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Volume 7, Issue 6, December Issue - 2019, Pages:521-528


Authors: Bassam Oudh Al johny
Abstract: Post-translational changes including acetylation are universal phenomena in protein and occur in both prokaryotes and eukaryotes. The process of post-translation modifications is initiated by phosphorylation of the acetyl group through an enzymatic pathway using the acetyltransferase enzyme. It is believed that several processes such as cellular process, DNA replication, bacterial chemotaxis and metabolism depend on protein acetylation. It is worth to say that protein acetylation is extremely important in bacterial virulence, as diverse factors have been involved in bacterial virulence. Therefore, current review article summarizes the role of protein acetylation, its mechanism, techniques of acetylome study and its regulation, which may help in the in-depth understanding of bacterial virulence. 
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Full Text: 1 Introduction There are enzymatic and non-enzymatic mechanisms for the regulation of acetylation as manifested in Figure 1. It is believed that during the enzymatic pathway of eN-acetylation the e-amino group of a deprotonated lysine received acetyl group from acetyl COA that is catalyzed by lysine acetyltransferase (KAT) enzyme (Jie Ren et al., 2017). There are three major categories of KATs which are (i) the Gcn5 which belongs to the family N-acetyltransferase (GNAT) (so-called after the Gcn5 protein of yeast), (ii) the family MYST (called after human MOZ, yeast Ybf2/Sas3, yeast Sas2, and human Tip60), and (iii) the p300/CBP family (named after human hp300 and hCBP). The family of GNAT is available in all sectors of life and MYST and p300/CBP are recognized merely in eukaryotic cells (Starai & Escalante-Semerena, 2004; Garrity et al., 2007; Wang et al., 2010). It is reported that different kind of KATs belonging to the same GNAT family have been known from several microorganisms (Thao & Escalante-Semerena., 2011). 2 Protein Acetylation Mechanism in Bacteria Among different KATs, acetyltransferase Pat of the Salmonella enterica protein was the most studied and first recognized protein (Garrity et al., 2007; Sang et al., 2016). In E.coli it has been reported that during a nonenzymatic mechanistic pathway the deprotonated lysine e-amino group received an acetyl group from acetyl phosphate (AcP) (Weinert et al., 2013; Kuhn et al., 2014). AcP is considered as the high energy intermediate where a phosphoryl moiety is best owing in a two component signal transduction process to particular response regulators (Lukat et al., 1992). The yfiQ deletion mutant has less effects on acetylation levels, while increasing AcP concentration will further increase the global acetylation (Weinert et al., 2013; Kuhn et al., 2014). In regulating the bacterial physiological progression, acetylation due to enzyme is more significant as compared to acetylation due to AcP, because there is a direct relation between AcP and global acetylation concentration, while the negligible effect on global acetylation due to the deletion of vfiQ mutant. Enzymatically the lysine deacetylases (KDACs) can remove the acetyl group. KDACs have been classified into two groups and four classes, which are as (i) Class III based on NAD+ dependent sirtuin family (Blander & Guarente, 2014) and (ii) Classes I, II, and IV based on zinc-dependent Rpd3/Hda1 family (Yang & Seto., 2008). NAD+-dependent Cob B, was initially reported in S. enterica and was largely studied in various bacterial strains (Starai et al.,2002), however, its homologs were also identified in other species of bacteria such as Bacillus subtilis (Gardner & Escalante-Semerena.,2009), Streptomyces coelicolor (Mikulik et al., 2012), E. coli (Zhao et al., 2004), and Rhodopseudomonas palustris (Crosby et al.,2010). Usually, CobB substrates take part in various cellular processes and giving no importance for AcP-dependent or acetylated lysines depends on Pat (AbouElfetouh et al., 2015). For instance, the CobB possibly deacetylate the AcP and Pat dependent acetylated DNA (Zhang  et al.,2016) and was believed that in