Transcriptomic studies of phosphate control of primary and secondary metabolism in Streptomyces coelicolor

Applied Microbiology and Biotechnology

Volumn 95, Issue 1, 2012, Pages 61-75

  Martín, Juan F ^a   Santos Beneit, Fernando ^b   Rodríguez García, Antonio ^a,b   Sola Landa, Alberto ^b   Smith, Margaret C M ^c   Ellingsen, Trond E ^d   Nieselt, Kay ^e   Burroughs, Nigel J ^f   Wellington, Ellizabeth M H ^f  

^a UNIVERSITY OF LEÓN   (Spain)

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

^c UNIVERSITY OF ABERDEEN   (United Kingdom)

^d SINTEF MATERIALS AND CHEMISTRY   (Norway)

^e UNIVERSITY OF TÜBINGEN   (Germany)

^f UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

Expression profiles; PhoP mediated regulation; Phosphate control; Secondary metabolite biosynthesis; Streptomyces genetics; Transcriptomic studies

Indexed keywords

EXPRESSION PROFILE; PHOP-MEDIATED REGULATION; SECONDARY METABOLITES; STREPTOMYCES GENETICS; TRANSCRIPTOMIC STUDIES;

BACTERIA; BIOCHEMISTRY; BIOSYNTHESIS; GENE EXPRESSION; METABOLISM; METABOLITES; PHOSPHORYLATION; POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

GENE EXPRESSION REGULATION;

ADENOSINE TRIPHOSPHATE; ANTIBIOTIC AGENT; FUNGAL PROTEIN; PHOSPHATE; PROTEIN AFSR; PROTEIN PHOR PHOP; PROTEIN PHOU; UNCLASSIFIED DRUG;

ANTIBIOTICS; BACTERIUM; GENE EXPRESSION; METABOLISM; METABOLITE; MOLECULAR ANALYSIS; MUTATION; PHOSPHATE; PROTEIN;

ACTINOBACTERIA; AFSS GENE; BINDING SITE; DNA FOOTPRINTING; FUNGAL GENE; FUNGAL STRAIN; GEL MOBILITY SHIFT ASSAY; GENE ACTIVATION; GENE EXPRESSION; GENE IDENTIFICATION; GENE REPRESSION; IN VIVO STUDY; METABOLIC REGULATION; METABOLITE; MUTANT; NONHUMAN; OPERON; PHOA GENE; PHOC GENE; PHOD GENE; PHOR GENE; PHOR PHOP GENE; PHOSPHATE METABOLISM; PITH2; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEOMICS; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; REPORTER GENE; RPOZ GENE; SHORT SURVEY; SIGNAL TRANSDUCTION; STREPTOMYCES COELICOLOR; TRANSCRIPTOMICS; UPREGULATION;

BACTERIAL PROTEINS; BASE SEQUENCE; BINDING SITES; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR SEQUENCE DATA; PHOSPHATES; STREPTOMYCES COELICOLOR; TRANSCRIPTOME;

ACTINOBACTERIA; STREPTOMYCES; STREPTOMYCES COELICOLOR;

EID: 84862001447     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-012-4129-6     Document Type: Short Survey

References (77)

