Metabolic switches and adaptations deduced from the proteomes of Streptomyces coelicolor wild type and phoP mutant grown in batch culture

Molecular and Cellular Proteomics

Volumn 11, Issue 2, 2012, Pages

  Thomas, Louise ^a   Hodgson, David A ^b   Wentzel, Alexander ^c,d   Nieselt, Kay ^e   Ellingsen, Trond E ^c   Moore, Jonathan ^f   Morrissey, Edward R ^f   Legaie, Roxane ^f   Wohlleben, Wolfgang ^e   Rodríguez García, Antonio ^g   Martín, Juan F ^g   Burroughs, Nigel J ^f   Wellington, Elizabeth M H ^b   Smith, Margaret C M ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b UNIVERSITY OF WARWICK   (United Kingdom)

^c SINTEF MATERIALS AND CHEMISTRY   (Norway)

^d NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^e UNIVERSITY OF TÜBINGEN   (Germany)

^f UNIVERSITY OF WARWICK   (United Kingdom)

^g UNIVERSITY OF LEÓN   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; NITROGEN; PHOSPHATE; PROTEOME; BACTERIAL PROTEIN; BACTERIAL RNA; BIOLOGICAL MARKER; MESSENGER RNA; PHOP PROTEIN, BACTERIA;

ARTICLE; BACTERIAL GENE; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIUM CULTURE; CARBON METABOLISM; GENE DELETION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NITROGEN METABOLISM; PHOP GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STREPTOMYCES COELICOLOR; ACCLIMATIZATION; BATCH CELL CULTURE; CELL CULTURE; COMPARATIVE STUDY; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PROTEOMICS;

STREPTOMYCES; STREPTOMYCES COELICOLOR;

ACCLIMATIZATION; BACTERIAL PROTEINS; BATCH CELL CULTURE TECHNIQUES; BIOLOGICAL MARKERS; CELLS, CULTURED; CHROMATOGRAPHY, LIQUID; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHATES; PROTEOME; PROTEOMICS; RNA, BACTERIAL; RNA, MESSENGER; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; STREPTOMYCES COELICOLOR;

EID: 84863035945     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M111.013797     Document Type: Article

References (45)