E. coli the CobB was merelythe histone deacetylase (HDAC). The research group of Tu et al. (2015) recognized the discovery of deacetylase YcgCin in E. coli which was related to the hydrolase family of serine. However, it had  non-significant homology with KDACs which were not dependent on Zn2+ or NAD+ known KDACs. In E. coli the YcgC have different catalyzed pathway for substrates deacetylases as well as different substrate as compared to CobB-regulated acetylated proteins. The auto ADP-ribosyltransferase and deacetylase potential of MSMEG_4620 was established in Mycobacterium smegmatis with the identification of MSMEG_4620 and SIRT4 homologue (Tan et al., 2015). Therefore, this study will open new ideas and explore the relationship between deacetylases and acetylation factors as well as novel bacterial deacetylases knowledge. 3 Protein Acetylome in Bacteria The use of antibodies in the acetylated peptides with great specificity involved in immunoprecipitation which largely increases the ability to identify more acetylated lysine residues (Wang et al.,2010; Chen et al., 2012). In this method the quality and amount of acetylated proteins largely depend on various factors including immunoprecipitation efficacy, anti-acetyllysine antibodies quality, strategies established for the fractionation of various sample, mass spectrometry (MS) techniques, software packages used for data acquisition (Mischerikow &Heck.,2011). Acetylome was the first published protein discovered in bacteria. After that, Yu et al. (2008) applied a hyphenated technique comprising of affinity immune-separation technique coupled with nano HPLC/MS/MS by using an anti-acetyllysine antibody for the identification of 125 acetylated sites among 85 different proteins in E. coli. Furthermore, E. coli comprises of 79 proteins where 81 phosphorylation sites and number of acetylated proteins was found to analogous (Macek et al., 2008). A vast detail on the Protein acetylome are available for different bacterial species (Hentchel & Escalante-Semerena, 2015). Most noticeable literature on the acetylome of pathogens are available on Spiroplasma eriocheiris (Liu et al., 2014; Xie et al., 2015; Meng et al., 2016), Porphyromonas gingivalis (Butler et al.,2015), Vibrio parahemolyticus (Pan et al.,2014), and Pseudomonas aeruginosa (Ouidir et al.,2015) and this help in the in-depth understanding of acetylated regulation bacterial virulence. The V. parahemolyticus, 517 succinyllysine sites (26.7%) on 288 proteins (44.9%) was also reported to acetylate (Pan et al., 2015), proposing the general intersection between acetylation and other PTMs enrich levels of regulation and are operating in different cellular practices. There are approximately 2000–5000 proteins in a typical bacterial proteome and among all of them 5% acetylated (Kim &Yang. 2011), but the acetylated proteins percentage is variable ranging from 2-45% depends on the bacterial species. It is also reported that the acetylated proteins is diverse in the same bacterium under different environments and laboratory conditions displayed no satisfactory replicability (Yu et al., 2008; Zhang et al., 2009). This phenomenon required high-throughput analyses to authenticate the experimental data, by avoiding any fabricated outcomes, and to validate the physiological significance in vivo of the acetylated proteins. 4 Mass spectrometry opens avenues for acetylation research Mass spectrometry studies in proteomic are one of the most emerging analysis techniques to determined acetylation. This practice have been applied either for global studies related to target protein analysis for cellular acetylomes determination under diverse conditions in diverse microbial species. In target analyses for instance, protein purification involved the purification of sample through immune affinity methods, and then digested by protease and fragmentation analysis was carried out by Mass spectrometry of the resultant peptides leads to the identification of acetylated sites (Barak & Eisenbach, 2001; Starai et al., 2002; Zhou et al., 2015; Zhang et al., 2016). Under particular conditions protein extraction is the initial step for the acetylome studies, in