1. Ahlert J, Distler J, Mansouri K, Piepersberg W (1997) Identification of stsC, the gene encoding the L-glutamine:scyllo-inosose aminotransferase from streptomycin-producing streptomycetes. Arch Microbiol 168:102-113 (Pubitemid 27359839)
2. Allen MP, Zumbrennen KB, McCleary WR (2001) Genetic evidence that the alpha5 helix of the receiver domain of PhoB is involved in interdomain interactions. J Bacteriol 183:2204-2211 (Pubitemid 32240388)
3. Apel AK, Sola-Landa A, Rodríguez-García A, Martín 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 (Pubitemid 47629556)
4. Bibb MJ (2005) Regulation of secondary metabolism in streptomycetes. Curr Opin Microbiol 8:208-215
5. Birck C, Chen Y, Hulett FM, Samama JP (2003) The crystal structure of the phosphorylation domain in PhoP reveals a functional tandem association mediated by an asymmetric interface. J Bacteriol 185:254-261 (Pubitemid 36008843)
6. Blanco AG, Solà M, Gomis-Rüth FX, Coll M (2002) Tandem DNA recognition by PhoB, a two-component signal transduction transcriptional activator. Structure 10:701-713
7. Browning DF, Busby SJ (2004) The regulation of bacterial transcription initiation. Nat Rev Microbiol 2:57-65 (Pubitemid 39490048)
8. Brzoska P, Boos W (1989) The ugp-encoded glycerophosphoryldiester phosphodiesterase, a transport-related enzyme of Escherichia coli. FEMS Microbiol Rev 5:115-124 (Pubitemid 19156380)
9. Chen Y, Birck C, Samama JP, Hulett FM (2003) Residue R113 is essential for PhoP dimerization and function: a residue buried in the asymmetric PhoP dimer interface determined in the PhoPN three-dimensional crystal structure. J Bacteriol 185:262-273 (Pubitemid 36008844)
10. Cheng YR, Hauck L, Demain AL (1995) Phosphate, ammonium, magnesium and iron nutrition of Streptomyces hygroscopicus with respect to rapamycin biosynthesis. J Ind Microbiol 14:424-427
11. Cheung J, Hendrickson WA (2010) Sensor domains of two-component regulatory systems. Curr Opin Microbiol 13:116-123
12. Chouayekh H, Virolle M-J (2002) The polyphosphate kinase plays a negative role in the control of antibiotic production in Streptomyces lividans. Mol Microbiol 43:919-930 (Pubitemid 34415716)
13. Dekeva ML, Titus JA, Strohl WR (1985) Nutrient effects on anthracycline production by Streptomyces peucetius in a defined medium. Can J Microbiol 31:287-294
14. Díaz M, Esteban A, Fernández-Abalos JM, Santamaría RI (2005) The high-affinity phosphate-binding protein PstS is accumulatedunder high fructose concentrations and mutation of the corresponding gene affects differentiation in Streptomyces lividans. Microbiology 151:2583-2592
15. Doull JL, Vining LC (1990) Nutritional control of actinorhodin production by Streptomyces coelicolor A3(2): suppressive effects of nitrogen and phosphate. Appl Microbiol Biotechnol 32:449-454 (Pubitemid 20095299)
16. Eder S, Liu W, Hulett FM (1999) Mutational analysis of the phoD promoter in Bacillus subtilis: implications for PhoP binding and promoter activation of Pho regulon promoters. J Bacteriol 181:2017-2025 (Pubitemid 29164953)
17. Ellison DW, McCleary WR (2000) The unphosphorylated receiver domain of PhoB silences the activity of its output domain. J Bacteriol 182:6592-6597 (Pubitemid 32249238)
18. Fabret C, Feher VA, Hoch JA (1999) Two-component signal transduction in Bacillus subtilis: how one organism sees its world. J Bacteriol 181:1975-1983 (Pubitemid 29164948)
19. Fink D, Weißschuh N, Reuther J, Wohlleben W, Engels A (2002) Two transcriptional regulators GlnR and GlnRII are involved in regulation of nitrogen metabolism in Streptomyces coelicolor A3(2). Mol Microbiol 46:331-347 (Pubitemid 35340947)
20. Galperin MY (2010) Diversity of structure and function of response regulator output domains. Curr Opin Microbiol 13:150-159
21. Ghorbel S, Kormanec J, Artus A, Virolle MJ (2006a) 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 (Pubitemid 43100555)
22. Ghorbel S, Smirnov A, Chouayekh H, Sperandio B, Esnault C, Kormanec J, Virolle M-J (2006b) Regulation of ppk expression and in vivo function of Ppk in Streptomyces lividans TK24. J Bacteriol 188:6269-6276 (Pubitemid 44448569)
23. Hobbs G, Frazer CM, Gardner DCJ, Flett F, Oliver SG (1990) Pigmented antibiotic production by Streptomyces coelicolorA3(2): kinetics and the influence of nutrients. J Gen Microbiol 136:2291-2296 (Pubitemid 20378735)
