Molecular analysis of the glucose-specific phosphoenolpyruvate : sugar phosphotransferase system from Lactobacillus casei and its links with the control of sugar metabolism

Yebra, Marı́a J.; Monedero, Vicente; Zúñiga, Manuel; Deutscher, Josef; Pérez-Martı́nez, Gaspar

doi:10.1099/mic.0.28293-0

Cited by 30 publications

(31 citation statements)

References 40 publications

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“…The specificity of the Mpt PTS has not been determined, but it is likely to be the mannose/glucose-specific PTS, as its expression in L. monocytogenes is induced by these two sugars (151). In addition, the EIID domain of the Mpt PTS possesses a C-terminal extension characteristic of mannose/glucose-specific PTS, and the various sugar-specific EII Mpt components exhibit the strongest similarity to those of the recently characterized mannose/glucose PTS of L. casei (975). Homologs of the Mpt PTS are present in E. faecalis and Listeria innocua, and the absence of expression of the mpt operon in these organisms also leads to resistance towards class IIa bacteriocins such as mesentericin Y105 for E. faecalis (320) and pediocin AcH for L. innocua (959).…”

Section: Discussionmentioning

confidence: 99%

How Phosphotransferase System-Related Protein Phosphorylation Regulates Carbohydrate Metabolism in Bacteria

Deutscher

Francke

Postma

2006

Microbiol Mol Biol Rev

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1,188

769

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SUMMARY The phosphoenolpyruvate(PEP):carbohydrate phosphotransferase system (PTS) is found only in bacteria, where it catalyzes the transport and phosphorylation of numerous monosaccharides, disaccharides, amino sugars, polyols, and other sugar derivatives. To carry out its catalytic function in sugar transport and phosphorylation, the PTS uses PEP as an energy source and phosphoryl donor. The phosphoryl group of PEP is usually transferred via four distinct proteins (domains) to the transported sugar bound to the respective membrane component(s) (EIIC and EIID) of the PTS. The organization of the PTS as a four-step phosphoryl transfer system, in which all P derivatives exhibit similar energy (phosphorylation occurs at histidyl or cysteyl residues), is surprising, as a single protein (or domain) coupling energy transfer and sugar phosphorylation would be sufficient for PTS function. A possible explanation for the complexity of the PTS was provided by the discovery that the PTS also carries out numerous regulatory functions. Depending on their phosphorylation state, the four proteins (domains) forming the PTS phosphorylation cascade (EI, HPr, EIIA, and EIIB) can phosphorylate or interact with numerous non-PTS proteins and thereby regulate their activity. In addition, in certain bacteria, one of the PTS components (HPr) is phosphorylated by ATP at a seryl residue, which increases the complexity of PTS-mediated regulation. In this review, we try to summarize the known protein phosphorylation-related regulatory functions of the PTS. As we shall see, the PTS regulation network not only controls carbohydrate uptake and metabolism but also interferes with the utilization of nitrogen and phosphorus and the virulence of certain pathogens.

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Section: Discussionmentioning

confidence: 99%

How Phosphotransferase System-Related Protein Phosphorylation Regulates Carbohydrate Metabolism in Bacteria

Deutscher

Francke

Postma

2006

Microbiol Mol Biol Rev

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1,188

769

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“…casei is a facultative heterofermentative lactic acid bacterium frequently used as a cheese starter culture and which is also employed as a probiotic. Extensive research has been carried out on the study of sugar catabolism (28,(39)(40)(41); however, the knowledge of the utilization of organic acids has received less attention. As previously indicated, physiological and biochemical studies identified two L-malate dissimilation pathways in L. casei.…”

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confidence: 99%

Requirement of theLactobacillus caseiMaeKR Two-Component System forl-Malic Acid Utilization via a Malic Enzyme Pathway