this the entire proteome digested by enzymatic action and then mass spectrometry was used for the analysis of acetylated peptides enriched with anti-acetyl-lysine antibodies. The degree of peptides acetylation depends on the specificity and affinity of antibodies and sensitivity of mass spectrometer. Many methods have been developed in order to increase the isolation efficiency of peptides, reduction in certain acetylation motifs applied several antibodies to captured acetyl-peptide (Macek et al., 2008; Crosby et al., 2010; Lee et al., 2013; Pan et al., 2014; AbouElfetouh et al ., 2015; Tu et al., 2015; Meng et al., 2016). Many procedure and protocols have been developed for isolation but still only between 25 to 40% isolation has been reported. Therefore, it is utmost to enhanced and improve the isolation efficacy and determination of acetylation sites in various protein (Mouslim et al., 2004; Meng et al., 2016). Lower abundance proteins identification might be improved by fractionations of peptides before capturing the acetyl-peptide, which in turn help to reduce the complexities originated in peptide identifications (AbouElfetouh et al., 2015; Xie et al., 2015; Pan et al., 2015; Zhang et al., 2016; Meng et al., 2016). Improvement in the proteome sectors might be improved with the improvement, development, and sensitivity of mass spectrometer. 4.1 Use of mass spectrometry for in-vivo studies for functional authentications Substitutions of amino acid such as Gln, Arg, and Ala and removal of protein i.e., KATs or sirtuins relied during the investigation of in-vivo studies. The impact of KATs or KDACs/sirtuins to a specific process of acetylation is usually evaluated through deletions, and the function of a specific site can be assessing through point mutants and side chain contribution through Ala substitutions. The side chain contribution is assessed by Ala substation Arg substitutions domain the positive charge without acetylation, so they copy the unacetylated state. The acetylated forms can be mimic from Gln substitutions, because of neutral charge and inability to acetylate (Kamieniarz & Schneider., 2009). These mutations might play an important role in acetylation at specific sites, for instance, during in vivo studies the influence of mutations on the function of protein can be assessed by reporter assays, such as transcriptional fusions to a transcription factors target genes. It is worth to say that data analysis can be performed with extreme cautions because the side chains are chemically different in acetyllysine, Lys, Gln, Ala, and Arg, and with the induction of other amino acid to the protein chain the whole properties such as secondary structure and stability of the protein chain might be greatly affect (Zhang et al., 2013). Furthermore, mutation that leads in a loss-of function phenotype will possibly measure the incorrect contribution of acetylation. Most of the sites is 1% acetylated so will not reproduced in vivo stoichiometry because the stoichiometry of a mutation is 100% (Barak & Eisenbach., 2001; Meyer et al.,2016; Weinert et al., 2017). The physiological effect of a specific acetylation is necessary to investigate in order to exactly determine the stoichiometry of acetylation for the loss-of-function mutations in brief the substation is very important in determining the role of acetylation in vivo studies, but still it is worthwhile that efficacy of such substation is variable in different proteins. For instance, Gln substitutions were found to recapitulate the impact of acetylation in vitro (Simonsson et al., 2006; Wang & Hayes, 2008) and in vivo studies in eukaryotic (Hecht  et al.,1995; Li et al.,2002; Yang et al.,2008), but it is different for different proteins (Sun et al.,2007; Kawai et al.,2011;). Any in vivo results can be supported by integration with in vitro studies. 