Lysine Propionylation Is a Prevalent Post-translational Modification in Thermus thermophilus

Okanishi, Hiroki; Masui, Ryoji; Kuramitsu, Seiki

doi:10.1074/mcp.m113.035659

Cited by 39 publications

(31 citation statements)

References 48 publications

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“…Many studies show PTM, such as propionylation and acetylation, play vital roles in the regulation of enzymatic activity ( Xiong and Guan, 2012 ; Okanishi et al, 2014 ; Verdin and Ott, 2015 ). In this work, we found that the activity of both MsPrpE and MsAcsA1 were negatively modulated after propionylation, as MsPrpE was almost deactivated, whereas MsAcsA1 activity also decreased by more than 75%.…”

Section: Resultsmentioning

confidence: 99%

GlnR-Mediated Regulation of Short-Chain Fatty Acid Assimilation in Mycobacterium smegmatis

et al. 2018

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Assimilation of short-chain fatty acids (SCFAs) plays an important role in the survival and lipid biosynthesis of Mycobacteria. However, regulation of this process has not been thoroughly described. In the present work, we demonstrate that GlnR as a well-known nitrogen-sensing regulator transcriptionally modulates the AMP-forming propionyl-CoA synthetase (MsPrpE), and acetyl-CoA synthetases (MsAcs) is associated with SCFAs assimilation in Mycobacterium smegmatis, a model Mycobacterium. GlnR can directly activate the expression of MsprpE and Msacs by binding to their promoter regions based upon sensed nitrogen starvation in the host. Moreover, GlnR can activate the expression of lysine acetyltransferase encoding Mspat, which significantly decreases the activity of MsPrpE and MsAcs through increased acylation. Next, growth curves and resazurin assay show that GlnR can further regulate the growth of M. smegmatis on different SCFAs to control the viability. These results demonstrate that GlnR-mediated regulation of SCFA assimilation in response to the change of nitrogen signal serves to control the survival of M. smegmatis. These findings provide insights into the survival and nutrient utilization mechanisms of Mycobacteria in their host, which may enable new strategies in drug discovery for the control of tuberculosis.

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Section: Resultsmentioning

confidence: 99%

GlnR-Mediated Regulation of Short-Chain Fatty Acid Assimilation in Mycobacterium smegmatis

et al. 2018

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“…Recent advances in mass spectrometry have facilitated the discovery of new acyl modifications of lysine residues, including propionylation, butyrylation, succinylation, malonylation, crotonylation, and glutarylation [ 27 – 31 ]. Of these, propionylation, succinylation, and malonylation have been reported in bacteria [ 28 , 29 , 32 – 34 ]. It is thought that the corresponding acyl-CoA molecule is utilized in these acyl modifications.…”

Section: Introductionmentioning

confidence: 99%

Changes in the Acetylome and Succinylome of Bacillus subtilis in Response to Carbon Source

et al. 2015

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Lysine residues can be post-translationally modified by various acyl modifications in bacteria and eukarya. Here, we showed that two major acyl modifications, acetylation and succinylation, were changed in response to the carbon source in the Gram-positive model bacterium Bacillus subtilis. Acetylation was more common when the cells were grown on glucose, glycerol, or pyruvate, whereas succinylation was upregulated when the cells were grown on citrate, reflecting the metabolic states that preferentially produce acetyl-CoA and succinyl-CoA, respectively. To identify and quantify changes in acetylation and succinylation in response to the carbon source, we performed a stable isotope labeling by amino acids in cell culture (SILAC)-based quantitative proteomic analysis of cells grown on glucose or citrate. We identified 629 acetylated proteins with 1355 unique acetylation sites and 204 succinylated proteins with 327 unique succinylation sites. Acetylation targeted different metabolic pathways under the two growth conditions: branched-chain amino acid biosynthesis and purine metabolism in glucose and the citrate cycle in citrate. Succinylation preferentially targeted the citrate cycle in citrate. Acetylation and succinylation mostly targeted different lysine residues and showed a preference for different residues surrounding the modification sites, suggesting that the two modifications may depend on different factors such as characteristics of acyl-group donors, molecular environment of the lysine substrate, and/or the modifying enzymes. Changes in acetylation and succinylation were observed in proteins involved in central carbon metabolism and in components of the transcription and translation machineries, such as RNA polymerase and the ribosome. Mutations that modulate protein acylation affected B. subtilis growth. A mutation in acetate kinase (ackA) increased the global acetylation level, suggesting that acetyl phosphate-dependent acetylation is common in B. subtilis, just as it is in Escherichia coli. Our results suggest that acyl modifications play a role in the physiological adaptations to changes in carbon nutrient availability of B. subtilis.

