The HPr protein of the phosphotransferase system links induction and catabolite repression of the Bacillus subtilis levanase operon

Stülke, Jörg; Martin‐Verstraete, Isabelle; Charrier, Véronique; Klier, André; Deutscher, Josef; Rapoport, Georges

doi:10.1128/jb.177.23.6928-6936.1995

Cited by 64 publications

(91 citation statements)

References 53 publications

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“…Although protein phosphorylation is implicated in both cases, the mechanisms of CCR and inducer control are quite different. In Gram-positive bacteria, PEP-dependent phosphorylation of HPr at His-15 is not only necessary for PTS-catalyzed sugar transport and phosphorylation, but is also implicated in phosphorylation and regulation of transcriptional effectors (36,37) and catabolic enzymes (29). By contrast, ATP-dependent phosphorylation of HPr at Ser-46 is involved in CCR (10) and inducer exclusion (35).…”

Section: Discussionmentioning

confidence: 99%

The Bacillus subtilis crh gene encodes a HPr-like protein involved in carbon catabolite repression

Galinier

Haiech

Kilhoffer

et al. 1997

Proc. Natl. Acad. Sci. U.S.A.

209

274

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Carbon catabolite repression (CCR) of several Bacillus subtilis catabolic genes is mediated by ATPdependent phosphorylation of histidine-containing protein (HPr), a phosphocarrier protein of the phosphoenolpyruvate (PEP): sugar phosphotransferase system. In this study, we report the discovery of a new B. subtilis gene encoding a HPr-like protein, Crh (for catabolite repression HPr), composed of 85 amino acids. Crh exhibits 45% sequence identity with HPr, but the active site His-15 of HPr is replaced with a glutamine in Crh. Crh is therefore not phosphorylated by PEP and enzyme I, but is phosphorylated by ATP and the HPr kinase in the presence of fructose-1,6-bisphosphate. We determined Ser-46 as the site of phosphorylation in Crh by carrying out mass spectrometry with peptides obtained by tryptic digestion or CNBr cleavage. In a B. subtilis ptsH1 mutant strain, synthesis of ␤-xylosidase, inositol dehydrogenase, and levanase was only partially relieved from CCR. Additional disruption of the crh gene caused almost complete relief from CCR. In a ptsH1 crh1 mutant, producing HPr and Crh in which Ser-46 is replaced with a nonphosphorylatable alanyl residue, expression of ␤-xylosidase was also completely relieved from glucose repression. These results suggest that CCR of certain catabolic operons requires, in addition to CcpA, ATP-dependent phosphorylation of Crh, and HPr at Ser-46.The bacterial phosphoenolpyruvate (PEP): sugar phosphotransferase system (PTS) catalyzes the transport and concomitant phosphorylation of carbohydrates via a protein phosphorylation chain including PEP-dependent phosphorylation of His-15 in histidine-containing protein (HPr) by enzyme I (EI). P-His-HPr phosphorylates the sugar-specific EIIAs. In Gram-positive bacteria, the PTS regulates also induction and carbon catabolite repression (CCR) of numerous catabolic genes (1). The central regulatory protein involved in these various functions is HPr. In Gram-positive bacteria, this small phosphoryl transfer protein can be phosphorylated at a regulatory serine (Ser-46) by ATP and the HPr kinase (2, 3), in addition to phosphorylation at the catalytic His-15 by PEP and EI (4, 5). PEP-dependent and ATP-dependent phosphorylation of HPr interfere with each other-i.e., P-His-HPr is a poor substrate for the HPr kinase and P-Ser-HPr is a poor substrate for EI (6, 7). ATP-dependent phosphorylation of HPr is stimulated by glycolytic intermediates such as fructose-1,6-bisphosphate (FBP) in Enterococcus faecalis (6) and in Streptococcus pyogenes (7). It has been reported that FBP is also implicated in CCR of the Bacillus subtilis gnt and iol operons (8, 9), and a potential role of phosphorylation of HPr at Ser-46 in CCR has therefore been investigated (10). The gnt operon contains the genes gntRKPZ encoding the repressor GntR, gluconate kinase, gluconate permease, and a gluconate-6-Pdehydrogenase (11), whereas the iol operon is composed of 10 genes encoding enzymes presumably implicated in inositol metabolism, including iolG encoding inositol dehydro...