Landete

García-Haro

Blasco

et al. 2010

Appl Environ Microbiol

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Lactobacillus casei can metabolize L-malic acid via malolactic enzyme (malolactic fermentation [MLF]) or malic enzyme (ME). Whereas utilization of L-malic acid via MLF does not support growth, the ME pathway enables L. casei to grow on L-malic acid. In this work, we have identified in the genomes of L. casei strains BL23 and ATCC 334 a cluster consisting of two diverging operons, maePE and maeKR, encoding a putative malate transporter (maeP), an ME (maeE), and a two-component (TC) system belonging to the citrate family (maeK and maeR). Homologous clusters were identified in Enterococcus faecalis, Streptococcus agalactiae, Streptococcus pyogenes, and Streptococcus uberis. Our results show that ME is essential for L-malic acid utilization in L. casei. Furthermore, deletion of either the gene encoding the histidine kinase or the response regulator of the TC system resulted in the loss of the ability to grow on L-malic acid, thus indicating that the cognate TC system regulates and is essential for the expression of ME. Transcriptional analyses showed that expression of maeE is induced in the presence of L-malic acid and repressed by glucose, whereas TC system expression was induced by L-malic acid and was not repressed by glucose. DNase I footprinting analysis showed that MaeR binds specifically to a set of direct repeats [5-TTATT(A/T)AA-3] in the mae promoter region. The location of the repeats strongly suggests that MaeR activates the expression of the diverging operons maePE and maeKR where the first one is also subjected to carbon catabolite repression.The metabolism of L-malic acid by lactic acid bacteria (LAB) has brought about considerable interest because of its relevance in winemaking (24). The degradation of L-malate to L-lactate leads to a reduction of the acidity of wine, and it provides microbiological stability by preventing the secondary growth of LAB after bottling. Most LAB decarboxylate Lmalate to L-lactate by an NAD ϩ -and Mn 2ϩ -dependent malolactic enzyme (MLE) (Fig. 1); nevertheless, a few LAB species can also degrade L-malate to pyruvate by a malic enzyme (ME) (Fig. 1). This pathway was first detected in Enterococcus faecalis (20) and later in Lactobacillus casei (23,33) and Streptococcus bovis (14). In contrast to the utilization of L-malate through MLE, the utilization of the ME pathway enables these organisms to grow with L-malate as a carbon source (22). However, whereas MLE has been the focus of an extensive research effort, the physiological role and the regulation of ME remain largely unknown.L. casei is a facultative heterofermentative lactic acid bacterium frequently used as a cheese starter culture and which is also employed as a probiotic. Extensive research has been carried out on the study of sugar catabolism (28, 39-41); however, the knowledge of the utilization of organic acids has received less attention. As previously indicated, physiological and biochemical studies identified two L-malate dissimilation pathways in L. casei. Furthermore, these studies showed that ME expression...

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“…These results, together with the lack of transcription during growth on rapidly metabolized substrates (glucose and sucrose), suggest that regulation of the sim operon is mediated via carbon catabolite repression. This mode of regulation of catabolic operons, particularly those involved in the dissimilation of sugars, is found in many species of gram-positive bacteria, including strains of L. casei (7,18,41,45). It is likely that the CRE region is the target for a multicomponent complex (phosphorylated disaccharide, catabolite control protein A [CcpA], and phospho-seryl-HPr) that modulates expression of the sim operon in L. casei ATCC 334.…”

Section: Discussionmentioning

confidence: 99%

“…Collectively, these interactive proteins constitute a fivestage phosphorelay that, via transfer of the high-energy phosphoryl moiety from PEP, catalyzes the simultaneous phosphorylation and translocation of sugars through the cytoplasmic membrane. Biochemical and physiological studies performed during the past 25 years have established the presence of a variety of sugar PEP-dependent PTSs in L. casei, including PTSs for glucose (41,45), galactose (2,6), lactose (4,5,8,9), sorbose (46), and pentitols (15,16). Significantly, in the past decade, the development and application of techniques for manipulation of LAB genomes have provided extensive (and in some instances unexpected) insight into the molecular basis for regulation of PEP-dependent PTSs in L. casei (18,42,45).…”

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confidence: 99%

“…Biochemical and physiological studies performed during the past 25 years have established the presence of a variety of sugar PEP-dependent PTSs in L. casei, including PTSs for glucose (41, 45), galactose (2, 6), lactose (4,5,8,9), sorbose (46), and pentitols (15, 16). Significantly, in the past decade, the development and application of techniques for manipulation of LAB genomes have provided extensive (and in some instances unexpected) insight into the molecular basis for regulation of PEP-dependent PTSs in L. casei (18,42,45).Many bacterial species, including L. casei, have the capacity to transport sucrose via an inducible sucrose-specific PEPdependent PTS (GenBank accession no. YP_807293).…”