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“…These results featured the potential for physiological conditions of the host to impact plasmid determined functions. Several lines of evidence suggested that the extent of protein acylation varies in different bacterial species (Okanishi et al, 2014;2017a). Furthermore, changes in the acylation profile could be elicited by stress conditions (Zhang et al, 2009) and various carbon sources (Weinert et al 2013a;Colak et al, 2013;Kosono et al, 2015;Mizuno et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

“…Recent studies have also proposed a second non-enzymatic mechanism for acetylation in bacteria with acetyl-phosphate serving as an acetyl donor (Weinert et al, 2013a;Kuhn et al, 2014). Various novel acyl modifications, including succinylation (Colak et al, 2013;Weinert et al, 2013b;Kosono et al, 2015;Pan et al, 2015;Yang et al, 2015;Mizuno et al, 2016;Okanishi et al, 2017a), propionylation (Okanishi et al, 2014;2017b;Sun et al, 2016), malonylation (Qian et al, 2016) and glutarylation (Xie et al, 2016) have been reported in bacteria and the corresponding acyl-CoA molecules are considered as acyl donors. Among those, protein lysine acetylation and succinylation have been demonstrated to occur frequently (Weinert et al, 2013b;Kosono et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Proteome and acylome analyses of the functional interaction network between the carbazole‐degradative plasmid pCAR1 and host Pseudomonas putida KT2440

Vasileva

Suzuki-Minakuchi

Kosono

et al. 2018

Environ Microbiol Rep

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Understanding the interplay between a plasmid and its host system is a bottleneck towards prediction of the fate of plasmid-harbouring strains in the natural environments. Here, we studied the impact of the conjugative plasmid pCAR1, involved in carbazole degradation, on the proteome of Pseudomonas putida KT2440 using SILAC method. Furthermore, we investigated two acyl lysine modifications (acetylation and succinylation) that respond to the metabolic status of the cell and are implicated in regulation of various cellular processes. The total proteome analysis revealed that the abundance of key proteins involved in metabolism, signal transduction and motility was affected by pCAR1 carriage. In total, we identified 1359 unique acetylation sites on 637 proteins and 567 unique succinylation sites on 259 proteins. Changes in the acylation status of proteins involved in metabolism and translation by pCAR1 carriage were detected. Remarkably, acylation was identified on proteins involved in important plasmid functions, including partitioning and carbazole degradation, and on nucleoid-associated proteins that play a key role in the functional interaction with the chromosome. This study provides a novel insight on the functional consequences of plasmid carriage and improves our understanding of the plasmid-host cross-talk.

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Lysine Propionylation Is a Prevalent Post-translational Modification in Thermus thermophilus

Cited by 39 publications

References 48 publications

GlnR-Mediated Regulation of Short-Chain Fatty Acid Assimilation in Mycobacterium smegmatis

GlnR-Mediated Regulation of Short-Chain Fatty Acid Assimilation in Mycobacterium smegmatis

Changes in the Acetylome and Succinylome of Bacillus subtilis in Response to Carbon Source

Proteome and acylome analyses of the functional interaction network between the carbazole‐degradative plasmid pCAR1 and host Pseudomonas putida KT2440

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