Previous Article | Next Article 
Journal of Bacteriology, November 2000, p. 5982-5989, Vol. 182, No. 21
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Control of Lactose Transport,
-Galactosidase Activity, and
Glycolysis by CcpA in Streptococcus thermophilus: Evidence
for Carbon Catabolite Repression by a Non-Phosphoenolpyruvate-Dependent
Phosphotransferase System Sugar
Patrick T. C.
van den
Bogaard,*
Michiel
Kleerebezem,
Oscar P.
Kuipers,
and
Willem M.
de Vos
Wageningen Centre for Food Sciences, NIZO
Food Research, Department of Flavour and Natural Ingredients, 6710 BA Ede, The Netherlands
Received 12 April 2000/Accepted 1 August 2000
Streptococcus thermophilus, unlike many other
gram-positive bacteria, prefers lactose over glucose as the primary
carbon and energy source. Moreover, lactose is not taken up by a
phosphoenolpyruvate-dependent phosphotransferase system (PTS) but by
the dedicated transporter LacS. In this paper we show that CcpA plays a
crucial role in the fine-tuning of lactose transport,
-galactosidase
(LacZ) activity, and glycolysis to yield optimal glycolytic flux and
growth rate. A catabolite-responsive element (cre) was
identified in the promoter of the lacSZ operon, indicating
a possible role for regulation by CcpA. Transcriptional analysis showed
a sevenfold relief of repression in the absence of a functional CcpA
when cells were grown on lactose. This CcpA-mediated repression of
lacSZ transcription did not occur in wild-type cells during
growth on galactose, taken up by the same LacS transport system.
Lactose transport during fermentation was increased significantly in
strains carrying a disrupted ccpA gene. Moreover, a
ccpA disruption strain was found to release substantial
amounts of glucose into the medium when grown on lactose.
Transcriptional analysis of the ldh gene showed that
expression was induced twofold during growth on lactose compared to
glucose or galactose, in a CcpA-dependent manner. A reduced rate of
glycolysis concomitant with an increased lactose transport rate could
explain the observed expulsion of glucose in a ccpA disruption mutant. We propose that CcpA in S. thermophilus
acts as a catabolic regulator during growth on the preferred non-PTS sugar lactose. In contrast to other bacteria, S. thermophilus possesses an overcapacity for lactose uptake that is
repressed by CcpA to match the rate-limiting glycolytic flux.
*
Corresponding author. Mailing address: Department of
Flavour and Natural Ingredients, NIZO food research, Wageningen Centre for Food Sciences, P.O. Box 20, 6710 BA Ede, The Netherlands. Phone:
(31) 318 659511. Fax: (31) 318 650400. E-mail:
bogaard{at}nizo.nl.

Present address: Molecular Genetics, Groningen Biomolecular
Sciences and Biotechnology Institute, University of Groningen,
9750 AA
Haren, The
Netherlands.
Journal of Bacteriology, November 2000, p. 5982-5989, Vol. 182, No. 21
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Arioli, S., Roncada, P., Salzano, A. M., Deriu, F., Corona, S., Guglielmetti, S., Bonizzi, L., Scaloni, A., Mora, D.
(2009). The relevance of carbon dioxide metabolism in Streptococcus thermophilus. Microbiology
155: 1953-1965
[Abstract]
[Full Text]
-
Zomer, A. L., Buist, G., Larsen, R., Kok, J., Kuipers, O. P.
(2007). Time-Resolved Determination of the CcpA Regulon of Lactococcus lactis subsp. cremoris MG1363. J. Bacteriol.
189: 1366-1381
[Abstract]
[Full Text]
-
Deutscher, J., Francke, C., Postma, P. W.
(2006). How Phosphotransferase System-Related Protein Phosphorylation Regulates Carbohydrate Metabolism in Bacteria. Microbiol. Mol. Biol. Rev.
70: 939-1031
[Abstract]
[Full Text]
-
Barrangou, R., Azcarate-Peril, M. A., Duong, T., Conners, S. B., Kelly, R. M., Klaenhammer, T. R.
(2006). Global analysis of carbohydrate utilization by Lactobacillus acidophilus using cDNA microarrays. Proc. Natl. Acad. Sci. USA
103: 3816-3821
[Abstract]
[Full Text]
-
Parche, S., Beleut, M., Rezzonico, E., Jacobs, D., Arigoni, F., Titgemeyer, F., Jankovic, I.