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Section: Discussionmentioning

confidence: 99%

The Bacillus subtilis crh gene encodes a HPr-like protein involved in carbon catabolite repression

Galinier

Haiech

Kilhoffer

et al. 1997

Proc. Natl. Acad. Sci. U.S.A.

209

274

View full text Add to dashboard Cite

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“…This latter type of control has so far only been identified in B. subtilis and is implicated in catabolite repression (Arnaud et al, 1996;Krü ger et al, 1996;Martin-Verstraete et al, 1995;Stü lke et al, 1995).…”

Section: Discussionmentioning

confidence: 99%

“…We have recently shown that, in addition to repression via CcpA/CRE, an alternative mechanism is involved in catabolite repression of the levanase operon (Martin-Verstraete et al, Stü lke et al, 1995). Mutants exhibiting glucose-resistant expression of the levanase operon (grl ) were isolated and mapped by transduction.…”

Section: Characterization Of Ptsg Mutant Allelesmentioning

confidence: 99%

“…The levanase operon, which encodes a fructosespecific PTS (lev-PTS) and an extracellular enzyme, levanase, is positively regulated by a NifA-like activator protein, LevR. The LevR protein which also shares domains of homology with antiterminator proteins is negatively regulated by components of the lev-PTS in the absence of fructose, in addition to positive regulation by HPr-dependent phosphorylation (Dé barbouillé et al, 1991a;MartinVerstraete et al, 1990;Stü lke et al, 1995).…”

Section: Introductionmentioning

confidence: 99%

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Induction of the Bacillus subtilis ptsGHI operon by glucose is controlled by a novel antiterminator, GlcT

Stülke

Martin‐Verstraete

Zagorec³

et al. 1997

Molecular Microbiology

165

187

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SummaryGlucose is the preferred carbon and energy source of Bacillus subtilis. It is transported into the cell by the glucose-specific phosphoenolpyruvate:sugar phosphotransferase system (PTS) encoded by the ptsGHI locus. We show here that these three genes (ptsG, ptsH, and ptsI ) form an operon, the expression of which is inducible by glucose. In addition, ptsH and ptsI form a constitutive ptsHI operon. The promoter of the ptsGHI operon was mapped and expression from this promoter was found to be constitutive. Deletion mapping of the promoter region revealed the presence of a transcriptional terminator as a regulatory element between the promoter and coding region of the ptsG gene. Mutations within the ptsG gene were characterized and their consequences on the expression of ptsG studied. The results suggest that expression of the ptsGHI operon is subject to negative autoregulation by the glucose permease, which is the ptsG gene product. A regulatory gene located upstream of the ptsGHI operon, termed glcT, was also identified. The GlcT protein is a novel member of the BglG family of transcriptional antiterminators and is essential for the expression of the ptsGHI operon. A deletion of the terminator alleviates the need for GlcT. The activity of GlcT is negatively regulated by the glucose permease.

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“…59) In addition, deletion of pstHI in a levD or levE background diminished expression from the lev promoter. 148) From these results it was concluded that similarly to PRDcontaining antiterminators, LevR also possesses positive and negative sites of regulation, which are expected to be the targets of phosphorylation by P-His-HPr and P-EIIB lev respectively. If glucose or other preferred PTS-sugars are present additionally, the phosphoryl group of P-His-HPr is preferentially used in sugar phosphorylation.…”

Section: Catabolite Control Mediated By Ccpb Ccpc Ccpn and Cggrmentioning

confidence: 96%

Carbon Catabolite Control of the Metabolic Network inBacillus subtilis

Fujita

2009

Bioscience, Biotechnology, and Biochemistry

257

284

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The HPr protein of the phosphotransferase system links induction and catabolite repression of the Bacillus subtilis levanase operon

Cited by 64 publications

References 53 publications

The Bacillus subtilis crh gene encodes a HPr-like protein involved in carbon catabolite repression

The Bacillus subtilis crh gene encodes a HPr-like protein involved in carbon catabolite repression

Induction of the Bacillus subtilis ptsGHI operon by glucose is controlled by a novel antiterminator, GlcT

Carbon Catabolite Control of the Metabolic Network inBacillus subtilis

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