Is PhoR-PhoP partner fidelity strict? PhoR is required for the activation of the pho regulon in Streptomyces coelicolor

Molecular Genetics and Genomics

Volumn 287, Issue 7, 2012, Pages 565-573

  Fernández Martínez, Lorena T ^a,b   Santos Beneit, Fernando ^a   Martín, Juan F ^a,c  

^a Institute of Biotechnology INBIOTEC Parque Científico de León   (Spain)

^b NORWICH RESEARCH PARK   (United Kingdom)

^c UNIVERSITY OF LEÓN   (Spain)

Author keywords

Phosphate; Sensor kinase; Streptomyces; Two component regulatory systems

Indexed keywords

PHOP PROTEIN; PROTEIN HISTIDINE KINASE; PROTEIN PHOR; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM MUTANT; CONTROLLED STUDY; GENE EXPRESSION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REGULON; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STREPTOMYCES COELICOLOR; WILD TYPE;

ANTHRAQUINONES; BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MUTATION; OPERON; PHOSPHATES; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTEIN KINASES; REGULON; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STREPTOMYCES COELICOLOR; TIME FACTORS; TRANSCRIPTION FACTORS;

STREPTOMYCES; STREPTOMYCES COELICOLOR;

EID: 84864826787     PISSN: 16174615     EISSN: 16174623     Source Type: Journal    
DOI: 10.1007/s00438-012-0698-4     Document Type: Article

References (33)