1. Bibb, M. (1996) 1995 Colworth Prize Lecture. The regulation of antibiotic production in Streptomyces coelicolor A3(2). Microbiology 142, 1335-1344
2. Martín, J. F., and Liras, P. (2010) Engineering of regulatory cascades and networks controlling antibiotic biosynthesis in Streptomyces. Curr. Opin. Microbiol. 13, 263-273
3. Bibb, M. J. (2005) Regulation of secondary metabolism in streptomycetes. Curr. Opin. Microbiol. 8, 208-215
4. Nieselt, K., Battke, F., Herbig, A., Bruheim, P., Wentzel, A., Jakobsen, Ø. M., Sletta, H., Alam, M. T., Merlo, M. E., Moore, J., Omara, W. A., Morrissey, E. R., Juarez-Hermosillo, M. A., Rodríguez-García, A., Nentwich, M., Thomas, L., Iqbal, M., Legaie, R., Gaze, W. H., Challis, G. L., Jansen, R. C., Dijkhuizen, L., Rand, D. A., Wild, D. L., Bonin, M., Reuther, J., Wohlleben, W., Smith, M. C., Burroughs, N. J., Martín, J. F., Hodgson, D. A., Takano, E., Breitling, R., Ellingsen, T. E., and Wellington, E. M. (2010) The dynamic architecture of the metabolic switch in Streptomyces coelicolor. BMC Genomics 11, 10-18
5. Pawlik, K., Kotowska, M., Chater, K. F., Kuczek, K., and Takano, E. (2007) A cryptic type I polyketide synthase (cpk) gene cluster in Streptomyces coelicolor A3(2). Arch. Microbiol. 187, 87-99 (Pubitemid 46197385)
6. Ishihama, Y., Oda, Y., Tabata, T., Sato, T., Nagasu, T., Rappsilber, J., and Mann, M. (2005) Exponentially modified protein abundance index (Em- PAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol. Cell. Proteomics 4, 1265-1272 (Pubitemid 41448714)
7. Santos-Beneit, F., Rodríguez-García, A., Sola-Landa, A., and Martín, J. F. (2009) Cross-talk between two global regulators in Streptomyces: PhoP and AfsR interact in the control of afsS, pstS and phoRP transcription. Mol. Microbiol. 72, 53-68
8. Rodríguez-García, A., Barreiro, C., Santos-Beneit, F., Sola-Landa, A., and Martín, J. F. (2007) Genome-wide transcriptomic and proteomic analysis of the primary response to phosphate limitation in Streptomyces coelicolor M145 and in a ΔphoP mutant. Proteomics 7, 2410-2429
9. Barsnes, H., Vizcaíno, J. A., Eidhammer, I., and Martens, L. (2009) PRIDE Converter: Making proteomics data-sharing easy. Nat. Biotechnol. 27, 598-599
10. Vizcaíno, J. A., Côté, R., Reisinger, F., Barsnes, H., Foster, J. M., Rameseder, J., Hermjakob, H., and Martens, L. (2010) The Proteomics Identifications database: 2010 update. Nucleic Acids Res. 38, D736-D742
11. Novotna, J., Vohradsky, J., Berndt, P., Gramajo, H., Langen, H., Li, X. M., Minas, W., Orsaria, L., Roeder, D., and Thompson, C. J. (2003) Proteomic studies of diauxic lag in the differentiating prokaryote Streptomyces coelicolor reveal a regulatory network of stress-induced proteins and central metabolic enzymes. Mol. Microbiol. 48, 1289-1303 (Pubitemid 36718223)
12. Bucca, G., Brassington, A. M., Hotchkiss, G., Mersinias, V., and Smith, C. P. (2003) Negative feedback regulation of dnaK, clpB and lon expression by the DnaK chaperone machine in Streptomyces coelicolor, identified by transcriptome and in vivo DnaK-depletion analysis. Mol. Microbiol. 50, 153-166 (Pubitemid 37222794)
13. de Crécy-Lagard, V., Servant-Moisson, P., Viala, J., Grandvalet, C., and Mazodier, P. (1999) Alteration of the synthesis of the Clp ATP-dependent protease affects morphological and physiological differentiation in Streptomyces. Mol. Microbiol. 32, 505-517 (Pubitemid 29233896)
14. Servant, P., Thompson, C., and Mazodier, P. (1993) Use of new Escherichia coli/Streptomyces conjugative vectors to probe the functions of the two groEL-like genes of Streptomyces albus G by gene disruption. Gene 134, 25-32
15. Pearce, M. J., Mintseris, J., Ferreyra, J., Gygi, S. P., and Darwin, K. H. (2008) Ubiquitin-like protein involved in the proteasome pathway of Mycobacterium tuberculosis. Science 322, 1104-1107
