Evidence that the essential response regulator YycF in Streptococcus pneumoniae modulates expression of fatty acid biosynthesis genes and alters membrane composition

Journal of Bacteriology

Volumn 187, Issue 7, 2005, Pages 2357-2367

  Mohedano, M Luz ^a   Overweg, Karin ^b   De La Fuente, Alicia ^a   Reuter, Mark ^b   Altabe, Silvia ^c   Mulholland, Francis ^b   De Mendoza, Diego ^c   López, Paloma ^a   Wells, Jerry M ^b  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^b INSTITUTE OF FOOD RESEARCH   (United Kingdom)

^c UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE LIPID; PROTEIN HISTIDINE KINASE;

ARTICLE; AUTOREGULATION; BACILLUS SUBTILIS; BACTERIAL CELL; BIOSYNTHESIS; CELL GROWTH; FATTY ACID SYNTHESIS; GENE EXPRESSION; GENOME; GRAM POSITIVE BACTERIUM; LIPID COMPOSITION; MASS SPECTROMETRY; METABOLISM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; REGULON; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STREPTOCOCCUS PNEUMONIAE; VIRULENCE;

BACTERIAL PROTEINS; CELL MEMBRANE; FATTY ACIDS; GENE EXPRESSION REGULATION, BACTERIAL; MICROARRAY ANALYSIS; PROTEOMICS; SIGNAL TRANSDUCTION; STREPTOCOCCUS PNEUMONIAE; TRANSCRIPTION, GENETIC;

EID: 15244344437     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.187.7.2357-2367.2005     Document Type: Article

References (44)

