Activity of the response regulator CiaR in mutants of Streptococcus pneumoniae R6 altered in acetyl phosphate production

Frontiers in Microbiology

Volumn 5, Issue DEC, 2014, Pages

  Marx, Patrick ^a,b   Meiers, Marina ^a   Brückner, Reinhold ^a  

^a University of Koblenz Landau   (Germany)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETATE KINASE; ACETIC ACID; ACETYL PHOSPHATE; BACTERIOCIN; BETA GALACTOSIDASE; COGNATE KINASE; DNA BINDING PROTEIN; DNA BINDING PROTEIN CIAR; PHOSPHATE ACETYLTRANSFERASE; PHOSPHORIC ACID DERIVATIVE; PHOSPHOTRANSFERASE; PYRUVATE OXIDASE; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; BACTERIUM COMPETENCE; BACTERIUM MUTANT; DNA BINDING; GENE EXPRESSION; GENE INACTIVATION; GENE OVEREXPRESSION; GENE REGULATORY NETWORK; NONHUMAN; PROTEIN PHOSPHORYLATION; STREPTOCOCCUS PNEUMONIAE;

STREPTOCOCCUS PNEUMONIAE;

EID: 84920670093     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00772     Document Type: Article

References (62)

1. Alloing, G., Granadel, C., Morrison, D.A., and Claverys, J.P. (1996). Competence pheromone, oligopeptide permease, and induction of competence in Streptococcus pneumoniae. Mol. Microbiol. 21, 471-478.
2. Avery, O.T., Macleod, C.M., and Mccarty, M. (1944). Studies on the chemical nature of the substance inducing transformation of pneumococcal types:Induction of transformation by a desoxyribonucleic acid fraction isolated from pneumococcus type III. J. Exp. Med. 79, 137-158.
3. Barak, R., Yan, J., Shainskaya, A., and Eisenbach, M. (2006). The chemotaxis response regulator CheY can catalyze its own acetylation. J. Mol. Biol. 359, 251-265.
4. Bättig, P., and Mühlemann, K. (2008). Influence of the spxB gene on competence in Streptococcus pneumoniae. J. Bacteriol. 190, 1184-1189.
5. Belanger, A.E., Clague, M.J., Glass, J.I., and Leblanc, D.J. (2004). Pyruvate oxidase is a determinant of Avery's rough morphology. J. Bacteriol. 186, 8164-8171.
6. Carvalho, S.M., Farshchi Andisi, V., Gradstedt, H., Neef, J., Kuipers, O.P., Neves, A.R., and Bijlsma, J.J. (2013). Pyruvate oxidase influences the sugar utilization pattern and capsule production in Streptococcus pneumoniae. PLoS One 8, e68277.
7. Cassone, M., Gagne, A.L., Spruce, L.A., Seeholzer, S.H., and Sebert, M.E. (2012). The HtrA Protease from Streptococcus pneumoniae Digests Both Denatured Proteins and the Competence-stimulating Peptide. J. Biol. Chemistry 287, 38449-38459.
8. Chan, S.H., Norregaard, L., Solem, C., and Jensen, P.R. (2014). Acetate kinase isozymes confer robustness in acetate metabolism. PLoS One 9, e92256.
9. Commichau, F.M., and Stülke, J. (2008). Trigger enzymes: bifunctional proteins active in metabolism and in controlling gene expression. Mol. Microbiol. 67, 692-702.
10. Crisostomo, M.I., Vollmer, W., Kharat, A.S., Inhulsen, S., Gehre, F., Buckenmaier, S., and Tomasz, A. (2006). Attenuation of penicillin resistance in a peptidoglycan O-acetyl transferase mutant of Streptococcus pneumoniae. Mol. Microbiol. 61, 1497-1509.
11. Dagkessamanskaia, A., Moscoso, M., Henard, V., Guiral, S., Overweg, K., Reuter, M., Martin, B., Wells, J., and Claverys, J.P. (2004). Interconnection of competence, stress and CiaR regulons in Streptococcus pneumoniae: competence triggers stationary phase autolysis of ciaR mutant cells. Mol. Microbiol. 51, 1071-1086.
12. Dawid, S., Sebert, M.E., and Weiser, J.N. (2009). Bacteriocin activity of Streptococcus pneumoniae is controlled by the serine protease HtrA via posttranscriptional regulation. J. Bacteriol. 191, 1509-1518.
13. Denapaite, D., Brückner, R., Hakenbeck, R., and Vollmer, W. (2012). Biosynthesis of Teichoic Acids in Streptococcus pneumoniae and Closely Related Species: Lessons from Genomes. Microb. Drug. Resist. 18, 344-358. doi: 10.1089/mdr.2012.0026 [doi].