4.2 Observing in vivo studies through in vitro verifications In vitro studies are helpful in order to examine the in-depth mechanism of acetylation (Barak & Eisenbach., 2001; Thao et al., 2010;Okanishi et al., 2013; Kuhn et al., 2014; Liao et al., 2014; Vergnolle et al., 2016; Song et al., 2016). Acetyl phosphate or acetyl-CoA leads to acetylation in substrates that go through nonenzymatic acetylation. In the in vitro studies, a specific target is acetylated by the purified KATs and deacetylate by deacetylases. Mass spectrometer and radioactive acetyl derivatives addition or deletion can be used to determine the specific sites for acetylation. During in vitro studies the promiscuous in acetylases are often created problem in analysis interpretation (Barak & Eisenbach., 2001), However, this problem could be resolved during in vitro studies by using the Gln substitution mutants isolated from E. coli (Sun et al., 2016; Qin et al., 2016), Interestingly a proteins acetylation can also be achieved through coevolved tRNA-tRNA synthetase pair present in E. coli strain which inserts acetyllysine after amber codon is read (Neumann et al., 2009), as a result, 100% site-specific acetylated protein used in biochemical analyses of in vitro function, till-date no explanatory data are available for the in vivo acetylation. The use of mass spectrometry in vitro and in vivo studies may potentially helped in understating the site-specific acetylation in various proteins. 5 Bacterial virulence regulation through acetylation of protein Various acetylomes of bacterial pathogens has been determined various virulence, but whether the virulence factor is acetylated or not is an area of curiosity. For a curiosity several studies have been put forward, which result that virulence is regulated by the acetylation of protein. 5.1 Bacterial Chemotaxis is regulated by Acetylation In 2004 CheY was identified and explored that it has an important functions in the excitatory response of bacterial chemotaxis (Barak et al., 2004; Kuhn et al., 2014). The lysine acetylated residues has adverse impacts such as aspartyl residue phosphorylation, rotational direction of flagellar, flagellar switch complex formation with kinase CheA, phosphatase CheZ, and the switch protein Film (Barak & Eisenbach, 2001; Barak & Eisenbach., 2004; Yan et al., 2008; Li et al.,2010; Liarzi et al., 2010). It is believed that acetylation is very important for the proper performance of CheY, therefore, acetylation is responsible for the regulation of bacterial virulence. The CheY acetylation has been studied in nonpathogenic strains of E. coli, therefore, it can be suggest that cheY acetylation might have a positive role in bacterial virulence. The involvement of CheY acetylation in bacterial virulence has been also reported in Campylobacter jejuni and Listeria monocytogenes (Yao et al., 1997; Dons et al., 2004). Similarly, involvement of RcsB in Salmonella and Erwinia amylovora virulence has been also reported by various researchers (Bereswill & Geider, 1997; Domínguez et al., 2004; Liao et al., 2014). Furthermore, acetylation is extremely important in the regulation of RcsB potential in E. coli (Thao et al., 2010), bacterial motility, lysine acetylation, impact on the biosynthesis of flagella and diminishing acid stress survival (Castaño et al., 2014). 5.2 Homeostasis of Acetylation process and its Influences on Bacterial Acid Resistance Typhimurium and S. enterica serovar are enteric pathogens that have strong resistance to pH and survive in stomach in the strong acidic medium of pH 2. These bacteria may also attack on other organs of the body such as liver, spleen and epithelium layer of intestine (Drecktrah et al., 2006). The transcriptional levels of pat and the genes Crp and CyaA encoded cyclic AMP receptor protein and adenylate cyclase and are down regulated due to the acidic environment as suggested from the transcriptome patterns. Higher survival rate and higher intracellular pH has been reported under acid stress conditions for the pat deletion mutant than the wild-type strain (Ren et al., 2015). The above discussion inferred that bacterial and other pathogenic virulence response to acidic environment is regulated by acetylation. It is concluded from the above discussion that acetylation is the key for regulating and contributing the bacterial, enteric and pathogenic virulence to acid stress and resistance.   Conflict of Interest The authors declare that there is no conflict of interest.
REFERENCES

