GalR Acts as a Transcriptional Activator of galKT in the Presence of Galactose in Streptococcus pneumoniae

Journal of Molecular Microbiology and Biotechnology

Volumn 25, Issue 6, 2015, Pages 363-371

  Afzal, Muhammad ^a,b   Shafeeq, Sulman ^c   Manzoor, Irfan ^b   Kuipers, Oscar P ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b GOVERNMENT COLLEGE UNIVERSITY   (Pakistan)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Carbon source; CcpA; Galactose; GalR; Leloir pathway; Pneumococcus; Tagatose pathway

Indexed keywords

BACTERIAL PROTEIN; GALACTOSE; REGULATOR PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GALE; TRANSCRIPTION FACTOR GALKT; TRANSCRIPTION FACTOR GALR; UNCLASSIFIED DRUG; BACTERIAL DNA; ESCHERICHIA COLI PROTEIN; GALACTOKINASE; GALACTOSE 1 PHOSPHATE URIDYLYLTRANSFERASE; GALACTOSE REPRESSOR PROTEINS; GLUCOSE; HEXOSE; REPRESSOR PROTEIN; TAGATOSE;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BASE PAIRING; CONTROLLED STUDY; GENETIC CONSERVATION; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STREPTOCOCCUS PNEUMONIAE; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; WILD TYPE; BACTERIAL GENE; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; OPERON; PROCEDURES;

BACTERIAL PROTEINS; BASE SEQUENCE; DNA, BACTERIAL; ESCHERICHIA COLI PROTEINS; GALACTOKINASE; GALACTOSE; GENES, BACTERIAL; GLUCOSE; HEXOSES; MICROARRAY ANALYSIS; MOLECULAR SEQUENCE DATA; MUTATION; OPERON; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION; REPRESSOR PROTEINS; STREPTOCOCCUS PNEUMONIAE; TRANSCRIPTIONAL ACTIVATION; UTP-HEXOSE-1-PHOSPHATE URIDYLYLTRANSFERASE;

EID: 84946781626     PISSN: 14641801     EISSN: 16602412     Source Type: Journal    
DOI: 10.1159/000439429     Document Type: Article

References (37)

