Lack of A-factor production induces the expression of nutrient scavenging and stress-related proteins in Streptomyces griseus

Molecular and Cellular Proteomics

Volumn 8, Issue 10, 2009, Pages 2396-2403

  Birkó, Zsuzsanna ^a   Swiatek, Magdalena ^d   Szájli, Emília ^b   Medzihradszky, Katalin F ^b,c   Vijgenboom, Erik ^d   Penyige, András ^a   Keseru, Judit ^a   Van Wezel, Gilles P ^d   Biro, Sándor ^a  

^a UNIVERSITY OF DEBRECEN   (Hungary)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d LEIDEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

FACTOR A; HYDROLASE; NUCLEIC ACID; SCAVENGER;

APOPTOSIS; ARTICLE; BACTERIAL STRAIN; CELL WALL; DEVELOPMENTAL GENE; ENVIRONMENTAL STRESS; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; MUTANT; MUTATION; MYCELIUM; NONHUMAN; NUTRIENT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; PROTEOMICS; REGULON; SPOROGENESIS; STARVATION; STREPTOMYCES GRISEUS; STRESS;

4-BUTYROLACTONE; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HEAT-SHOCK PROTEINS; MOLECULAR SEQUENCE DATA; PROTEOME; STREPTOMYCES GRISEUS; STRESS, PHYSIOLOGICAL; TRANSCRIPTION, GENETIC;

STREPTOMYCES GRISEUS; STREPTOMYCINEAE;

EID: 71049147860     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M900194-MCP200     Document Type: Article

References (46)