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confidence: 99%

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ThesimOperon Facilitates the Transport and Metabolism of Sucrose Isomers inLactobacillus caseiATCC 334

Thompson¹,

Jakubovics²,

Abraham

et al. 2008

J Bacteriol

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Inspection of the genome sequence of Lactobacillus casei ATCC 334 revealed two operons that might dissimilate the five isomers of sucrose. To test this hypothesis, cells of L. casei ATCC 334 were grown in a defined medium supplemented with various sugars, including each of the five isomeric disaccharides. Extracts prepared from cells grown on the sucrose isomers contained high levels of two polypeptides with M r s of ϳ50,000 and ϳ17,500. Neither protein was present in cells grown on glucose, maltose or sucrose. Proteomic, enzymatic, and Western blot analyses identified the ϳ50-kDa protein as an NAD ؉ -and metal ion-dependent phospho-␣-glucosidase. The oligomeric enzyme was purified, and a catalytic mechanism is proposed. The smaller polypeptide represented an EIIA component of the phosphoenolpyruvate-dependent sugar phosphotransferase system. Phospho-␣-glucosidase and EIIA are encoded by genes at the LSEI_0369 (simA) and LSEI_0374 (simF) loci, respectively, in a block of seven genes comprising the sucrose isomer metabolism (sim) operon. Northern blot analyses provided evidence that three mRNA transcripts were up-regulated during logarithmic growth of L. casei ATCC 334 on sucrose isomers. Internal simA and simF gene probes hybridized to ϳ1.5-and ϳ1.3-kb transcripts, respectively. A 6.8-kb mRNA transcript was detected by both probes, which was indicative of cotranscription of the entire sim operon.Comparative genomics and phylogenetic analyses of the lactic acid bacteria (LAB) have provided evidence that the order Lactobacillales comprises the families Lactobacillaceae, Streptococcaceae, Enterococcaceae, and Leuconostocaceae (17, 25; http://www.ncbi.nlm.nih.gov/Taxonomy/). These generally fastidious gram-positive organisms are used extensively for the fermentation of dairy, meat, and vegetable products. The industrial importance of LAB, and Lactobacillus casei strains in particular, results from the capacity of these microorganisms to metabolize carbohydrates rapidly (and primarily) to lactic acid. Prior to their homolactic fermentation via the glycolytic pathway, many carbohydrates are accumulated simultaneously with phosphorylation via sugar-specific phosphoenolpyruvate (PEP)-dependent phosphotransferase systems (PTSs) (7,24,29). The multicomponent PEP-dependent PTSs comprise membrane-localized, sugar-specific transporters (IICB enzymes) that may be fused or associated with a third protein (EIIA), as well as two general cytoplasmic proteins (EI and HPr). Collectively, these interactive proteins constitute a fivestage phosphorelay that, via transfer of the high-energy phosphoryl moiety from PEP, catalyzes the simultaneous phosphorylation and translocation of sugars through the cytoplasmic membrane. Biochemical and physiological studies performed during the past 25 years have established the presence of a variety of sugar PEP-dependent PTSs in L. casei, including PTSs for glucose (41, 45), galactose (2, 6), lactose (4,5,8,9), sorbose (46), and pentitols (15, 16). Significantly, in the past decade, the development ...

show abstract

Molecular analysis of the glucose-specific phosphoenolpyruvate : sugar phosphotransferase system from Lactobacillus casei and its links with the control of sugar metabolism

Cited by 30 publications

References 40 publications

How Phosphotransferase System-Related Protein Phosphorylation Regulates Carbohydrate Metabolism in Bacteria

How Phosphotransferase System-Related Protein Phosphorylation Regulates Carbohydrate Metabolism in Bacteria

Requirement of theLactobacillus caseiMaeKR Two-Component System forl-Malic Acid Utilization via a Malic Enzyme Pathway

ThesimOperon Facilitates the Transport and Metabolism of Sucrose Isomers inLactobacillus caseiATCC 334

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