AbouElfetouh A, Kuhn ML, Hu LI, Scholle MD, Sorensen DJ, Sahu AK, Becher D, Antelmann H, Mrksich M, Anderson WF (2015) The E. coli sirtuin CobB shows no preference for enzymatic and nonenzymatic lysine acetylation substrate sites. Microbiology Open 4: 66-83.

Barak R, Eisenbach M (2001) Acetylation of the response regulator, CheY, is involved in bacterial chemotaxis. Molecular Microbiology 40: 731-743.

Barak R, Eisenbach M (2004) Co-regulation of acetylation and phosphorylation of CheY, a response regulator in chemotaxis of Escherichia coli. Journal of Molecular Biology342: 375-381.

Barak R, Prasad K, Shainskaya A, Wolfe AJ, Eisenbach M (2004) Acetylation of the chemotaxis response regulator CheY by acetyl-CoA synthetase purified from Escherichia coli. Journal of Molecular Biology 342: 383-401.

Bereswill S, Geider K (1997) Characterization of the rcsB gene from Erwinia amylovora and its influence on exoploysaccharide synthesis and virulence of the fire blight pathogen. Journal of Bacteriology 179: 1354-1361.

Blander G, Guarente L (2014) The Sir2 family of protein deacetylases. Annual Review of Biochemistry 73: 417-435.

Butler CA, Veith PD, Nieto MF, Dashper SG, Reynolds EC (2015) Lysine acetylation is a common post-translational modification of key metabolic pathway enzymes of the anaerobe Porphyromonas gingivalis. Journal of Proteomics 128: 352-364.

Castaño?Cerezo S, Bernal V, Post H, Fuhrer T, Cappadona S, Sánchez?Díaz NC, Sauer U, Heck AJ, Altelaar AM, Cánovas M (2014) Protein acetylation affects acetate metabolism, motility and acid stress response in Escherichia coli. Molecular Systems Biology 10: 762.

Chen Y, Zhao W, Yang JS, Cheng Z, Luo H, Lu Z, Tan M, Gu W, Zhao T (2012) Quantitative acetylome analysis reveals the roles of SIRT1 in regulating diverse substrates and cellular pathways. Molecular and Cellular Proteomics 11: 1048-1062.

Crosby HA, Heiniger EK, Harwood CS, Escalante?Semerena JC (2010) Reversible Nε-lysine acetylation regulates the activity of acyl?CoA synthetases involved in anaerobic benzoate catabolism in Rhodopseudomonas palustris. Molecular Microbiology 76: 874-888.

Domínguez?Bernal G, Pucciarelli MG, Ramos?Morales F, García?Quintanilla M, Cano DA, Casadesús J, García?del Portillo F (2004) Repression of the RcsC?YojN?RcsB phosphorelay by the IgaA protein is a requisite for Salmonella virulence. Molecular Microbiology 53: 1437-1449.

Dons L, Eriksson E, Jin Y, Rottenberg ME, Kristensson K, Larsen CN, Bresciani J, Olsen JE (2004) Role of flagellin and the two-component CheA/CheY system of Listeria monocytogenes in host cell invasion and virulence. Infection and Immunity 72: 3237-3244.

Drecktrah D, Knodler LA, Ireland R, Steele?Mortimer O (2006) The mechanism of Salmonella entry determines the vacuolar environment and intracellular gene expression. Traffic 7: 39-51.

Gardner JG, Escalante-Semerena JC (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 coenzyme A synthetase. Journal of Bacteriology 191: 1749-1755.

Garrity J, Gardner JG, Hawse W, Wolberger C, Escalante-Semerena JC (2007) N-lysine propionylation controls the activity of propionyl-CoA synthetase. Journal of Biological Chemistry 282: 30239-30245.

Hecht A, Laroche T, Strahl-Bolsinger S, Gasser SM, Grunstein M (1995) Histone H3 and H4 N-termini interact with SIR3 and SIR4 proteins: a molecular model for the formation of heterochromatin in yeast. Cell 80: 583–592.

Hentchel KL, Escalante-Semerena JC (2015) Acylation of biomolecules in prokaryotes: a widespread strategy for the control of biological function and metabolic stress. Microbiology and Molecular Biology Reviews 79: 321-346.

Jie Ren, Yu Sang, Jie Lu, Yu-Feng Yao (2017) Protein Acetylation and Its Role in Bacterial Virulence. Trends in Microbiology 25: 768-779.

Kamieniarz K, Schneider R (2009) Tools to tackle protein acetylation. Chemistry and Biology 16: 1027–1029.

Kawai Y, Garduno L, Theodore M, Yang J, Arinze IJ (2011) Acetylation deacetylation of the transcription factor Nrf2 (nuclear factor erythroid 2-related factor 2) regulates its transcriptional activity and nucleocytoplasmic localization. The Journal of Biological Chemistry 286: 7629 –7640.

Kim GW, Yang XJ (2011) Comprehensive lysine acetylomes emerging from bacteria to humans. Trends in Biochemical Sciences 36: 211-220.

