW, Kim D, Lee YJ, Kim JA, Choi JY, Kang S, et al. Proteomic analysis of acetylation in thermophilic Geobacillus kaustophilus. Proteomics 2013; 13: 2278-2282. doi: 10.1002/pmic.201200072 PMID: 23696451
7. Kim D, Yu BJ, Kim JA, Lee YJ, Choi SG, Kang S, et al. The acetylproteome of gram-positive model bacterium Bacillus subtilis. Proteomics 2013; 13: 1726-1736. doi: 10.1002/pmic.201200001 PMID: 23468065
8. Okanishi H, Kim K, Masui R, Kuramitsu S. Acetylome with structural mapping reveals the significance of lysine acetylation in Thermus thermophilus. J Proteome Res. 2013; 12: 3952-3968. doi: 10.1021/pr400245k PMID: 23901841
9. Weinert BT, Iesmantavicius V, Wagner SA, Schölz C, Gummesson B, Beli P, et al. Acetyl-phosphate is a critical determinant of lysine acetylation in E.coli. Mol Cell 2013; 51: 265-272. doi: 10.1016/j.molcel. 2013.06.003 PMID: 23830618
10. Wu X, Vellaichamy A, Wang D, Zamdborg L, Kelleher NL, Huber SC, et al. Differential lysine acetylation profiles of Erwinia amylovora strains revealed by proteomics. J Proteomics 2013; 79: 60-71. doi: 10. 1016/j.jprot.2012.12.001 PMID: 23234799
11. Zhang K, Zheng S, Yang JS, Chen Y, Cheng Z. Comprehensive profiling of protein lysine acetylation in Escherichia coli. J Proteome Res. 2013; 12: 844-851. doi: 10.1021/pr300912q PMID: 23294111
12. Kuhn ML, Zemaitaitis B, Hu LI, Sahu A, Sorensen D, Minasov G, et al. Structural, kinetic and proteomic characterization of acetyl phosphate-dependent bacterial protein acetylation. PLoS ONE 2014; 9: E94816. doi: 10.1371/journal.pone.0094816.s047 PMID: 24756028
13. Liao G, Xie L, Li X, Cheng Z, Xie J. Unexpected extensive lysine acetylation in the trump-card antibiotic producer Streptomyces roseosporus revealed by proteome-wide profiling. J Proteomics 2014; 106: 260-269. doi: 10.1016/j.jprot.2014.04.017 PMID: 24768905
14. Liu F, Yang M, Wang X, Yang S, Gu J, Zhou J, et al. Acetylome analysis reveals diverse functions of lysine acetylation in Mycobacterium tuberculosis. Mol Cell Proteomics 2014; 13: 3352-3366. doi: 10. 1074/mcp.M114.041962 PMID: 25180227
15. Pan J, Ye Z, Cheng Z, Peng X, Wen L, Zhao F. Systematic analysis of the lysine acetylome in Vibrio parahemolyticus. J Proteome Res. 2014; 13: 3294-3302. doi: 10.1021/pr500133t PMID: 24874924
16. Caron CC, Boyault C, Khochbin S. Regulatory cross-talk between lysine acetylation and ubiquitination: Role in the control of protein stability. BioEssays 2005; 27: 408-415. doi: 10.1002/bies.20210 PMID: 15770681
17. Yang X-J, Seto E. Lysine acetylation: Codified crosstalk with other posttranslational modifications. Mol Cell 2008; 31: 449-461. doi: 10.1016/j.molcel.2008.07.002 PMID: 18722172
18. Sadoul K, Boyault C, Pabion M, Khochbin S. Regulation of protein turnover by acetyltransferases and deacetylases. Biochimie 2008; 90: 306-312. doi: 10.1016/j.biochi.2007.06.009 PMID: 17681659
19. Sadoul K, Wang J, Diagouraga B, Khochbin S. The tale of protein lysine acetylation in the cytoplasm. J Biomed Biotechnol. 2011; 2011: 970382. doi: 10.1155/2011/970382 PMID: 21151618
20. Xiong Y, Guan KL. Mechanistic insights into the regulation of metabolic enzymes by acetylation. J Cell Biol. 2012; 198: 155-164. doi: 10.1016/S0092-8674(03)00552-X PMID: 22826120