14. Gao, R., and Stock, A.M. (2009). Biological insights from structures of two-component proteins. Annu. Rev. Microbiol. 63, 133-154.
15. Guenzi, E., Gasc, A.M., Sicard, M.A., and Hakenbeck, R. (1994). A two-component signal transducing system is involved in competence and penicillin susceptibility in laboratory mutants of Streptococcus pneumoniae. Mol. Microbiol. 12, 505-515.
16. Gueriri, I., Bay, S., Dubrac, S., Cyncynatus, C., and Msadek, T. (2008). The Pta-AckA pathway controlling acetyl phosphate levels and the phosphorylation state of the DegU orphan response regulator both play a role in regulating Listeria monocytogenes motility and chemotaxis. Mol. Microbiol. 70, 1342-1357.
17. Halfmann, A., Hakenbeck, R., and Brückner, R. (2007a). A new integrative reporter plasmid for Streptococcus pneumoniae. FEMS Microbiol. Lett. 268, 217-224.
18. Halfmann, A., Kovács, M., Hakenbeck, R., and Brückner, R. (2007b). Identification of the genes directly controlled by the response regulator CiaR in Streptococcus pneumoniae: five out of 15 promoters drive expression of small non-coding RNAs. Mol. Microbiol. 66, 110-126.
19. Halfmann, A., Schnorpfeil, A., Müller, M., Marx, P., Günzler, U., Hakenbeck, R., and Brückner, R. (2011). Activity of the two-component regulatory system CiaRH in Streptococcus pneumoniae R6. J. Mol. Microbiol. Biotechnol. 20, 96-104.
20. Hanahan, D. (1983). Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166, 557-580.
21. Hoskins, J., Alborn, W.E., Jr., Arnold, J., Blaszczak, L.C., Burgett, S., Dehoff, B.S., Estrem, S.T., Fritz, L., Fu, D.J., Fuller, W., Geringer, C., Gilmour, R., Glass, J.S., Khoja, H., Kraft, A.R., Lagace, R.E., Leblanc, D.J., Lee, L.N., Lefkowitz, E.J., Lu, J., Matsushima, P., Mcahren, S.M., Mchenney, M., Mcleaster, K., Mundy, C.W., Nicas, T.I., Norris, F.H., M, O.G., Peery, R.B., Robertson, G.T., Rockey, P., Sun, P.M., Winkler, M.E., Yang, Y., Young-Bellido, M., Zhao, G., Zook, C.A., Baltz, R.H., Jaskunas, S.R., Rosteck, P.R., Jr., Skatrud, P.L., and Glass, J.I. (2001). Genome of the Bacterium Streptococcus pneumoniae Strain R6. J. Bacteriol. 183, 5709-5717.
22. Hu, L.I., Chi, B.K., Kuhn, M.L., Filippova, E.V., Walker-Peddakotla, A.J., Basell, K., Becher, D., Anderson, W.F., Antelmann, H., and Wolfe, A.J. (2013). Acetylation of the response regulator RcsB controls transcription from a small RNA promoter. J. Bacteriol. 195, 4174-4186.
23. Ibrahim, Y.M., Kerr, A.R., Mccluskey, J., and Mitchell, T.J. (2004). Control of virulence by the two-component system CiaR/H is mediated via HtrA, a major virulence factor of Streptococcus pneumoniae. J. Bacteriol. 186, 5258-5266.
24. Kochan, T.J., and Dawid, S. (2013). The HtrA Protease of Streptococcus pneumoniae Controls Density-Dependent Stimulation of the Bacteriocin blp Locus via Disruption of Pheromone Secretion. J. Bacteriol. 195, 1561-1572. doi: 10.1128/jb.01964-12.
25. Krell, T., Lacal, J., Busch, A., Silva-Jimenez, H., Guazzaroni, M.E., and Ramos, J.L. (2010). Bacterial sensor kinases: diversity in the recognition of environmental signals. Annu. Rev. Microbiol. 64, 539-559.
26. Kuhn, M.L., Zemaitaitis, B., Hu, L.I., Sahu, A., Sorensen, D., Minasov, G., Lima, B.P., Scholle, M., Mrksich, M., Anderson, W.F., Gibson, B.W., Schilling, B., and Wolfe, A.J. (2014). Structural, kinetic and proteomic characterization of acetyl phosphate-dependent bacterial protein acetylation. PLoS One 9, e94816.
27. Kumar, R., Shah, P., Swiatlo, E., Burgess, S.C., Lawrence, M.L., and Nanduri, B. (2010). Identification of novel non-coding small RNAs from Streptococcus pneumoniae TIGR4 using high-resolution genome tiling arrays. BMC Genomics 11, 350.
28. Lacks, S., and Hotchkiss, R.D. (1960). A study of the genetic material determining an enzyme in Pneumococcus. Biochim. Biophys. Acta. 39, 508-518.