24. Hoi LT, Voigt B, Jürgen B, Ehrenreich A, Gottschalk G, Evers S, Feesche J, Maurer K-H, Hecker M, Schweder T (2006) The phosphate-starvation response of Bacillus licheniformis. Proteomics 6:3582-3601 (Pubitemid 44000187)
25. 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 (Pubitemid 39317782)
26. Krol E, Becker A (2004) Global transcriptional analysis of the phosphate starvation response in Sinorhizobium meliloti strains 1021 and 2011. Mol Genet Genomics 272:1-17 (Pubitemid 39222581)
27. Liras P, Asturias JA, Martín JF (1990) Phosphate control sequences involved in transcriptional regulation of antibiotic biosynthesis. Trends Biotechnol 8:184-189
28. Liu W, Eder S, Hulett FM (1998) Analysis of Bacillus subtilis tagAB and tagDEF expression during phosphate starvation identifies a repressor role for PhoP-P. J Bacteriol 180:753-758 (Pubitemid 28100565)
29. Lounes A, Lebrihi A, Benslimane C, Lefebvre G, Germain P (1996) Regulation of spiramycin synthesis in Streptomyces ambofaciens: effects of glucose and inorganic phosphate. Appl Microbiol Biotechnol 45:204-211 (Pubitemid 26114757)
30. Makarewicz O, Dubrac S, Msadek T, Borriss R (2006) Dual role of the PhoP P response regulator: Bacillus amyloliquefaciens FZB45 phytase gene transcription is directed by positive and negative interactions with the phyC promoter. J Bacteriol 188:6953-6965 (Pubitemid 44497908)
31. Manteca A, Ye J, Sánchez J, Jensen ON (2011) Phosphoproteome analysis of Streptomyces development reveals extensive protein phosphorylation accompanying bacterial differentiation. J Proteome Res 10:5481-5492
32. Martín JF (1989) Molecular mechanism for the control by phosphate of the biosynthesis of antibiotic and secondary metabolites. In: Shapiro S (ed) Regulation of secondary metabolism in actinomycetes. CRC, Boca Raton, pp 213-236
33. Martín JF (2004) Phosphate control of the biosynthesis of antibiotics and other secondary metabolites is mediated by the PhoR-PhoP system: an unfinished story. J Bacteriol 186:5197-5201
34. Martín JF, Demain A (1980) Control of antibiotic biosynthesis. Microbiol Rev 44:230-251 (Pubitemid 11128309)
35. Martín JF, Marcos AT, Martín A, Asturias JA, Liras P (1994) Phosphate control of antibiotic biosynthesis at the transcriptional level. In: Torriani-Gorini A, Yagil E, Silver S (eds) Phosphate in microorganisms. ASM, Washington, pp 140-147
36. Martín JF, Gutiérrez S, Aparicio JF (2000) Secondary metabolites. In: Lederberg J (ed) Encyclopedia of microbiology, vol 4, 2nd edn. Academic, San Diego, pp 213-237
37. Martín JF, Sola-Landa A, Santos-Beneit F, Rodríguez- García A (2011) Network mechanisms of phosphate control of primary and secondary metabolism. In: Dyson P (ed) Streptomyces: molecular biology and biotechnology. Caister Academic, Norwich, pp 137-149
38. Martín JF, Sola-Landa A, Rodríguez-García A (2012) Two-component systems in Streptomyces. In: Gross R, Beier D (eds) Twocomponent systems in bacteria. Caister Academic, Würzburg, pp 315-331
39. Masuma R, Tanaka Y, Tanaka H, Omura S (1986) Production of nanaomycin and other antibiotics by phosphate-depressed fermentation using phosphate-trapping agents. J Antibiot (Tokyo) 39:1557-1564 (Pubitemid 17181850)
40. Mendes MV, Tunca S, Antón N, Recio E, Sola-Landa A, Aparicio JF, Martín JF (2007) The two-component phoR-phoP system of Streptomyces natalensis: inactivation or deletion of phoP reduces the negative phosphate regulation of pimaricin biosynthesis. Metabol Engineer 9:217-227 (Pubitemid 46350704)
41. Nieselt K, Battke F, Herbig A, Bruheim P, Wentzel A, Jakobsen OM, Sletta H, Alam MT, Merlo ME, Moore J, Omara WA, Morrissey ER, Juarez-Hermosillo MA, Rodríguez-García A, Nentwich M, Thomas L, Iqbal M, Legaie R, Gaze WH, Challis GL, Jansen RC, Dijkhuizen L, Rand DA, Wild DL, Bonin M, Reuther J, Wohlleben W, Smith MC, Burroughs NJ, Martín JF, Hodgson DA, Takano E, Breitling R, Ellingsen TE, Wellington EM (2010) The dynamic architecture of the metabolic switch in Streptomyces coelicolor. BMC Genomics 11:10-19
42. Perron-Savard P, De Crescenzo G, Le Moual H (2005) Dimerization and DNA binding of the Salmonella enterica PhoP response regulator are phosphorylation independent. Microbiology 151:3979-3987 (Pubitemid 41829977)
43. Prágai Z, Allenby NE, O'Connor N, Dubrac S, Rapoport G, Msadek T, Harwood CR (2004) Transcriptional regulation of the phoPR operon in Bacillus subtilis. J Bacteriol 186:1182-1190 (Pubitemid 38209479)