21. Hu LI, Lima BP, Wolfe AJ. Bacterial protein acetylation: The dawning of a new age. Mol Microbiol. 2010; 77: 15-21. doi: 10.1111/j.1365-2958.2010.07204.x PMID: 20487279
22. Jones JD, O'Connor CD. Protein acetylation in prokaryotes. Proteomics 2011; 11: 3012-3022. doi: 10. 1002/pmic.201000812 PMID: 21674803
23. Kim GW, Yang XJ. Comprehensive lysine acetylomes emerging from bacteria to humans. Trends Biochem Sci. 2011; 36: 211-220. doi: 10.1016/j.tibs.2010.10.001 PMID: 21075636
24. Thao S, Escalante-Semerena JC. Control of protein function by reversible Ne-lysine acetylation in bacteria. Curr Opin Microbiol. 2011; 14: 200-204. doi: 10.1016/j.mib.2010.12.013 PMID: 21239213
25. Wagner GR, Payne RM. Widespread and enzyme-independent Ne-acetylation and Ne-succinylation of proteins in the chemical conditions of the mitochondrial matrix. J Biol Chem. 2013; 288: 29036-29045. doi: 10.1074/jbc.M113.486753 PMID: 23946487
26. AbouElfetouh A, Kuhn ML, Hu LI, Scholle MD, Sorensen DJ, Sahu AK, et al. The E.coli sirtuin CobB shows no preference for enzymatic and nonenzymatic lysine acetylation substrate sites. MicrobiologyOpen 2014; 4: 66-83. doi: 10.1002/mbo3.223 PMID: 25417765
27. Chen Y, Sprung R, Tang Y, Ball H, Sangras B, Kim SC, et al. Lysine propionylation and butyrylation are novel post-translational modifications in histones. Mol Cell Proteomics 2007; 6: 812-819. doi: 10.1074/mcp.M700021-MCP200 PMID: 17267393
28. Zhang Z, Tan M, Xie Z, Dai L, Chen Y, Zhao Y. Identification of lysine succinylation as a new post-translational modification. Nature Chem Biol. 2010; 7: 58-63. doi: 10.1038/nchembio.495
29. Peng C, Lu Z, Xie Z, Cheng Z, Chen Y, Tan M, et al. The first identification of lysine malonylation substrates and its regulatory enzyme. Mol Cell Proteomics 2011; 10: M111.012658. doi: 10.1074/mcp. M111.012658-1
30. Tan M, Luo H, Lee S, Jin F, Yang JS, Montellier E, et al. Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell 2011; 146: 1016-1028. doi: 10.1016/j.cell.2011.08.008 PMID: 21925322
31. Tan M, Peng C, Anderson KA, Chhoy P, Xie Z, Dai L, et al. Lysine glutarylation is a protein posttranslational modification regulated by SIRT5. Cell Metabolism 2014; 19: 605-617. doi: 10.1016/j.cmet.2014. 03.014 PMID: 24703693
32. Garrity J, Gardner JG, Hawse W, Wolberger C, Escalante-Semerena JC. N-lysine propionylation controls the activity of propionyl-CoA synthetase. J Biol Chem. 2007; 282: 30239-30245. doi: 10.1074/jbc. M704409200 PMID: 17684016
33. Colak G, Xie Z, Zhu AY, Dai L, Lu Z, Zhang Y, et al. Identification of lysine succinylation substrates and the succinylation regulatory enzyme CobB in Escherichia coli. Mol Cell Proteomics 2013; 12: 3509-3520. doi: 10.1074/mcp.M113.031567 PMID: 24176774
34. Okanishi H, Kim K, Masui R, Kuramitsu S. Lysine propionylation is a prevalent post-translational modification in Thermus thermophilus. Mol Cell Proteomics 2014; 13: 2382-2398. doi: 10.1074/mcp.M113. 035659 PMID: 24938286
35. Vallari DS, Jackowski S, Rock CO. Regulation of pantothenate kinase by coenzyme A and its thioesters. J Biol Chem. 1987; 262: 2466-2471.