1. Amemura M, Makino K, Shinagawa H, Nakata A (1990) Cross talk to the phosphate regulon of Escherichia coli by PhoM protein: PhoM is a histidine protein kinase and catalyzes phosphorylation of PhoB and PhoM-open reading frame 2. J Bacteriol 172:6300-6307
2. Apel AK, Sola-Landa A, Rodriguez-Garcia A, Martin JF (2007) Phosphate control of phoA, phoC and phoD gene expression in Streptomyces coelicolor reveals significant differences in binding of PhoP to their promoter regions. Microbiology 153:3527-3537
3. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97:6640-6645
4. Fedoryshyn M, Welle E, Bechthold A, Luzhetskyy A (2008) Functional expression of the Cre recombinase in actinomycetes. Appl Microbiol Biotechnol 78:1065-1070
5. Fernández-Martínez LT, Del Sol R, Evans MC, Fielding S, Herron PR, Chandra G, Dyson PJ (2011) A transposon insertion singlegene knockout library and new ordered cosmid library for the model organism Streptomyces coelicolor A3 (2). Antonie Van Leeuwenhoek 99:515-522
6. Fisher SL, Jiang W, Wanner BL, Walsh CT (1995) Cross-talk between the histidine protein kinase VanS and the response regulator PhoB. Characterization and identification of a VanS domain that inhibits activation of PhoB. J Biol Chem 270:23143-23149
7. Flett F, Mersinias V, Smith CP (1997) High efficiency intergeneric conjugal transfer of plasmid DNA from Escherichia coli to methyl DNA-restricting streptomycetes. FEMS Microbiol Lett 155:223-229
8. Ghorbel S, Kormanec J, Artus A, Virolle MJ (2006) Transcriptional studies and regulatory interactions between the phoR-phoP operon and the phoU, mtpA, and ppk genes of Streptomyces lividans TK24. J Bacteriol 188:677-686
9. Gust B, Challis GL, Fowler K, Kieser T, Chater KF (2003) PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc Natl Acad Sci USA 100:1541-1546
10. Hakenbeck R, Stock JB (1996) Analysis of two-component signal transduction systems involved in transcriptional regulation. Methods Enzymol 273:281-300
11. Hanahan D (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166:557-580
12. Hutchings MI, Hoskisson PA, Chandra G, Buttner MJ (2004) Sensing and responding to diverse extracellular signals? Analysis of the sensor kinases and response regulators of Streptomyces coelicolor A3 (2). Microbiology 150:2795-2806
13. Khodakaramian G, Lissenden S, Gust B, Moir L, Hoskisson PA, Chater KF, Smith MC (2006) Expression of Cre recombinase during transient phage infection permits efficient marker removal in Streptomyces. Nucleic Acids Res 34:e20
14. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA (2000) Practical Streptomyces genetics. The John Innes Foundation, Norwich
15. Martin JF, Sola-Landa A, Santos-Beneit F, Fernández- Martínez LT, Prieto C, Rodriguez-Garcia A (2011) Cross-talk of global nutritional regulators in the control of primary and secondary metabolism in Streptomyces. Microb Biotechnol 4:165-174
16. McCleary WR, Stock JB (1994) Acetyl phosphate and the activation of two-component response regulators. J Biol Chem 269:31567-31572
17. Mendes MV, Tunca S, Anton N, Recio E, Sola-Landa A, Aparicio JF, Martin JF (2007) The two-component phoR-phoP system of Streptomyces natalensis: inactivation or deletion of phoP reduces the negative phosphate regulation of pimaricin biosynthesis. Metab Eng 9:217-227
18. Paul S, Birkey S, Liu W, Hulett FM (2004) Autoinduction of Bacillus subtilis phoPR operon transcription results from enhanced transcription from EsigmaA-and EsigmaE-responsive promoters by phosphorylated PhoP. J Bacteriol 186:4262-4275
19. Rodriguez-Garcia A, Barreiro C, Santos-Beneit F, Sola-Landa A, Martin JF (2007) Genome-wide transcriptomic and proteomic analysis of the primary response to phosphate limitation in Streptomyces coelicolor M145 and in a DeltaphoP mutant. Proteomics 7:2410-2429
20. Rodriguez-Garcia A, Sola-Landa A, Apel K, Santos-Beneit F, Martin JF (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
21. Sambrook JFE, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor, New York
22. Santos-Beneit F, Rodriguez-Garcia A, Franco-Dominguez E, Martin JF (2008) Phosphate-dependent regulation of the low-and highaffinity transport systems in the model actinomycete Streptomyces coelicolor. Microbiology 154:2356-2370
23. Santos-Beneit F, Rodriguez-Garcia A, Apel AK, Martin JF (2009a) Phosphate and carbon source regulation of two PhoP-dependent glycerophosphodiester phosphodiesterase genes of Streptomyces coelicolor. Microbiology 155:1800-1811
24. Santos-Beneit F, Rodriguez-Garcia A, Sola-Landa A, Martin JF (2009b) 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
25. Santos-Beneit F, Barriuso-Iglesias M, Fernández-Martínez LT, Martínez-Castro M, Sola-Landa A, Rodríguez-Garćia A, Martín JF (2011) The RNA polymerase omega factor RpoZ is regulated by PhoP and has an important role in antibiotic biosynthesis and morphological differentiation in Streptomyces coelicolor. Appl Environ Microbiol 77(21):7586-7594
26. Sola-Landa A, Moura RS, Martin JF (2003) The two-component PhoR-PhoP system controls both primary metabolism and secondary metabolite biosynthesis in Streptomyces lividans. Proc Natl Acad Sci USA 100:6133-6138
27. Sola-Landa A, Rodriguez-Garcia A, Franco-Dominguez E, Martin JF (2005) Binding of PhoP to promoters of phosphate-regulated genes in Streptomyces coelicolor: identification of PHO boxes. Mol Microbiol 56:1373-1385
28. Sola-Landa A, Rodriguez-Garcia A, Apel AK, Martin JF (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
29. Sun G, Birkey SM, Hulett FM (1996) Three two-component signaltransduction systems interact for Pho regulation in Bacillus subtilis. Mol Microbiol 19:941-948
30. Szurmant H, Hoch JA (2010) Interaction fidelity in two-component signaling. Curr Opin Microbiol 13:190-197
31. Tunca S, Barreiro C, Sola-Landa A, Coque JJ, Martin JF (2007) Transcriptional regulation of the desferrioxamine gene cluster of Streptomyces coelicolor is mediated by binding of DmdR1 to an iron box in the promoter of the desA gene. FEBS J 274:1110-1122
32. Yanisch-Perron C, Vieira J, Messing J (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103-119
33. Zhou L, Gregori G, Blackman JM, Robinson JP, Wanner BL (2005) Stochastic activation of the response regulator PhoB by noncognate histidine kinases. J Integr Bioinform 2(1):11