1. Abranches J, Chen YY, Burne RA: Galactose metabolism by Streptococcus mutans. Appl Environ Microbiol 2004;70:6047-6052. 10.1128/AEM.70.10.6047-6052.2004 15466549
2. Afzal M, Manzoor I, Kuipers OP: A fast and reliable pipeline for bacterial transcriptome analysis case STUDY: serine-dependent gene regulation in Streptococcus pneumoniae. J Vis Exp 2015a, DOI: 10.3791/52649. 10.3791/52649 25938895
3. Afzal M, Shafeeq S, Henriques-Normark B, Kuipers OP: UlaR activates expression of the ula operon in Streptococcus pneumoniae in the presence of ascorbic acid. Microbiol Read Engl 2015b;161:41-49. 10.1099/mic.0.083899-0 25355938
4. Afzal M, Shafeeq S, Kuipers OP: LacR is a repressor of lacABCD and LacT is an activator of lacTFEG, constituting the lac gene cluster in Streptococcus pneumoniae. Appl Environ Microbiol 2014;80:5349-5358. 10.1128/AEM.01370-14 24951784
5. Ajdic D, Sutcliffe IC, Russell RR, Ferretti JJ: Organization and nucleotide sequence of the Streptococcus mutans galactose operon. Gene 1996;180:137-144. 10.1016/S0378-1119(96)00434-9 8973358
6. Baerends RJS, Smits WK, de Jong A, Hamoen LW, Kok J, Kuipers OP: Genome2D: a visualization tool for the rapid analysis of bacterial transcriptome data. Genome Biol 2004;5:R37. 10.1186/gb-2004-5-5-r37 15128451
7. Bailey TL, Elkan C: Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 1994;2:28-36. 7584402
8. Bidossi A, Mulas L, Decorosi F, Colomba L, Ricci S, Pozzi G, et al. A functional genomics approach to establish the complement of carbohydrate transporters in Streptococcus pneumoniae. PLoS One 2012;7:e33320. 10.1371/journal.pone.0033320 22428019
9. Buckwalter CM, King SJ: Pneumococcal carbohydrate transport: food for thought. Trends Microbiol 2012;20:517-522. 10.1016/j.tim.2012.08.008 22959614
10. Carvalho SM, Kloosterman TG, Kuipers OP, Neves AR: CcpA ensures optimal metabolic fitness of Streptococcus pneumoniae. PloS One 2011;6:e26707. 10.1371/journal.pone.0026707 22039538
11. de Vos WM, Vaughan EE: Genetics of lactose utilization in lactic acid bacteria. FEMS Microbiol Rev 1994;15:217-237. 10.1111/j.1574-6976.1994.tb00136.x 7946468
12. Frey PA: The Leloir pathway: a mechanistic imperative for three enzymes to change the stereochemical configuration of a single carbon in galactose. FASEB J 1996;10:461-470. 8647345
13. Fridovich-Keil JL: Galactosemia: the good, the bad, and the unknown. J Cell Physiol 2006;209:701-705. 10.1002/jcp.20820 17001680
14. Gorke B, Stulke J: Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat Rev Microbiol 2008;6:613-624. 10.1038/nrmicro1932 18628769
15. Hamilton IR, Lo GC: Co-induction of β-galactosidase and the lactose-P-enolpyruvate phosphotransferase system in Streptococcus salivarius and Streptococcus mutans. J Bacteriol 1978;136:900-908. 214423
16. Ispahani P, Slack RCB, Donald FE, Weston VC, Rutter N: Twenty year surveillance of invasive pneumococcal disease in Nottingham: serogroups responsible and implications for immunisation. Arch Dis Child 2004;89:757-762. 10.1136/adc.2003.036921 15269078
17. Iyer R, Baliga NS, Camilli A: Catabolite control protein A (CcpA) contributes to virulence and regulation of sugar metabolism in Streptococcus pneumoniae. J Bacteriol 2005;187:8340-8349. 10.1128/JB.187.24.8340-8349.2005 16321938
18. Jagusztyn-Krynicka EK, Hansen JB, Crow VL, Thomas TD, Honeyman AL, Curtiss R 3rd: Streptococcus mutans serotype c tagatose 6-phosphate pathway gene cluster. J Bacteriol 1992;174:6152-6158. 1328153
19. Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M: Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res 2014;42:D199-D205. 10.1093/nar/gkt1076 24214961
20. King SJ: Pneumococcal modification of host sugars: a major contributor to colonization of the human airway? Mol Oral Microbiol 2010;25:15-24. 10.1111/j.2041-1014.2009.00564.x 20331791
21. Kloosterman TG, Bijlsma JJE, Kok J, Kuipers OP: To have neighbour's fare: extending the molecular toolbox for Streptococcus pneumoniae. Microbiol Read Engl 2006;152:351-359. 10.1099/mic.0.28521-0 16436423
22. Lanie JA, Ng WL, Kazmierczak KM, Andrzejewski TM, Davidsen TM, Wayne KJ, et al. Genome sequence of Avery's virulent serotype 2 strain D39 of Streptococcus pneumoniae and comparison with that of unencapsulated laboratory strain R6. J Bacteriol 2007;189:38-51. 10.1128/JB.01148-06 17041037
23. Nguyen CC, Saier MH: Phylogenetic, structural and functional analyses of the LacI-GalR family of bacterial transcription factors. FEBS Lett 1995;377:98-102. 10.1016/0014-5793(95)01344-X 8543068
24. Nieto C, Espinosa M, Puyet A: The maltose/maltodextrin regulon of Streptococcus pneumoniae: differential promoter regulation by the transcriptional repressor MalR. J Biol Chem 1997;272:30860-30865. 10.1074/jbc.272.49.30860 9388231
25. O'Brien KL, Wolfson LJ, Watt JP, Henkle E, Deloria-Knoll M, McCall N, et al. Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates. Lancet 2009;374:893-902. 10.1016/S0140-6736(09)61204-6 19748398
26. Russell RR, Aduse-Opoku J, Sutcliffe IC, Tao L, Ferretti JJ: A binding protein-dependent transport system in Streptococcus mutans responsible for multiple sugar metabolism. J Biol Chem 1992;267:4631-4637. 1537846
27. T method. Nat Protoc 2008;3:1101-1108. 10.1038/nprot.2008.73 18546601
28. Shafeeq S, Afzal M, Henriques-Normark B, Kuipers OP: Transcriptional profiling of UlaR-regulated genes in Streptococcus pneumoniae. Genomics Data 2015;4:57-59. 10.1016/j.gdata.2015.02.004 26484177
29. Shafeeq S, Kloosterman TG, Kuipers OP: CelR-mediated activation of the cellobiose-utilization gene cluster in Streptococcus pneumoniae. Microbiol Read Engl 2011a;157:2854-2861. 10.1099/mic.0.051359-0 21778207
30. Shafeeq S, Kuipers OP, Kloosterman TG: Cellobiose-mediated gene expression in Streptococcus pneumoniae: a repressor function of the novel GntR-type regulator BguR. PloS One 2013;8:e57586. 10.1371/journal.pone.0057586 23469031
31. Shafeeq S, Yesilkaya H, Kloosterman TG, Narayanan G, Wandel M, Andrew PW, et al. The cop operon is required for copper homeostasis and contributes to virulence in Streptococcus pneumoniae. Mol Microbiol 2011b;81:1255-1270. 10.1111/j.1365-2958.2011.07758.x 21736642
32. Swint-Kruse L, Matthews KS: Allostery in the LacI/GalR family: variations on a theme. Curr Opin Microbiol 2009;12:129-137. 10.1016/j.mib.2009.01.009 19269243
33. Tettelin H, Nelson KE, Paulsen IT, Eisen JA, Read TD, Peterson S, et al. Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 2001;293:498-506. 10.1126/science.1061217 11463916
34. Titgemeyer F, Hillen W: Global control of sugar metabolism: a gram-positive solution. Antonie Van Leeuwenhoek 2002;82:59-71. 10.1023/A:1020628909429 12369205
35. Yesilkaya H, Manco S, Kadioglu A, Terra VS, Andrew PW: The ability to utilize mucin affects the regulation of virulence gene expression in Streptococcus pneumoniae. FEMS Microbiol Lett 2008;278:231-235. 10.1111/j.1574-6968.2007.01003.x 18053067
36. Zeng L, Das S, Burne RA: Utilization of lactose and galactose by Streptococcus mutans: transport, toxicity, and carbon catabolite repression. J Bacteriol 2010;192:2434-2444. 10.1128/JB.01624-09 20190045
37. Zomer AL, Buist G, Larsen R, Kok J, Kuipers OP: Time-resolved determination of the CcpA regulon of Lactococcus lactis subsp. cremoris MG1363. J Bacteriol 2007;189:1366-1381. 10.1128/JB.01013-06 17028270