36. Weinert BT, Schölz C, Wagner SA, Iesmantavicius V, Su D, Daniel JA, et al. Lysine succinylation is a frequently occurring modification in prokaryotes and eukaryotes and extensively overlaps with acetylation. Cell Reports 2013; 4: 842-851. doi: 10.1016/j.celrep.2013.07.024 PMID: 23954790
37. Gardner JG, Grundy FJ, Henkin TM, Escalante-Semerena JC. Control of acetyl-coenzyme A synthetase (AcsA) activity by acetylation/deacetylation without NAD+ involvement in Bacillus subtilis. J Bacteriol. 2006; 188: 5460-5468. doi: 10.1128/JB.00215-06 PMID: 16855235
38. Gardner JG, Escalante-Semerena JC. 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. 2008; 190: 5132-5136. doi: 10.1128/JB.00340-08 PMID: 18487328
39. Gardner JG, Escalante-Semerena JC. 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 coenzyme A synthetase. J Bacteriol. 2009; 191: 1749-1755. doi: 10.1128/JB.01674-08 PMID: 19136592
40. Guan K-L, Xiong Y. Regulation of intermediary metabolism by protein acetylation. Trends Biochem Sci. 2011; 36: 108-116. doi: 10.1016/j.tibs.2010.09.003 PMID: 20934340
41. Chubukov V, Uhr M, Le Chat L, Kleijn RJ, Jules M, Link H, et al. Transcriptional regulation is insufficient to explain substrate-induced flux changes in Bacillus subtilis. Mol Syst Biol. 2013; 9: 709. doi: 10.1038/msb.2013.66 PMID: 24281055
42. Buescher JM, Liebermeister W, Jules M, Uhr M, Muntel J, Botella E, et al. Global network reorganization during dynamic adaptations of Bacillus subtilis metabolism. Science 2012; 335: 1099-1103. doi: 10.1126/science.1206871 PMID: 22383848
43. Nicolas P, Mäder U, Dervyn E, Rochat T, Leduc A, Pigeonneau N, et al. Condition-dependent transcriptome reveals high-level regulatory architecture in Bacillus subtilis. Science 2012; 335: 1103-1106. doi: 10.1126/science.1206848 PMID: 22383849
44. Yano K, Wada T, Suzuki S, Tagami K, Matsumoto T, Shiwa Y, et al. Multiple rRNA operons are essential for efficient cell growth and sporulation as well as outgrowth in Bacillus subtilis. Microbiology 2013; 159: 2225-2236. doi: 10.1099/mic.0.067025-0 PMID: 23970567
45. Imamura D, Kobayashi K, Sekiguchi J, Ogasawara N, Takeuchi M, Sato T. spoIVH (ykvV), a requisite cortex formation gene, is expressed in both sporulating compartments of Bacillus subtilis. J Bacteriol. 2004; 186: 5450-5459. doi: 10.1128/JB.186.16.5450-5459.2004 PMID: 15292147
46. Itaya M, Kondo K, Tanaka T. A neomycin resistance gene cassette selectable in a single copy state in the Bacillus subtilis chromosome. Nucleic Acids Res. 1989; 17: 4410. doi: 10.1093/nar/17.11.4410 PMID: 2500645
47. Toda T, Tanaka T, Itaya M. A method to invert DNA segments of the Bacillus subtilis 168 genome by recombination between two homologous sequences. Biosci Biotechnol Biochem. 1996; 60: 773-778. doi: 10.1271/bbb.60.773 PMID: 8704305
48. Tagami K, Nanamiya H, Kazo Y, Maehashi M, Suzuki S, Namba E, et al. Expression of a small (p) ppGpp synthetase, YwaC, in the (p)ppGpp0 mutant of Bacillus subtilis triggers YvyD-dependent dimerization of ribosome. MicrobiologyOpen 2012; 1: 115-134. doi: 10.1002/mbo3.16 PMID: 22950019
49. Guan KL, Yu W, Lin Y, Xiong Y, Zhao S. Generation of acetyllysine antibodies and affinity enrichment of acetylated peptides. Nature Protocols 2010; 5: 1583-1595. doi: 10.1038/nprot.2010.117 PMID: 21085124
50. Silva JC, Gorenstein MV, Li GZ, Vissers JPC, Geromanos SJ. Absolute quantification of proteins by LCMSE. Mol Cell Proteomics 2006; 5: 144-156. doi: 10.1074/mcp.M500230-MCP200 PMID: 16219938
51. Vizcaino JA, Cote RG, Csordas A, Dianes JA, Fabregat A, Foster JM, et al. The proteomics identifications (PRIDE) database and associated tools: Status in 2013. Nucleic Acids Res. 2012; 41: D1063-D1069. doi: 10.1093/nar/gks1262 PMID: 23203882
52. Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols 2009; 4: 44-57. doi: 10.1038/nprot.2008.211 PMID: 19131956
53. Colaert N, Helsens K, Martens L, Vandekerckhove J, Gevaert K. Improved visualization of protein consensus sequences by iceLogo. Nature Methods 2009; 6: 786-787. doi: 10.1038/nmeth1109-786 PMID: 19876014
