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Glucose-Mediated Protein Arginine Phosphorylation/Dephosphorylation Regulates ylxR Encoding Nucleoid-Associated Protein and Cell Growth in Bacillus subtilis.

ABSTRACT: Glucose is the most favorable carbon source for many bacteria, and these bacteria have several glucose-responsive networks. We proposed new glucose responsive system, which includes protein acetylation and probable translation control through TsaEBD, which is a tRNA modification enzyme required for the synthesis of threonylcarbamoyl adenosine (t6A)-tRNA. The system also includes nucleoid-associated protein YlxR, regulating more than 400 genes including many metabolic genes and the ylxR-containing operon driven by the PylxS promoter is induced by glucose. Thus, transposon mutagenesis was performed for searching regulatory factors for PylxS expression. As a result, ywlE was identified. The McsB kinase phosphorylates arginine (Arg) residues of proteins and the YwlE phosphatase counteracts against McsB through Arg-dephosphorylation. Phosphorylated Arg has been known to function as a tag for ClpCP-dependent protein degradation. The previous analysis identified TsaD as an Arg-phosphorylated protein. Our results showed that the McsB/YwlE system regulates PylxS expression through ClpCP-mediated protein degradation of TsaD. In addition, we observed that glucose induced ywlE expression and repressed mcsB expression. It was concluded that these phenomena would cause glucose induction (GI) of PylxS, based on the Western blot analyses of TsaD-FLAG. These observations and the previous those that many glycolytic enzymes are Arg-phosphorylated suggested that the McsB/YwlE system might be involved in cell growth in glucose-containing medium. We observed that the disruption of mcsB and ywlE resulted in an increase of cell mass and delayed growth, respectively, in semi-synthetic medium. These results provide us broader insights to the physiological roles of the McsB/YwlE system and protein Arg-phosphorylation.

SUBMITTER: Ogura M

PROVIDER: S-EPMC7546277 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Glucose-Mediated Protein Arginine Phosphorylation/Dephosphorylation Regulates ylxR Encoding Nucleoid-Associated Protein and Cell Growth in Bacillus subtilis.

Ogura Mitsuo M

Frontiers in microbiology 20200925

Glucose is the most favorable carbon source for many bacteria, and these bacteria have several glucose-responsive networks. We proposed new glucose responsive system, which includes protein acetylation and probable translation control through TsaEBD, which is a tRNA modification enzyme required for the synthesis of threonylcarbamoyl adenosine (t6A)-tRNA. The system also includes nucleoid-associated protein YlxR, regulating more than 400 genes including many metabolic genes and the ...[more]

PMID: 33101263

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Project description:Bacteria must survive harsh environmental fluctuations at times and have evolved several strategies. "Collective" behaviors have been identified due to recent progress in single-cell analysis. Since most bacteria exist as single cells, bacterial populations are often considered clonal. However, accumulated evidence suggests this is not the case. Gene expression and protein expression are often not homogeneous, resulting in phenotypic heterogeneity. In extreme cases, this leads to bistability, the existence of two stable states. In many cases, expression of key master regulators is bimodal via positive feedback loops causing bimodal expression of the target genes. We observed bimodal expression of metabolic genes for alternative carbon sources. Expression profiles of the frlBONMD-yurJ operon driven by the frlB promoter (PfrlB), which encodes degradation enzymes and a transporter for amino sugars including fructoselysine, were investigated using transcriptional lacZ and gfp, and translational fluorescence reporter mCherry fusions. Disruption effects of genes encoding CodY, FrlR, RNaseY, and nucleoid-associated protein YlxR, four known regulatory factors for PfrlB, were examined for expression of each fusion construct. Expression of PfrlB-gfp and PfrlB-mCherry, which were located at amyE and its original locus, respectively, was bimodal; and disruption of ylxR resulted in the disappearance of the clear bimodal expression pattern in flow cytometric analyses. This suggested a role for YlxR on the bimodal expression of PfrlB. The data indicated that YlxR acted on the bimodal expression of PfrlB through both transcription and translation. YlxR regulates many genes, including those related to translation, supporting the above notion. Depletion of RNaseY abolished heterogenous expression of transcriptional PfrlB-gfp but not bimodal expression of translational PfrlB-mCherry, suggesting the role of RNaseY in regulation of the operon through mRNA stability control and regulatory mechanism for PfrlB-mCherry at the translational level. Based on these results, we discuss the meaning and possible cause of bimodal PfrlB expression.

Dataset Information

Glucose-Mediated Protein Arginine Phosphorylation/Dephosphorylation Regulates ylxR Encoding Nucleoid-Associated Protein and Cell Growth in Bacillus subtilis.

Publications

Glucose-Mediated Protein Arginine Phosphorylation/Dephosphorylation Regulates <i>ylxR</i> Encoding Nucleoid-Associated Protein and Cell Growth in <i>Bacillus subtilis</i>.

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