Kuhn ML, Zemaitaitis B, Hu LI, Sahu A, Sorensen D, Minasov G, Lima BP, Scholle M, Mrksich M, Anderson WF, Gibson BW, Schilling B, Wolfe AJ (2014) Structural, kinetic and proteomic characterization of acetyl phosphate-dependent bacterial protein acetylation. PLoSOne 9: 94816.

Lee DW, Kim D, Lee YJ, Kim JA, Choi JY, Kang S, Pan JG (2013) Proteomic analysis of acetylation in thermophilic Geobacillus kaustophilus. Proteomics 13: 2278 –2282.

Li M, Luo J, Brooks CL, Gu W (2002) Acetylation of p53 inhibits its ubiquitination by Mdm2. The Journal of Biological Chemistry 277: 50607–50611.

Li R, Gu J, Chen YY, Xiao CL, Wang LW, Zhang ZP, Bi LJ, Wei HP, Wang XD, Deng GY (2010) CobB regulates Escherichia coli chemotaxis by deacetylating the response regulator CheY. Molecular Microbiology 76: 1162-1174.

Liao G, Xie L, Li X, Cheng Z, Xie J (2014) Unexpected extensive lysine acetylation in the trump-card antibiotic producer Streptomyces roseosporus revealed by proteome-wide profiling. Journal of Proteomics 106: 260-269.

Liarzi O, Barak R, Bronner V, Dines M, Sagi Y, Shainskaya A, Eisenbach M (2010) Acetylation represses the binding of CheY to its target proteins. Molecular Microbiology 76: 932-943.

Liu F, Yang M, Wang X, Yang S, Gu J, Zhou J, Zhang XE, Deng J, Ge F (2014) Acetylome analysis reveals diverse functions of lysine acetylation in Mycobacterium tuberculosis. Molecular and  Cellular Proteomics 13: 3352-3366.

Lukat GS, McCleary WR, Stock AM, Stock JB (1992) Phosphorylation of bacterial response regulator proteins by low molecular weight phospho-donors. Proceedings of the National Academy of Sciences 89: 718-722.

Macek B, Gnad F, Soufi B, Kumar C, Olsen JV, Mijakovic I, Mann M (2008) Phosphoproteome analysis of E. coli reveals evolutionary conservation of bacterial Ser/Thr/Tyr phosphorylation. Molecular and Cellular Proteomics 7: 299-307.

Meng Q, Liu P, Wang J, Wang Y, Hou L, Gu W, Wang W (2016) Systematic analysis of the lysine acetylome of the pathogenic bacterium Spiroplasma eriocheiris reveals acetylated proteins related to metabolism and helical structure, Journal of Proteomics 148: 159-169.

Meyer JG, D’Souza AK, Sorensen DJ, Rardin MJ, Wolfe AJ, Gibson BW, Schilling B (2016) Quantification of lysine acetylation and succinylation stoichiometry in proteins using mass spectrometric data-independent acquisitions (SWATH). Journal of the American Society for Mass Spectrometry 27: 1758 –1771.

Mikulik K, Felsberg J, Kudrná?ová E, Bezoušková S, Šetinová D, Stod?lková E, Zidkova J, Zidek V (2012) CobB1 deacetylase activity in Streptomyces coelicolor. Biochemistry and Cell Biology 90: 179-187.

Mischerikow N, Heck AJ (2011) Targeted large?scale analysis of protein acetylation. Proteomics 11: 571-589.

Mouslim C, Delgado M, Groisman EA (2004) Activation of the RcsC/YojN/RcsB phosphorelay system attenuates Salmonella virulence. Molecular Microbiology 54: 386-395.

Neumann H, Hancock SM, Buning R, Routh A, Chapman L, Somers J, Owen-Hughes T, van Noort J, Rhodes D, Chin JW (2009) A method for genetically installing site-specific acetylation in recombinant histories defines the effects of H3 K56 acetylation. Molecular Cell 36: 153–163.