29. Lanie, J.A., Ng, W.L., Kazmierczak, K.M., Andrzejewski, T.M., Davidsen, T.M., Wayne, K.J., Tettelin, H., Glass, J.I., and Winkler, M.E. (2007). Genome sequence of Avery's virulent serotype 2 strain D39 of Streptococcus pneumoniae and comparison with that of unencapsulated laboratory strain R6. J. Bacteriol. 189, 38-51.
30. Laub, M.T., and Goulian, M. (2007). Specificity in two-component signal transduction pathways. Annu. Rev. Genet. 41, 121-145.
31. Lima, B.P., Antelmann, H., Gronau, K., Chi, B.K., Becher, D., Brinsmade, S.R., and Wolfe, A.J. (2011). Involvement of protein acetylation in glucose-induced transcription of a stress589 responsive promoter. Mol. Microbiol. 81, 1190-1204.
32. Lima, B.P., Thanh Huyen, T.T., Basell, K., Becher, D., Antelmann, H., and Wolfe, A.J. (2012). Inhibition of acetyl phosphate-dependent transcription by an acetylatable lysine on RNA polymerase. J. Biol. Chem. 287, 32147-32160.
33. Lukat, G.S., Mc cleary, W.R., Stock, A.M., and Stock, J.B. (1992). Phosphorylation of bacterial response regulator proteins by low molecular weight phospho-donors. Proc. Natl. Acad. Sci. U S A 89, 718-722.
34. Mann, B., Van Opijnen, T., Wang, J., Obert, C., Wang, Y.D., Carter, R., Mcgoldrick, D.J., Ridout, G., Camilli, A., Tuomanen, E.I., and Rosch, J.W. (2012). Control of Virulence by Small RNAs in Streptococcus pneumoniae. PLoS Pathog. 8, e1002788.
35. Marra, A., Asundi, J., Bartilson, M., Lawson, S., Fang, F., Christine, J., Wiesner, C., Brigham, D., Schneider, W.P., and Hromockyj, A.E. (2002). Differential fluorescence induction analysis of Streptococcus pneumoniae identifies genes involved in pathogenesis. Infect. Immun. 70, 1422-1433.
36. Martínez-Hackert, E., and Stock, A.M. (1997). Structural relationships in the OmpR family of winged-helix transcription factors. J. Mol. Biol. 269, 301-312.
37. Mascher, T., Heintz, M., Zähner, D., Merai, M., and Hakenbeck, R. (2006a). The CiaRH system of Streptococcus pneumoniae prevents lysis during stress induced by treatment with cell wall inhibitors and mutations in pbp2x involved in ß-lactam resistance. J. Bacteriol. 188, 1959-1978.
38. Mascher, T., Helmann, J.D., and Unden, G. (2006b). Stimulus perception in bacterial signal transducing histidine kinases. Microbiol. Mol. Biol. Rev. 70, 910-938.
39. Müller, M., Marx, P., Hakenbeck, R., and Brückner, R. (2011). Effect of new alleles of the histidine kinase gene ciaH on the activity of the response regulator CiaR in Streptococcus pneumoniae R6. Microbiology 157, 3104-3112.
40. Ottolenghi, E., and Hotchkiss, R.D. (1962). Release of genetic transforming agent from pneumococcal cultures during growth and disintegration. J. Exp. Med. 116, 491-519.
41. Pericone, C.D., Park, S., Imlay, J.A., and Weiser, J.N. (2003). Factors contributing to hydrogen peroxide resistance in Streptococcus pneumoniae include pyruvate oxidase (SpxB) and avoidance of the toxic effects of the fenton reaction. J. Bacteriol. 185, 6815-6825.
42. Prüss, B.M., and Wolfe, A.J. (1994). Regulation of acetyl phosphate synthesis and degradation, and the control of flagellar expression in Escherichia coli. Mol. Microbiol. 12, 973-984.
43. Puri, P., Goel, A., Bochynska, A., and Poolman, B. (2014). Regulation of acetate kinase isozymes and its importance for mixed-acid fermentation in Lactococcus lactis. J. Bacteriol. 196, 1386-1393.
44. Ramos-Montanez, S., Kazmierczak, K.M., Hentchel, K.L., and Winkler, M.E. (2010). Instability of ackA (Acetate Kinase) Mutations and Their Effects on Acetyl Phosphate (AcP) and ATP Amounts in Streptococcus pneumoniae D39. J. Bacteriol. 192, 6390-6400.