16. Sanssouci, E., Lerat, S., Grondin, G., Shareck, F., and Beaulieu, C. (2011) tdd8: a TerD domain-encoding gene involved in Streptomyces coelicolor differentiation. Antonie van Leeuwenhoek 100, 385-398
17. Paget, M. S., Kang, J. G., Roe, J. H., and Buttner, M. J. (1998) SigmaR, an RNA polymerase sigma factor that modulates expression of the thioredoxin system in response to oxidative stress in Streptomyces coelicolor A3(2). EMBO J. 17, 5776-5782 (Pubitemid 28445988)
18. Facey, P. D., Hitchings, M. D., Saavedra-Garcia, P., Fernandez-Martinez, L., Dyson, P. J., and Del Sol, R. (2009) Streptomyces coelicolor Dps-like proteins: Differential dual roles in response to stress during vegetative growth and in nucleoid condensation during reproductive cell division. Mol. Microbiol. 73, 1186-1202
19. Fernández Martínez, L., Bishop, A., Parkes, L., Del Sol, R., Salerno, P., Sevcikova, B., Mazurakova, V., Kormanec, J., and Dyson, P. (2009) Osmoregulation in Streptomyces coelicolor: Modulation of SigB activity by OsaC. Mol. Microbiol. 71, 1250-1262
20. Bursy, J., Kuhlmann, A. U., Pittelkow, M., Hartmann, H., Jebbar, M., Pierik, A. J., and Bremer, E. (2008) Synthesis and uptake of the compatible solutes ectoine and 5-hydroxyectoine by Streptomyces coelicolor A3(2) in response to salt and heat stresses. Appl. Environ. Microbiol. 74, 7286-7296 (Pubitemid 352773580)
21. Schneider, D., Bruton, C. J., and Chater, K. F. (2000) Duplicated gene clusters suggest an interplay of glycogen and trehalose metabolism during sequential stages of aerial mycelium development in Streptomyces coelicolor A3(2). Mol. Gen. Genet. 263, 543-553
22. Sevcikova, B., Rezuchova, B., Homerova, D., and Kormanec, J. (2010) The anti-anti-sigma factor BldG is involved in activation of the stress response sigma factor sigma(H) in Streptomyces coelicolor A3(2). J. Bacteriol. 192, 5674-5681
23. Bignell, D. R., Warawa, J. L., Strap, J. L., Chater, K. F., and Leskiw, B. K. (2000) Study of the bldG locus suggests that an anti-anti-sigma factor and an anti-sigma factor may be involved in Streptomyces coelicolor antibiotic production and sporulation. Microbiology 146, 2161-2173
24. van Keulen, G., Siebring, J., and Dijkhuizen, L. (2011) In Streptomyces: Molecular Biology and Biotechnology (Dyson, P. J., ed) pp. 105-123, Caister Academic Press, Norfolk, UK
25. Tian, J., Bryk, R., Itoh, M., Suematsu, M., and Nathan, C. (2005) Variant tricarboxylic acid cycle in Mycobacterium tuberculosis: Identification of α-ketoglutarate decarboxylase. Proc. Natl. Acad. Sci. U.S.A. 102, 10670-10675 (Pubitemid 41061612)
26. Fischer, M., Alderson, J., van Keulen, G., White, J., and Sawers, R. G. (2010) The obligate aerobe Streptomyces coelicolor A3(2) synthesizes three active respiratory nitrate reductases. Microbiology 156, 3166-3179
27. Chasteen, T. G., Fuentes, D. E., Tantaleán, J. C., and Vásquez, C. C. (2009) Tellurite: History, oxidative stress, and molecular mechanisms of resistance. FEMS Microbiol. Rev. 33, 820-832
28. Tiffert, Y., Franz-Wachtel, M., Fladerer, C., Nordheim, A., Reuther, J., Wohlleben, W., and Mast, Y. (2011) Proteomic analysis of the GlnRmediated response to nitrogen limitation in Streptomyces coelicolor M145. Appl. Microbiol. Biotechnol. 89, 1149-1159
29. Tiffert, Y., Supra, P., Wurm, R., Wohlleben, W., Wagner, R., and Reuther, J. (2008) The Streptomyces coelicolor GlnR regulon: Identification of new GlnR targets and evidence for a central role of GlnR in nitrogen metabolism in actinomycetes. Mol. Microbiol. 67, 861-880 (Pubitemid 351143689)
30. Fisher, S. H. (1989) Glutamate synthesis in Streptomyces coelicolor. J. Bacteriol. 171, 2372-2377
31. Wohlleben, W., Mast, Y., and Reuther, J. (2011) In Streptomyces: Molecular Biology and Biotechnology (Dyson, P., ed) pp. 125-136, Caister Academic Press, Norfolk, UK