54. Schwartz D, Gygi SP. An iterative statistical approach to the identification of protein phosphorylation motifs from large-scale data sets. Nature Biotechnol. 2005; 23: 1391-1398. doi: 10.1038/nbt1146
55. Castano-Cerezo S, Bernal V, Post H, Fuhrer T, Cappadona S, Sanchez-Diaz NC, et al. Protein acetylation affects acetate metabolism, motility and acid stress response in Escherichia coli. Mol Syst Biol. 2014; 10: 762-762. doi: 10.15252/msb.20145227 PMID: 25518064
56. Zhao S, Xu W, Jiang W, Yu W, Lin Y, Zhang T, et al. Regulation of cellular metabolism by protein lysine acetylation. Science 2010; 327: 1000-1004. doi: 10.1126/science.1179689 PMID: 20167786
57. Rardin MJ, Newman JC, Held JM, Cusack MP, Sorensen DJ, Li B, et al. Label-free quantitative proteomics of the lysine acetylome in mitochondria identifies substrates of SIRT3 in metabolic pathways. Proc Natl Acad Sci USA 2013; 110: 6601-6606. doi: 10.1073/pnas.1302961110 PMID: 23576753
58. Lima BP, Antelmann H, Gronau K, Chi BK, Becher D, Brinsmade SR, et al. Involvement of protein acetylation in glucose-induced transcription of a stress-responsive promoter. Mol Microbiol. 2011; 81: 1190-1204. doi: 10.1111/j.1365-2958.2011.07742.x PMID: 21696463
59. Lima BP, Thanh Huyen TT, Basell K, Becher D, Antelmann H, Wolfe AJ. Inhibition of acetyl phosphatedependent transcription by an acetylatable lysine on RNA polymerase. J Biol Chem. 2012; 287: 32147-32160. doi: 10.1074/jbc.M112.365502 PMID: 22829598
60. Vassylyev DG, Sekine SI, Laptenko O, Lee J, Vassylyeva MN, Borukhov S, et al. Crystal structure of a bacterial RNA polymerase holoenzyme at 2.6 Å resolution. Nature 2002; 417: 712-719. doi: 10.1038/nature752 PMID: 12000971
61. Murakami KS. X-ray crystal structure of Escherichia coli RNA polymerase s70 holoenzyme. J Biol Chem. 2013; 288: 9126-9134. doi: 10.1074/jbc.M112.430900 PMID: 23389035
62. Grundy FJ, Waters DA, Allen SH, Henkin TM. Regulation of the Bacillus subtilis acetate kinase gene by CcpA. J Bacteriol. 1993; 175: 7348-7355. PMID: 8226682
63. Presecan-Siedel E, Galinier A, Longin R, Deutscher J, Danchin A, Glaser P, et al. Catabolite regulation of the pta gene as part of carbon flow pathways in Bacillus subtilis. J Bacteriol. 1999; 181: 6889-6897. PMID: 10559153
64. Wanner BL, Wilmes-Riesenberg MR. Involvement of phosphotransacetylase, acetate kinase, and acetyl phosphate synthesis in control of the phosphate regulon in Escherichia coli. J Bacteriol. 1992; 174: 2124-2130. PMID: 1551836
65. Chang YY, Cronan JE Jr. Genetic and biochemical analyses of Escherichia coli strains having a mutation in the structural gene (poxB) for pyruvate oxidase. J Bacteriol. 1983; 154: 756-762. PMID: 6341362
66. Grabau C, Cronan JE Jr. Molecular cloning of the gene (poxB) encoding the pyruvate oxidase of Escherichia coli, a lipid-activated enzyme. J Bacteriol. 1984; 160: 1088-1092. PMID: 6209262
67. Pericone CD, Park S, Imlay JA, Weiser JN. Factors contributing to hydrogen peroxide resistance in Streptococcus pneumoniae include pyruvate oxidase (SpxB) and avoidance of the toxic effects of the fenton reaction. J Bacteriol. 2003; 185: 6815-6825. doi: 10.1128/JB.185.23.6815-6825.2003 PMID: 14617646
68. Ramos-Montanez S, Kazmierczak KM, Hentchel KL, Winkler ME. Instability of ackA (acetate kinase) mutations and their effects on acetyl phosphate and ATP amounts in Streptococcus pneumoniae D39. J Bacteriol. 2010; 192: 6390-6400. doi: 10.1128/JB.00995-10 PMID: 20952579
69. Schröder S, Herker E, Itzen F, He D, Thomas S, Gilchrist DA, et al. Acetylation of RNA polymerase II regulates growth-factor-induced gene transcription in mammalian cells. Mol Cell 2013; 52: 314-324. doi: 10.1016/j.molcel.2013.10.009 PMID: 24207025
70. Hirschey MD, Zhao Y. Metabolic regulation by lysine malonylation, succinylation and glutarylation. Mol Cell Proteomics 2015; R114.046664. doi: 10.1074/mcp.R114.046664