1. Acebo, P., C. Nieto, M. A. Corrales, M. Espinosa, and P. López. 2000. Quantitative detection of Streptococcus pneumoniae cells harbouring single or multiple copies of the green fluorescence protein. Microbiology 146:1267-1273.
2. Alekshun, M. N., S. B. Levy, T. R. Mealy, B. A. Seaton, and J. F. Head. 2001. The crystal structure of MarR, a regulator of multiple antibiotic resistance, at 2.3 A resolution. Nat. Struct. Biol. 8:710-714.
3. Alves, R., and M. A. Savageau. 2003. Comparative analysis of prototype two-component systems with either bifunctional or monofunctional sensors: differences in molecular structure and physiological function. Mol. Microbiol. 48:25-51.
4. Birnboim, H. C., and J. Doly. 1979. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 7:1513-1523.
5. Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purification. Can. J. Med. Sci. 37:911-917.
6. Brown, J. S., S. M. Gilliland, and D. W. Holden. 2001. A Streptococcus pneumoniae pathogenicity island encoding an ABC transporter involved in iron uptake and virulence. Mol. Microbiol. 40:572-585.
7. Brown, J. S., and D. W. Holden. 2002., Iron acquisition by gram-positive bacterial pathogens. Microbes Infect. 4:1149-1156.
8. Christie, W. 1989. Gas chromatography and lipids. The Oily Press, Ayr, Scotland.
9. Clevel, W. S., and S. J. Devlin. 1988. Locally-weighted regression: an approach to regression analysis by local fitting. J. Am. Stat. Assoc. 83:596-610.
10. Cronan, J. E., and E. P. Gelmann. 1975. Physical properties of membrane lipids: biological relevance and regulation. Bacteriol. Rev. 39:232-256.
11. Davis, M. S., and J. E. Cronan, Jr. 2001. Inhibition of Escherichia coli acetyl coenzyme A carboxylase by acyl-acyl carrier protein. J. Bacteriol. 183:1499-1503.
12. Dietz, P., G. Gerlach, and D. Beier. 2002. Identification of target genes regulated by the two-component system HP166-HP165 of Helicobacter pylori. J. Bacteriol. 184:350-362.
13. Dubrac, S., and T. Msadek. 2004. Identification of genes controlled by the essential YycG/YycF two-component system of Staphylococcus aureus. J. Bacteriol. 186:1175-1181.
14. Echenique, J. R., and M. C. Trombe. 2001. Competence repression under oxygen limitation through the two-component MicAB signal transducing system in Streptococcus pneumoniae and involvement of the PAS domain of MicB. J. Bacteriol. 183:4599-4608.
15. Ermolaeva, M. D., O. White, and S. L. Salzberg. 2001. Prediction of operons in microbial genomes. Nucleic Acids Res. 29:1216-1221.
16. Fabret, C., and J. A. Hoch. 1998. A two-component signal transduction system essential for growth of Bacillus subtilis: implications for antiinfective therapy. J. Bacteriol. 180:6375-6383.
17. Fukuchi, K., Y. Kasahara, K. Asai, K. Kobayashy, S. Moriya, and N. Ogaswara. 2000. The essential two component regulatory system encoded by yycF and yycG modulates expression of the ftsAZ operon in Bacillus subtilis. Microbiology 146:1573-1583.
18. Galperin, M. Y., A. N. Nikolskaya, and E. V. Koonin. 2001. Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol. Lett. 203:11-21.
19. Giard, J. C., A. Rince, H. Capiaux, Y. Auffray, and A. Hartke. 2000. Inactivation of the stress- and starvation-inducible gls24 operon has a pleiotrophic effect on cell morphology, stress sensitivity, and gene expression in Enterococcus faecalis. J. Bacteriol. 182:4512-4520.
20. Havarstein, L. S., P. Gaustad, I. F. Nes, and D. A. Morrison. 1996. Identification of the streptococcal competence-pheromone receptor. Mol. Microbiol. 21:863-869.
21. Heath, R. J., S. W. White, and C. O. Rock. 2001. Lipid biosynthesis as a target for antibacterial agents. Prog. Lipid Res. 40:467-497.
22. Hinds, J., A. A. Witney, and J. K. Vass. 2002. Microarray design for bacterial genomes, p. 67-82. In B. W. Wren and N. Dorrell (ed.), Methods in microbiology: functional microbial genomics. Academic Press, London, United Kingdom.
23. Hoch, J. A., and T. J. Silhavy (ed.). 1995. Two-component signal transduction. ASM Press, Washington, D.C.
24. Howell, A., S. Dubrac, K. K. Andersen, D. Noone, J. Fert, T. Msadek, and K. Devine. 2003. Genes controlled by the essential YycG/YycF two-component system of Bacillus subtilis revealed through a novel hybrid regulator approach. Mol. Microbiol. 49:1639-1655.
25. Kadioglu, A., J. Echenique, S. Manco, M. C. Trombe, and P. W. Andrew. 2003. The MicAB two-component signaling system is involved in virulence of Streptococcus pneumoniae. Infect. Immun. 71:6676-6679.
26. Lacks, S. 1968. Genetic regulation of maltosaccharide utilization in Pneumococcus. Genetics 60:685-706.
27. Lange, R., C. Wagner, A. de Saizieu, N. Flint, J. Molnos, M. Stieger, et al. 1999. Domain organization and molecular characterization of 13 two-component systems identified by genome sequencing of Streptococcus pneumoniae. Gene 237:223-234.
28. Marrakchi, H., K. H. Choi, and C. O. Rock. 2002. A new mechanism for anaerobic unsaturated fatty acid formation in Streptococcus pneumoniae. J. Biol. Chem. 277:44809-44816.
29. Martin, P. K., T. Li, D. Sun, D. P. Biek, and M. B. Schmid. 1999. Role in cell permeability of an essential two-component system in Staphylococcus aureus. J. Bacteriol. 181:3666-3673.
30. Mileykovskaya, E., I. Fishov, X. Fu, B. D. Corbin, W. Margolin, and W. Dowhan. 2003. Effects of phospholipid composition on MinD-membrane interactions in vitro and in vivo. J. Biol. Chem. 278:22193-22198.
31. Morein, S., A. Andersson, L. Rilfors, and G. Lindblom. 1996. Wild-type Escherichia coli cells regulate the membrane lipid composition in a "window" between gel and non-lamellar structures. J. Biol. Chem. 271:6801-6809.
32. Ng, W. L., G. T. Robertson, K. M. Kazmierczak, J. Zhao, R. Gilmour, and M. E. Winkler. 2003. Constitutive expression of PcsB suppresses the requirement for the essential VicR (YycF) response regulator in Streptococcus pneumoniae R6. Mol. Microbiol. 50:1647-1663.
33. Nieto, C., P. Fernández de Palencia, P. López, and M. Espinosa. 2000. Construction of tightly regulated plasmid vector for Streptococcus pneumoniae: controlled expression of the green fluorescent protein. Plasmid 43:205-213.
34. M. Influence of a proximal divergent promoter region and competition between MaIR and RNA polymerase proteins. J. Biol. Chem. 276:14946-14954.
35. Ogura, M., H. Yamaguchi, K. Yoshida, Y. Fujita, and T. Tanaka. 2001. DNA microarray analysis of Bacillus subtilis DegU, ComA and PhoP regulons: an approach to comprehensive analysis of B. subtilis two-component regulatory systems. Nucleic Acids Res. 29:3804-3813.
36. Pearson, B. M., C. Pin, J. Wright, K. I'Anson, T. Humphrey, and J. M. Wells. 2003. Comparative genome analysis of Campylobacter jejuni using whole genome DNA microarrays. FEBS Lett. 554:224-230.
37. Stassi, D. L., P. Lopez, M. Espinosa, and S. A. Lacks. 1981. Cloning of chromosomal genes in Streptococcus pneumoniae. Proc. Natl. Acad. Sci. USA 78:7028-7032.
38. Stephenson, K., and J. A. Hoch. 2002. Virulence- and antibiotic resistance-associated two-component signal transduction systems of gram-positive pathogenic bacteria as targets for antimicrobial therapy. Pharmacol. Ther. 93:293-305.
39. Taylor, B. L., and I. B. Zhulin. 1999. PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol. Mol. Biol. Rev. 63:479-506.
40. Tettelin, H., K. E. Nelson, I. T. Paulsen, J. A. Eisen, T. D. Read, S. Peterson, et al. 2001. Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 293:498-506.
41. Throup, J. P., K. K. Koretke, A. P. Bryan, K. A. Ingraham, A. F. Chalker, Y. Ge, et al. 2000. A genomic analysis of two component signal transduction in Streptococcus pneumoniae. Mol. Microbiol. 35:566-576.
42. Wagner, C., A. de Saizieu, H. J. Schönfeld, M. Kamber, R. Lange, C. J. Thompson, and M. G. Page. 2002. Genetic analysis and functional characterization of the Streptococcus pneumoniae vic operon. Infect. Immun. 70: 6121-6128.
43. White, D. C., and F. E. Frerman. 1968. Fatty acid composition of complex lipids in Staphylococcus aureus during formation of the membrane-bound electron transport system. J. Bacteriol. 95:2198-2209.
44. Yamamoto, K., A. Shibahara, T. Nakayama, and G. Kajimoto. 1991. Determination of double-bond positions in methylene-interrupted dienoic fatty acids by GC-MS as their dimethyl disulfide adducts. Chem. Phys. Lipids 60:39-50.