32. Rodríguez-García, A., Sola-Landa, A., Apel, K., Santos-Beneit, F., and Martín, J. F. (2009) Phosphate control over nitrogen metabolism in Streptomyces coelicolor: Direct and indirect negative control of glnR, glnA, glnII and amtB expression by the response regulator PhoP. Nucleic Acids Res. 37, 3230-3242
33. Sola-Landa, A., Rodríguez-García, A., Apel, A. K., and Martín, J. F. (2008) Target genes and structure of the direct repeats in the DNA-binding sequences of the response regulator PhoP in Streptomyces coelicolor. Nucleic Acids Res. 36, 1358-1368 (Pubitemid 351330950)
34. Fernández-Moreno, M. A., Caballero, J. L., Hopwood, D. A., and Malpartida, F. (1991) The act cluster contains regulatory and antibiotic export genes, direct targets for translational control by the bldA tRNA gene of Streptomyces. Cell 66, 769-780 (Pubitemid 121001710)
35. Tahlan, K., Ahn, S. K., Sing, A., Bodnaruk, T. D., Willems, A. R., Davidson, A. R., and Nodwell, J. R. (2007) Initiation of actinorhodin export in Streptomyces coelicolor. Mol. Microbiol. 63, 951-961 (Pubitemid 46184507)
36. Saito, N., Xu, J., Hosaka, T., Okamoto, S., Aoki, H., Bibb, M. J., and Ochi, K. (2006) EshA accentuates ppGpp accumulation and is conditionally required for antibiotic production in Streptomyces coelicolor A3(2). J. Bacteriol. 188, 4952-4961 (Pubitemid 43956092)
37. Bentley, S. D., Chater, K. F., Cerdeño-Tárraga, A. M., Challis, G. L., Thomson, N. R., James, K. D., Harris, D. E., Quail, M. A., Kieser, H., Harper, D., Bateman, A., Brown, S., Chandra, G., Chen, C. W., Collins, M., Cronin, A., Fraser, A., Goble, A., Hidalgo, J., Hornsby, T., Howarth, S., Huang, C. H., Kieser, T., Larke, L., Murphy, L., Oliver, K., O'Neil, S., Rabbinowitsch, E., Rajandream, M. A., Rutherford, K., Rutter, S., Seeger, K., Saunders, D., Sharp, S., Squares, R., Squares, S., Taylor, K., Warren, T., Wietzorrek, A., Woodward, J., Barrell, B. G., Parkhill, J., and Hopwood, D. A. (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417, 141-147 (Pubitemid 34506788)
38. McKenzie, N. L., and Nodwell, J. R. (2007) Phosphorylated AbsA2 negatively regulates antibiotic production in Streptomyces coelicolor through interactions with pathway-specific regulatory gene promoters. J. Bacteriol. 189, 5284-5292 (Pubitemid 47076074)
39. Yepes, A., Rico, S., Rodríguez-García, A., Santamaría, R. I., and Díaz, M. (2011) Novel two-component systems implied in antibiotic production in Streptomyces coelicolor. PloS One 6, e19980
40. Ryding, N. J., Anderson, T. B., and Champness, W. C. (2002) Regulation of the Streptomyces coelicolor calcium-dependent antibiotic by absA, encoding a cluster-linked two-component system. J. Bacteriol. 184, 794-805 (Pubitemid 34150227)
41. Hunt, A. C., Servín-González, L., Kelemen, G. H., and Buttner, M. J. (2005) The bldC developmental locus of Streptomyces coelicolor encodes a member of a family of small DNA-binding proteins related to the DNAbinding domains of the MerR family. J. Bacteriol. 187, 716-728 (Pubitemid 40096258)
42. Ryu, Y. G., Butler, M. J., Chater, K. F., and Lee, K. J. (2006) Engineering of primary carbohydrate metabolism for increased production of actinorhodin in Streptomyces coelicolor. Appl. Environ. Microbiol. 72, 7132-7139 (Pubitemid 44748426)
43. Diacovich, L., Peirú, S., Kurth, D., Rodríguez, E., Podestá, F., Khosla, C., and Gramajo, H. (2002) Kinetic and structural analysis of a new group of Acyl-CoA carboxylases found in Streptomyces coelicolor A3(2). J. Biol. Chem. 277, 31228-31236 (Pubitemid 34970830)
44. Rodríguez, E., Banchio, C., Diacovich, L., Bibb, M. J., and Gramajo, H. (2001) Role of an essential acyl coenzyme A carboxylase in the primary and secondary metabolism of Streptomyces coelicolor A3(2). Appl. Environ. Microbiol. 67, 4166-4176 (Pubitemid 33641713)
45. Wang, L., Tian, X., Wang, J., Yang, H., Fan, K., Xu, G., Yang, K., and Tan, H. (2009) Autoregulation of antibiotic biosynthesis by binding of the end product to an atypical response regulator. Proc. Natl. Acad. Sci. U.S.A. 106, 8617-8622