The Global Regulator CodY in Streptococcus Thermophilus Controls the Metabolic Network for Escalating Growth in the Milk Environment

Overview

Journal Appl Environ Microbiol

Specialties Environmental Health
Microbiology

Date 2015 Jan 25

PMID 25616791

Citations 9

Authors

W W Lu

Y Wang

T Wang

J Kong

Affiliations

Soon will be listed here.

Abstract

CodY is a transcriptional regulator conserved in the low-GC group of Gram-positive bacteria. In this work, we demonstrated the presence in Streptococcus thermophilus ST2017 of a functional member of the CodY family of global regulatory proteins, S. thermophilus CodY (CodYSt). The CodYSt regulon was identified by transcriptome analysis; it consisted predominantly of genes involved in amino acid metabolism but also included genes involved in several other cellular processes, including carbon metabolism, nutrient transport, and stress response. It was revealed that CodYSt repressed the transformation of the central metabolic pathway to amino acid metabolism and improved lactose utilization. Furthermore, the glutamate dehydrogenase gene (gdhA), repressed by CodYSt, was suggested to coordinate the interconversion between carbon metabolism and amino acid metabolism and to play an important role on the optimal growth of S. thermophilus ST2017 in milk. A conserved CodYSt box [AA(T/A)(A/T)TTCTGA(A/C)AATT] was indeed required for in vitro binding of CodYSt to the target regions of DNA. These results provided evidence for the function of CodYSt, by which this strain coordinately regulates its various metabolic pathways so as to adapt to the milk environment.

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References

van den Bogaard P, Kleerebezem M, Kuipers O, de Vos W . Control of lactose transport, beta-galactosidase activity, and glycolysis by CcpA in Streptococcus thermophilus: evidence for carbon catabolite repression by a non-phosphoenolpyruvate-dependent phosphotransferase system sugar. J Bacteriol. 2000; 182(21):5982-9. PMC: 94730. DOI: 10.1128/JB.182.21.5982-5989.2000. View

Guedon E, Serror P, Ehrlich S, Renault P, Delorme C . Pleiotropic transcriptional repressor CodY senses the intracellular pool of branched-chain amino acids in Lactococcus lactis. Mol Microbiol. 2001; 40(5):1227-39. DOI: 10.1046/j.1365-2958.2001.02470.x. View

Levdikov V, Blagova E, Joseph P, Sonenshein A, Wilkinson A . The structure of CodY, a GTP- and isoleucine-responsive regulator of stationary phase and virulence in gram-positive bacteria. J Biol Chem. 2006; 281(16):11366-73. DOI: 10.1074/jbc.M513015200. View

Biswas I, Gruss A, Ehrlich S, Maguin E . High-efficiency gene inactivation and replacement system for gram-positive bacteria. J Bacteriol. 1993; 175(11):3628-35. PMC: 204764. DOI: 10.1128/jb.175.11.3628-3635.1993. View

Delorme C, Bartholini C, Bolotine A, Ehrlich S, Renault P . Emergence of a cell wall protease in the Streptococcus thermophilus population. Appl Environ Microbiol. 2009; 76(2):451-60. PMC: 2805209. DOI: 10.1128/AEM.01018-09. View

Hols P, Hancy F, Fontaine L, Grossiord B, Prozzi D, Leblond-Bourget N . New insights in the molecular biology and physiology of Streptococcus thermophilus revealed by comparative genomics. FEMS Microbiol Rev. 2005; 29(3):435-63. DOI: 10.1016/j.femsre.2005.04.008. View

Tamime A, Deeth H . Yogurt: Technology and Biochemistry . J Food Prot. 2019; 43(12):939-977. DOI: 10.4315/0362-028X-43.12.939. View

Hendriksen W, Bootsma H, Estevao S, Hoogenboezem T, de Jong A, de Groot R . CodY of Streptococcus pneumoniae: link between nutritional gene regulation and colonization. J Bacteriol. 2007; 190(2):590-601. PMC: 2223708. DOI: 10.1128/JB.00917-07. View

Fontaine L, Boutry C, Henry de Frahan M, Delplace B, Fremaux C, Horvath P . A novel pheromone quorum-sensing system controls the development of natural competence in Streptococcus thermophilus and Streptococcus salivarius. J Bacteriol. 2009; 192(5):1444-54. PMC: 2820839. DOI: 10.1128/JB.01251-09. View

10.

Malke H, Steiner K, McShan W, Ferretti J . Linking the nutritional status of Streptococcus pyogenes to alteration of transcriptional gene expression: the action of CodY and RelA. Int J Med Microbiol. 2006; 296(4-5):259-75. DOI: 10.1016/j.ijmm.2005.11.008. View

11.

Gunnewijk M, Poolman B . HPr(His approximately P)-mediated phosphorylation differently affects counterflow and proton motive force-driven uptake via the lactose transport protein of Streptococcus thermophilus. J Biol Chem. 2000; 275(44):34080-5. DOI: 10.1074/jbc.M003513200. View

12.

Mitchell T . The pathogenesis of streptococcal infections: from tooth decay to meningitis. Nat Rev Microbiol. 2004; 1(3):219-30. DOI: 10.1038/nrmicro771. View

13.

Pagels M, Fuchs S, Pane-Farre J, Kohler C, Menschner L, Hecker M . Redox sensing by a Rex-family repressor is involved in the regulation of anaerobic gene expression in Staphylococcus aureus. Mol Microbiol. 2010; 76(5):1142-61. PMC: 2883068. DOI: 10.1111/j.1365-2958.2010.07105.x. View

14.

Molle V, Nakaura Y, Shivers R, Yamaguchi H, Losick R, Fujita Y . Additional targets of the Bacillus subtilis global regulator CodY identified by chromatin immunoprecipitation and genome-wide transcript analysis. J Bacteriol. 2003; 185(6):1911-22. PMC: 150151. DOI: 10.1128/JB.185.6.1911-1922.2003. View

15.

Guo T, Kong J, Zhang L, Zhang C, Hu S . Fine tuning of the lactate and diacetyl production through promoter engineering in Lactococcus lactis. PLoS One. 2012; 7(4):e36296. PMC: 3338672. DOI: 10.1371/journal.pone.0036296. View

16.

Sonenshein A . Control of key metabolic intersections in Bacillus subtilis. Nat Rev Microbiol. 2007; 5(12):917-27. DOI: 10.1038/nrmicro1772. View

17.

Garault P, Letort C, Juillard V, Monnet V . Branched-chain amino acid biosynthesis is essential for optimal growth of Streptococcus thermophilus in milk. Appl Environ Microbiol. 2000; 66(12):5128-33. PMC: 92433. DOI: 10.1128/AEM.66.12.5128-5133.2000. View

18.

Petranovic D, Guedon E, Sperandio B, Delorme C, Ehrlich D, Renault P . Intracellular effectors regulating the activity of the Lactococcus lactis CodY pleiotropic transcription regulator. Mol Microbiol. 2004; 53(2):613-21. DOI: 10.1111/j.1365-2958.2004.04136.x. View

19.

Letort C, Juillard V . Development of a minimal chemically-defined medium for the exponential growth of Streptococcus thermophilus. J Appl Microbiol. 2002; 91(6):1023-9. DOI: 10.1046/j.1365-2672.2001.01469.x. View

20.

Neviani E, Giraffa G, Brizzi A, Carminati D . Amino acid requirements and peptidase activities of Streptococcus salivarius subsp. thermophilus. J Appl Bacteriol. 1995; 79(3):302-7. DOI: 10.1111/j.1365-2672.1995.tb03141.x. View