45. Ramos-Montanez, S., Tsui, H.C., Wayne, K.J., Morris, J.L., Peters, L.E., Zhang, F., Kazmierczak, K.M., Sham, L.T., and Winkler, M.E. (2008). Polymorphism and regulation of the spxB (pyruvate oxidase) virulence factor gene by a CBS-HotDog domain protein (SpxR) in serotype 2 Streptococcus pneumoniae. Mol. Microbiol. 67, 729-746.
46. Schnorpfeil, A., Kranz, M., Kovacs, M., Kirsch, C., Gartmann, J., Brunner, I., Bittmann, S., and Brückner, R. (2013). Target evaluation of the non-coding csRNAs reveals a link of the two-component regulatory system CiaRH to competence control in Streptococcus pneumoniae R6. Mol. Microbiol. 89, 334-349.
47. Sebert, M.E., Palmer, L.M., Rosenberg, M., and Weiser, J.N. (2002). Microarray-based identification of htrA, a Streptococcus pneumoniae gene that is regulated by the CiaRH two-component system and contributes to nasopharyngeal colonization. Infect. Immun. 70, 4059-4067.
48. Sebert, M.E., Patel, K.P., Plotnick, M., and Weiser, J.N. (2005). Pneumococcal HtrA protease mediates inhibition of competence by the CiaRH two-component signaling system. J. Bacteriol. 187, 3969-3979.
49. Spellerberg, B., Cundell, D.R., Sandros, J., Pearce, B.J., Idanpaan-Heikkila, I., Rosenow, C., and Masure, H.R. (1996). Pyruvate oxidase, as a determinant of virulence in Streptococcus pneumoniae. Mol. Microbiol. 19, 803-813.
50. Sung, C.K., Li, H., Claverys, J.P., and Morrison, D.A. (2001). An rpsL cassette, janus, for gene replacement through negative selection in Streptococcus pneumoniae. Appl. Environ. Microbiol. 67, 5190-5196.
51. Throup, J.P., Koretke, K.K., Bryant, A.P., Ingraham, K.A., Chalker, A.F., Ge, Y., Marra, A., Wallis, N.G., Brown, J.R., Holmes, D.J., Rosenberg, M., and Burnham, M.K. (2000). A genomic analysis of two-component signal transduction in Streptococcus pneumoniae. Mol. Microbiol. 35, 566-576.
52. Tsui, H.C., Mukherjee, D., Ray, V.A., Sham, L.T., Feig, A.L., and Winkler, M.E. (2010). Identification and characterization of noncoding small RNAs in Streptococcus pneumoniae serotype 2 strain D39. J. Bacteriol. 192, 264-279.
53. Verdin, E., and Ott, M. (2013). Acetylphosphate: a novel link between lysine acetylation and intermediary metabolism in bacteria. Mol. Cell. 51, 132-134.
54. Vollmer, W. (2008). Structural variation in the glycan strands of bacterial peptidoglycan. FEMS Microbio.l Rev. 32, 287-306.
55. Vollmer, W., and Tomasz, A. (2000). The pgdA gene encodes for a peptidoglycan N661 acetylglucosamine deacetylase in Streptococcus pneumoniae. J. Biol. Chem. 275, 20496- 20501.
56. Wang, G., Xia, Y., Cui, J., Gu, Z., Song, Y., Chen, Y.Q., Chen, H., Zhang, H., and Chen, W. (2013). The Roles of Moonlighting Proteins in Bacteria. Curr. Issues Mo.l Biol. 16, 15- 22.
57. Wanner, B.L. (1992). Is cross regulation by phosphorylation of two-component response regulator proteins important in bacteria? J. Bacteriol. 174, 2053-2058.
58. Weinert, B.T., Iesmantavicius, V., Wagner, S.A., Scholz, C., Gummesson, B., Beli, P., Nystrom, T., and Choudhary, C. (2013). Acetyl-phosphate is a critical determinant of lysine acetylation in E. coli. Mol Cell 51, 265-272.
59. Wolfe, A.J. (2005). The acetate switch. Microbiol. Mol. Biol. Rev. 69, 12-50.
60. Xu, H., Caimano, M.J., Lin, T., He, M., Radolf, J.D., Norris, S.J., Gherardini, F., Wolfe, A.J., and Yang, X.F. (2010). Role of acetyl-phosphate in activation of the Rrp2-RpoN-RpoS pathway in Borrelia burgdorferi. PLoS Pathog 6, e1001104.
61. Yesilkaya, H., Spissu, F., Carvalho, S.M., Terra, V.S., Homer, K.A., Benisty, R., Porat, N., Neves, A.R., and Andrew, P.W. (2009). Pyruvate formate lyase is required for pneumococcal fermentative metabolism and virulence. Infect. Immun. 77, 5418-5427.
62. Zähner, D., Kaminski, K., Van Der Linden, M., Mascher, T., Merai, M., and Hakenbeck, R. (2002). The ciaR/ciaH regulatory network of Streptococcus pneumoniae. J. Mol. Microbiol. Biotechnol. 4, 211-216.