1. Chater, K. F. (1993) Genetics of differentiation in Streptomyces. Annu. Rev. Microbiol. 47, 685-713
2. Rigali, S., Nothaft, H., Noens, E. E., Schlicht, M., Colson, S., Müller, M., Joris, B., Koerten, H. K., Hopwood, D. A., Titgemeyer, F., and van Wezel, G. P. (2006) The sugar phosphotransferase system of Streptomyces coelicolor is regulated by the GntR-family regulator DasR and links N-acetylglucosamine metabolism to the control of development. Mol. Microbiol. 61, 1237-1251
3. Chater, K. F. (2006) Streptomyces inside-out: a new perspective on the bacteria that provide us with antibiotics. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361, 761-768
4. Horinouchi, S., and Beppu, T. (1992) Autoregulatory factors and communication in actinomycetes. Annu. Rev. Microbiol. 46, 377-398
5. Horinouchi, S., and Beppu, T. (1994) A-factor as a microbial hormone that controls cellular differentiation and secondary metabolism in Streptomyces griseus. Mol. Microbiol. 12, 859-864
6. Nakano, H., Takehara, E., Nihira, T., and Yamada, Y. (1998) Gene replacement analysis of the Streptomyces virginiae barA gene encoding the butyrolactone autoregulator receptor reveals that BarA acts as a repressor in virginiamycin biosynthesis. J. Bacteriol. 180, 3317-3322 (Pubitemid 28307203)
7. Takano, E., Chakraburtty, R., Nihira, T., Yamada, Y., and Bibb, M. J. (2001) A complex role for the gamma-butyrolactone SCB1 in regulating antibiotic production in Streptomyces coelicolor A3(2). Mol. Microbiol. 41, 1015-1028
8. Takano, E., Kinoshita, H., Mersinias, V., Bucca, G., Hotchkiss, G., Nihira, T., Smith, C. P., Bibb, M., Wohlleben, W., and Chater, K. (2005) A bacterial hormone (the SCB1) directly controls the expression of a pathway-specific regulatory gene in the cryptic type I polyketide biosynthetic gene cluster of Streptomyces coelicolor. Mol. Microbiol. 56, 465-479
9. Ohnishi, Y., Yamazaki, H., Kato, J. Y., Tomono, A., and Horinouchi, S. (2005) AdpA, a central transcriptional regulator in the A-factor regulatory cascade that leads to morphological development and secondary metabolism in Streptomyces griseus. Biosci. Biotechnol. Biochem. 69, 431-439
10. Horinouchi, S. (2007) Mining and polishing of the treasure trove in the bacterial genus Streptomyces. Biosci. Biotechnol. Biochem. 71, 283-299
11. Biró, S., Békési, I., Vitális, S., and Szabó, G. (1980) A substance effecting differentiation in Streptomyces griseus. Purification and properties. Eur. J. Biochem. 103, 359-363
12. Kiss, Z., Ward, A. C., Birkó, Z., Chater, K. F., and Biró, S. (2008) Streptomyces griseus 45H, a producer of the extracellular autoregulator protein factor C, is a member of the species Streptomyces albidoflavus. Int. J. Syst. Evol. Microbiol. 58, 1029-1031
13. Birkó, Z., Sümegi, A., Vinnai, A., van Wezel, G., Szeszák, F., Vitális, S., Szabó, P. T., Kele, Z., Janáky, T., and Biró, S. (1999) Characterization of the gene for factor C, an extracellular signal protein involved in morphological differentiation of Streptomyces griseus. Microbiology 145, 2245-2253
14. Birkó, Z., Bialek, S., Buzás, K., Szájli, E., Traag, B. A., Medzihradszky, K. F., Rigali, S., Vijgenboom, E., Penyige, A., Kele, Z., van Wezel, G. P., and Biró, S. (2007) The secreted signaling protein factor C triggers the A-factor response regulon in Streptomyces griseus: overlapping signaling routes. Mol. Cell. Proteomics 6, 1248-1256
15. Szeszák, F., Vitális, S., Tóth, F., Valu, G., Fachet, J., and Szabó, G. (1990) Detection and determination of factor C - a regulatory protein - in Streptomyces strains by antiserum and monoclonal antibody. Arch. Microbiol. 154, 82-84
16. Biró, S., Birkó, Z., and van Wezel, G. P. (2000) Transcriptional and functional analysis of the gene for factor C, an extracellular signal protein involved in cytodifferentiation of Streptomyces griseus. Antonie van Leeuwenhoek 78, 277-285 (Pubitemid 32401249)
17. Ohnishi, Y., Ishikawa, J., Hara, H., Suzuki, H., Ikenoya, M., Ikeda, H., Yamashita, A., Hattori, M., and Horinouchi S. (2008) The genome sequence of the streptomycin-producing microorganism Streptomyces griseus IFO 13350. J. Bacteriol. 190, 4050-4060 (Pubitemid 351732884)
18. Kieser, T., Bibb, M. J., Buttner, M. J., Chater, K. F., and Hopwood, D. A. (2000) Practical Streptomyces Genetics, p. 408, John Innes Foundation, Norwich, UK
19. Candiano, G., Bruschi, M., Musante, L., Santucci, L., Ghiggeri, G. M., Carnemolla, B., Orecchia, P., Zardi, L., and Righetti, P. G. (2004) Blue silver: a very sensitive colloidal Coornassie G-250 staining for proteome analysis. Electrophoresis 25, 1327-1333 (Pubitemid 38801651)
20. Haebel, S., Albrecht, T., Sparbier, K., Walden, P., Körner, R., and Steup, M. (1998) Electrophoresis-related protein modification: alkylation of carboxy residues revealed by mass spectrometry. Electrophoresis 19, 679-686 (Pubitemid 28236666)
21. Noens, E. E., Mersinias, V., Willemse, J., Traag, B. A., Laing, E., Chater, K. F., Smith, C. P., Koerten, H. K., and van Wezel, G. P. (2007) Loss of the controlled localization of growth stage-specific cell-wall synthesis pleiotropically affects developmental gene expression in an ssgA mutant of Streptomyces coelicolor. Mol Microbiol. 64, 1244-1259 (Pubitemid 46849015)