Okanishi H, Kim K, Masui R, Kuramitsu S (2013) Acetylome with structural mapping reveals the significance of lysine acetylation in Thermus thermophilus. Journal of Proteome Research 12: 3952-3968.

Ouidir T, Cosette P, Jouenne T, Hardouin J (2015) Proteomic profiling of lysine acetylation in Pseudomonas aeruginosa reveals the diversity of acetylated proteins. Proteomics 15: 2152-2157.

Pan J, Chen R, Li C, Li W, Ye Z (2015) Global analysis of protein lysine succinylation profiles and their overlap with lysine acetylation in the marine bacterium Vibrio parahemolyticus. Journal of Proteome Research 14: 4309-4318.

Pan J, Ye Z, Cheng Z, Peng X, Wen L, Zhao F (2014) Systematic analysis of the lysine acetylome in Vibrio parahemolyticus. Journal of Proteome Research 13: 3294-3302.

Qin R, Sang Y, Ren J, Zhang Q, Li S, Cui Z, Yao YF (2016) The bacterial two-hybrid system uncovers the involvement of acetylation in regulating of lrp activity in Salmonella Typhimurium. Frontiers in Microbiology 7: 261896.

Ren J, Sang Y, Ni J, Tao J, Lu J, Zhao M, Yao YF (2015) Acetylation regulates survival of Salmonella enterica Serovar Typhimurium under acid stress. Applied and Environmental Microbiology 81: 5675-5682.

Sang Y, Ren J, Ni J, Tao J, Lu J, Yao YF (2016) Protein acetylation is involved in Salmonella enterica Serovar Typhimurium virulence. The Journal of Infectious Diseases 213: 1836 –1845.

Simonsson M, Kanduri M, Gronroos E, Heldin CH, Ericsson J (2006) The DNA binding activities of Smad2 and Smad3 are regulated by coactivator-mediated acetylation. Journal of Biological Chemistry 281: 39870 –39880.

Song L, Wang G, Malhotra A, Deutscher MP, Liang W (2016) Reversible acetylation on Lys501 regulates the activity of RNase II. Nucleic Acids Research 44: 1979 –1988.

Starai V, Celic I, Cole RN, Boeke J, Escalante-Semerena J (2002) Sir2-dependent activation of acetyl-CoA synthetase by deacetylation of active lysine. Science298: 2390-2392.

Starai VJ, Escalante-Semerena JC (2004) Identification of the protein acetyltransferase (Pat) enzyme that acetylates acetyl-CoA synthetase in Salmonellaenterica. Journal of Molecular Biology 340: 1005-1012.

Sun M, Guo H, Lu G, Gu J, Wang X, Zhang XE, Deng J (2016) Lysine acetylation regulates the activity of Escherichia coli S-adenosylmethionine synthase. Acta Biochimica et Biophysica Sinica 48: 723–731.

Sun Y, Xu Y, Roy K, Price BD (2007) DNA damage-induced acetylation of lysine 3016 of ATM activates ATM kinase activity. Molecular and Cellular Biology l27: 8502–8509.

Tan Y, Xu Z, Tao J, Ni J, Zhao W, Lu J, Yao YF (2015) A SIRT4-like auto ADP-ribosyltransferase is essential for the environmental growth of Mycobacterium smegmatis. Acta Biochimica et Biophysica Sinica 48: 145-152.

Thao S, Chen CS, Zhu H, Escalante-Semerena JC (2010) Nε− lysine acetylation of a bacterial transcription factor inhibits its DNA-binding activity. PloS One 5: 15123.

Thao S, Escalante-Semerena JC (2011) Control of protein function by reversible N?-lysine acetylation in bacteria. Current Opinion in Microbiology 14: 200-204.

Tu S, Guo SJ, Chen CS, Liu CX, Jiang HW, Ge F, Deng JY, Zhou YM, Czajkowsky DM, Li Y (2015) YcgC represents a new protein deacetylase family in prokaryotes. Elife 4: 05322.