(2006). Lactose-over-Glucose Preference in Bifidobacterium longum NCC2705: glcP, Encoding a Glucose Transporter, Is Subject to Lactose Repression. J. Bacteriol.
188: 1260-1265
[Abstract]
[Full Text]
-
Iyer, R., Baliga, N. S., Camilli, A.
(2005). Catabolite Control Protein A (CcpA) Contributes to Virulence and Regulation of Sugar Metabolism in Streptococcus pneumoniae. J. Bacteriol.
187: 8340-8349
[Abstract]
[Full Text]
-
Derzelle, S., Bolotin, A., Mistou, M.-Y., Rul, F.
(2005). Proteome Analysis of Streptococcus thermophilus Grown in Milk Reveals Pyruvate Formate-Lyase as the Major Upregulated Protein. Appl. Environ. Microbiol.
71: 8597-8605
[Abstract]
[Full Text]
-
Labrie, S., Bart, C., Vadeboncoeur, C., Moineau, S.
(2005). Use of an {alpha}-Galactosidase Gene as a Food-Grade Selection Marker for Streptococcus thermophilus. J DAIRY SCI
88: 2341-2347
[Abstract]
[Full Text]
-
Cochu, A., Roy, D., Vaillancourt, K., LeMay, J.-D., Casabon, I., Frenette, M., Moineau, S., Vadeboncoeur, C.
(2005). The Doubly Phosphorylated Form of HPr, HPr(Ser-P)(His~P), Is Abundant in Exponentially Growing Cells of Streptococcus thermophilus and Phosphorylates the Lactose Transporter LacS as Efficiently as HPr(His~P). Appl. Environ. Microbiol.
71: 1364-1372
[Abstract]
[Full Text]
-
Caescu, C. I., Vidal, O., Krzewinski, F., Artenie, V., Bouquelet, S.
(2004). Bifidobacterium longum Requires a Fructokinase (Frk; ATP:D-Fructose 6-Phosphotransferase, EC 2.7.1.4) for Fructose Catabolism. J. Bacteriol.
186: 6515-6525
[Abstract]
[Full Text]
-
Asanuma, N., Yoshii, T., Hino, T.
(2004). Molecular Characterization of CcpA and Involvement of This Protein in Transcriptional Regulation of Lactate Dehydrogenase and Pyruvate Formate-Lyase in the Ruminal Bacterium Streptococcus bovis. Appl. Environ. Microbiol.
70: 5244-5251
[Abstract]
[Full Text]
-
Vaillancourt, K., LeMay, J.-D., Lamoureux, M., Frenette, M., Moineau, S., Vadeboncoeur, C.
(2004). Characterization of a Galactokinase-Positive Recombinant Strain of Streptococcus thermophilus. Appl. Environ. Microbiol.
70: 4596-4603
[Abstract]
[Full Text]
-
Giammarinaro, P., Paton, J. C.
(2002). Role of RegM, a Homologue of the Catabolite Repressor Protein CcpA, in the Virulence of Streptococcus pneumoniae. Infect. Immun.
70: 5454-5461
[Abstract]
[Full Text]
-
Vaillancourt, K., Moineau, S., Frenette, M., Lessard, C., Vadeboncoeur, C.
(2002). Galactose and Lactose Genes from the Galactose-Positive Bacterium Streptococcus salivarius and the Phylogenetically Related Galactose-Negative Bacterium Streptococcus thermophilus: Organization, Sequence, Transcription, and Activity of the gal Gene Products. J. Bacteriol.
184: 785-793
[Abstract]
[Full Text]
-
Degeest, B., Vaningelgem, F., Laws, A. P., De Vuyst, L.
(2001). UDP-N-Acetylglucosamine 4-Epimerase Activity Indicates the Presence of N-Acetylgalactosamine in Exopolysaccharides of Streptococcus thermophilus Strains. Appl. Environ. Microbiol.
67: 3976-3984
[Abstract]
[Full Text]
-
Muscariello, L., Marasco, R., De Felice, M., Sacco, M.
(2001). The Functional ccpA Gene Is Required for Carbon Catabolite Repression in Lactobacillus plantarum. Appl. Environ. Microbiol.
67: 2903-2907
[Abstract]
[Full Text]
-
Vaughan, E. E., van den Bogaard, P. T. C., Catzeddu, P., Kuipers, O. P., de Vos, W. M.
(2001). Activation of Silent gal Genes in the lac-gal Regulon of Streptococcus thermophilus. J. Bacteriol.
183: 1184-1194
[Abstract]
[Full Text]