22. Rigali, S., Titgemeyer, F., Barends, S., Mulder, S., Thomae, A. W., Hopwood, D. A., and van Wezel, G. P. (2008) Feast or famine: the global regulator DasR links nutrient stress to antibiotic production by Streptomyces. EMBO Rep. 9, 670-675
23. González-Pastor, J. E., Hobbs, E. C., and Losick, R. (2003) Cannibalism by sporulating bacteria. Science 301, 510-513
24. Henderson, I. R., Cappello, R., and Nataro, J. P. (2000) Autotransporter proteins, evolution and redefining protein secretion: response. Trends Microbiol. 8, 534-535
25. Bertram, R., Schlicht, M., Mahr, K., Nothaft, H., Saier, M. H., Jr., and Titgemeyer, F. (2004) In silico and transcriptional analysis of carbohydrate uptake systems of Streptomyces coelicolor A3(2). J. Bacteriol. 186, 1362-1373
26. van Wezel, G. P., White, J., Young, P., Postma, P. W., and Bibb, M. J. (1997) Substrate induction and glucose repression of maltose utilization. Mol. Microbiol. 23, 537-549
27. van Wezel, G. P., White, J., Bibb, M. J., and Postma, P. W. (1997) The malEFG gene cluster of Streptomyces coelicolor A3(2): characterization, disruption and transcriptional analysis. Mol. Gen. Genet. 254, 604-608
28. H-regulated promoter. Gene 217, 31-40 (Pubitemid 28427305)
29. Méndez, C., Braña, A. F., Manzanal, M. B., and Hardisson, C. (1985) Role of substrate mycelium in colony development in Streptomyces. Can. J. Microbiol. 31, 446-450
30. Miguélez, E. M., Hardisson, C., and Manzanal, M. B. (1999) Hyphal death during colony development in Streptomyces antibioticus: morphological evidence for the existence of a process of cell deletion in a multicellular prokaryote. J. Cell Biol. 145, 515-525 (Pubitemid 29215716)
31. Hirano, S., Kato, J. Y., Ohnishi, Y., and Horinouchi, S. (2006) Control of the Streptomyces subtilisin inhibitor gene by AdpA in the A-factor regulatory cascade in Streptomyces griseus. J. Bacteriol. 188, 6207-6216 (Pubitemid 44448562)
32. van der Heide, T., and Poolman, B. (2002) ABC transporters: one, two or four extracytoplasmic substrate-binding sites? EMBO Rep. 3, 938-943
33. Sugawara, K., Dohmae, N., Kasai, K., Saido-Sakanaka, H., Okamoto, S., Takio, K., and Ochi, K. (2002) Isolation and identification of novel ADP-ribosylated proteins from Streptomyces coelicolor A3(2). Biosci. Biotechnol. Biochem. 66, 2292-2296
34. Colson, S., van Wezel, G. P., Craig, M., Noens, E. E., Nothaft, H., Mommaas, A. M., Titgemeyer, F., Joris, B., and Rigali, S. (2008) The chitobiose-binding protein, DasA, acts as a link between chitin utilization and morphogenesis in Streptomyces coelicolor. Microbiology 154, 373-382
35. Saito, A., and Schrempf, H. (2004) Mutational analysis of the binding affinity and transport affinity for N-acetylglucosamine of the novel ABC transporter Ngc in the chitin-degrader Streptomyces olivaceoviridis. Mol. Genet. Genomics 271, 545-553
36. Nothaft, H., Dresel, D., Willimek, A., Mahr, K., Niederweis, M., and Titgemeyer, F. (2003) The phosphotransferase system of Streptomyces coelicolor is biased for N-acetylglucosamine metabolism. J. Bacteriol. 185, 7019-7023
37. Kamionka, A., Parche, S., Nothaft, H., Siepelmeyer, J., Jahreis, K., and Titgemeyer, F. (2002) The phosphotransferase system of Streptomyces coelicolor. Eur. J. Biochem. 269, 2143-2150
38. Kim, D. W., Chater, K. F., Lee, K. J., and Hesketh, A. (2005) Effects of growth phase and the developmentally significant bldA-specified tRNA on the membrane-associated proteome of Streptomyces coelicolor. Microbiology 151, 2707-2720
39. Saito, A., Shinya, T., Miyamoto, K., Yokoyama, T., Kaku, H., Minami, E., Shibuya, N., Tsujibo, H., Nagata, Y., Ando, A., Fujii, T., and Miyashita, K. (2007) The dasABC gene cluster, adjacent to dasR, encodes a novel ABC transporter for the uptake of N,N′-diacetylchitobiose in Streptomyces coelicolor A3(2). Appl. Environ. Microbiol. 73, 3000-3008
40. Seo, J. W., Ohnishi, Y., Hirata, A., and Horinouchi, S. (2002) ATP-binding cassette transport system involved in regulation of morphological differentiation in response to glucose in Streptomyces griseus. J. Bacteriol. 184, 91-103 (Pubitemid 34003288)
41. Ohnishi, Y., Seo, J. W., and Horinouchi, S. (2002) Deprogrammed sporulation in Streptomyces. FEMS Microbiol. Lett. 216, 1-7
42. Nodwell, J. R., McGovern, K., and Losick, R. (1996) An oligopeptide permease responsible for the import of an extracellular signal governing aerial mycelium formation in Streptomyces coelicolor. Mol. Microbiol. 22, 881-893
43. Hillerich, B., and Westpheling, J. (2006) A new GntR family transcriptional regulator in Streptomyces coelicolor is required for morphogenesis and antibiotic production and controls transcription of an ABC transporter in response to carbon source. J. Bacteriol. 188, 7477-7487 (Pubitemid 44646247)
44. Folcher, M., Gaillard, H., Nguyen, L. T., Nguyen, K. T., Lacroix, P., Bamas-Jacques, N., Rinkel, M., and Thompson, C. J. (2001) Pleiotropic functions of a Streptomyces pristinaespiralis autoregulator receptor in development, antibiotic biosynthesis, and expression of a superoxide dismutase. J. Biol. Chem. 276, 44297-44306
45. Cho, Y. H., Lee, E. J., and Roe, J. H. (2000) A developmentally regulated catalase required for proper differentiation and osmoprotection of Streptomyces coelicolor. Mol. Microbiol. 35, 150-160
46. Kim, F. J., Kim, H. P., Hah, Y. C., and Roe, J. H. (1996) Differential expression of superoxide dismutases containing Ni and Fe/Zn in Streptomyces coelicolor. Eur. J. Biochem. 241, 178-185