Vergnolle O, Xu H, Tufariello JM, Favrot L, Malek AA, Jacobs WR, Jr, Blanchard JS (2016) Post-translational acetylation of MbtA modulates mycobacterial siderophore biosynthesis. Journal of Biological Chemistry 291: 22315–22326.

Wang Q, Zhang Y, Yang C,  Xiong H, Lin Y, Yao J, Li  H, Xie L ,Zhao W,Yao Y (2010) Acetylation of metabolic enzymes coordinates carbon source utilization and metabolic flux. Science 327: 1004-1007.

Wang X, Hayes JJ (2008) Acetylation mimics within individual core histone tail domains indicate distinct roles in regulating the stability of higher-order chromatin structure. Molecular and Cellular Biology 28: 227–236.

Weinert BT, Iesmantavicius V, Wagner SA, Schölz C, Gummesson B, Beli P, Nyström T, Choudhary C (2013) Acetyl-phosphate is a critical determinant of lysine acetylation in E. coli. Molecular cell 51: 265-272.

Weinert BT, Satpathy S, Hansen BK, Lyon D, Jensen LJ, Choudhary C (2017) Accurate quantification of site-specific acetylation stoichiometry reveals the impact of sirtuin deacetylase CobB on the E. coli acetylome. Molecular and Cellular Proteomics 16: 759 –769.

Xie L, Wang X, Zeng J, Zhou M, Duan X, Li Q, Zhang Z, Luo H, Pang L, Li W (2015) Proteome-wide lysine acetylation profiling of the human pathogen Mycobacterium tuberculosis. The international Journal of Biochemistry & Cell biology 59: 193-202.

Yan J, Barak R, Liarzi O, Shainskaya A, Eisenbach M (2008) In vivo acetylation of CheY, a response regulator in chemotaxis of Escherichia coli. Journal of Molecular Biology 376: 1260-1271.

Yang X-J, Seto E (2008) The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nature reviews Molecular Cell biology 9: 206.

Yang Y, Rao R, Shen J, Tang Y, Fiskus W, Nechtman J, Atadja P, Bhalla K (2008) Role of acetylation and extracellular location of heat shock protein 90 alpha in tumor cell invasion. Cancer Research 68: 4833– 4842.

Yao R, Burr DH, Guerry P (1997) CheY?mediated modulation of Campylobacter jejuni virulence. Molecular Microbiology 23: 1021-1031.

Yu BJ, Kim JA, Moon JH, Ryu SE, Pan JG (2008) The diversity of lysine-acetylated proteins in Escherichia coli. Journal of Microbiology and Biotechnology 18: 1529-1536.

Zhang J, Sprung R, Pei J, Tan X, Kim S, Zhu H, Liu CF, Grishin NV, Zhao Y (2009) Lysine acetylation is a highly abundant and evolutionarily conserved modification in Escherichia coli. Molecular and Cellular Proteomics 8: 215-225.

Zhang Q, Zhou A, Li S, Ni J, Tao J, Lu J, Wan B, Li S, Zhang J, Zhao S (2016) Reversible lysine acetylation is involved in DNA replication initiation by regulating activities of initiator DnaA in Escherichia coli. Scientific Reports 6: 30837.

Zhang QF, Gu J, Gong P, Wang XD, Tu S, Bi LJ, Yu ZN, Zhang ZP, Cui ZQ, Wei HP, Tao SC, Zhang XE, Deng JY (2013) Reversibly acetylated lysineresidues play important roles in the
enzymatic activity of Escherichia coli N-hydroxyarylamine O-acetyltransferase. FEBS Journal 280: 1966 –1979.

Zhao K, Chai X, Marmorstein R (2004) Structure and substrate binding properties of cobB, a Sir2 homolog protein deacetylase from Escherichia coli. Journal of Molecular Biology 337: 731-741.

Zhou Y, Chen T, Zhou L, Fleming J, Deng J, Wang X, Wang L, Wang Y, Zhang X, Wei W, Bi L (2015) Discovery and characterization of Kuacetylation in Mycobacterium smegmatis. FEMS Microbiology Letters 362: 051.

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