44. Pullan ST, Chandra G, Bibb MJ, Merrick M (2011) Genome-wide analysis of the role of GlnR in Streptomyces venezuelae provides new insights into global nitrogen regulation in actinomycetes. BMC Genomics 12:175-189
45. Puri-Taneja A, Paul S, Chen Y, Hulett FM (2006) CcpA causes repression of the phoPR promoter through a novel transcription start site, PA6. J Bacteriol 188:1266-1278 (Pubitemid 43228659)
46. Quiquampoix H, Mousain D (2005) Enzymatic hydrolysis of organic phosphorus. In: Turner BL, Frossard E, Baldwin DS (eds) Organic phosphorus in the environment. CABI, Cambridge, pp 89-112
47. Reuther J, Wohlleben W (2007) Nitrogen metabolism in Streptomyces coelicolor: transcriptional and post-translational regulation. J Mol Microbiol Biotechnol 12:139-146 (Pubitemid 46011135)
48. Rigali S, Titgemeyer F, Barends S, Mulder S, Thomae AW, Hopwood DA, van Wezel GP (2008) Feast or famine: the global regulator DasR links nutrient stress to antibiotic production by Streptomyces. EMBO Rep 9:670-675 (Pubitemid 351927688)
49. Rodríguez-García A, Barreiro C, Santos-Beneit F, Sola-Landa A, Martín JF (2007) Genome-wide transcriptomic and proteomic analysis of the primary response to phosphate limitation inStreptomyces coelicolor M145 and in a ΔphoP mutant. Proteomics 7:2410-2429
50. Rodríguez-García A, Sola-Landa A, Apel K, Santos-Beneit F, Martín 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
51. Romero J, Liras P, Martín JF (1984) Dissociation of cephamycin and clavulanic acid biosynthesis in Streptomyces clavuligerus. Appl Microbiol Biotechnol 20:318-325 (Pubitemid 15224270)
52. Saito N, Xu J, Hosaka T, Okamoto S, Aoki H, Bibb MJ, 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)
53. Santos-Beneit F, Rodríguez-García A, Franco- Domínguez E, Martín JF (2008) Phosphate-dependent regulation of the low- and highaffinity transport systems in the model actinomycete Streptomyces coelicolor. Microbiology 154:2356-2370
54. Santos-Beneit F, Rodríguez-García A, Sola-Landa A, Martín JF (2009a) 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
55. Santos-Beneit F, Rodríguez-García A, Apel AK, Martín JF (2009b) Phosphate and carbon source regulation of two PhoP-dependent glycerophosphodiester phosphodiesterase genes of Streptomyces coelicolor. Microbiology 155:1800-1811
56. Santos-Beneit F, Rodríguez-García A, Martín JF (2011a) Complex transcriptional control of the antibiotic regulator afsS in Streptomyces: PhoP and AfsR are overlapping, competitive activators. J Bacteriol 193:2242-2251
57. Santos-Beneit F, Barriuso-Iglesias M, Fernández-Martínez LT, Martínez-Castro M, Sola-Landa A, Rodríguez-García A, Martín JF (2011b) 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 77:7586-7594
58. Schaaf S, Bott M (2007) Target genes and DNA-binding sites of the response regulator PhoR from Corynebacterium glutamicum. J Bacteriol 189:5002-5011 (Pubitemid 47076045)
59. Schneider TD (1997) Information content of individual genetic sequences. J Theor Biol 189:427-441
60. Sinha A, Gupta S, Bhutani S, Pathak A, Sarkar D (2008) PhoP-PhoP interaction at adjacent PhoP binding sites is influenced by protein phosphorylation. J Bacteriol 190:1317-1328 (Pubitemid 351215013)
61. Sola-Landa A, Moura RS, Martín 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 (Pubitemid 36576943)
62. Sola-Landa A, Rodríguez-García A, Franco-Domínguez E, Martín JF (2005) Binding of PhoP to promoters of phosphate-regulated genes in Streptomyces coelicolor: identification of PHO boxes. Mol Microbiol 56:1373-1385 (Pubitemid 40756017)
63. Sola-Landa A, Rodríguez-García A, Apel AK, Martín 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 (Pubitemid 351330950)
64. Stieglitz KA, Seaton BA, Roberts MF (2001) Binding of proteolytically processed phospholipase D from Streptomyces chromofuscus to phosphatidylcholine membranes facilitates vesicle aggregation and fusion. Biochemistry 40:13954-13963 (Pubitemid 33078865)
65. Suzuki S, Ferjani A, Suzuki I, Murata N (2004) The SphS-SphR two component system is the exclusive sensor for the induction of gene expression in response to phosphate limitation in Synechocystis. J Biol Chem 279:13234-13240 (Pubitemid 38445902)
66. Tamegai H, Eguchi T, Kakinuma K (2002) First identification of Streptomyces genes involved in the biosynthesis of 2-deoxystreptaminecontaining aminoglycoside antibiotics - genetic and evolutionary analysis of L-glutamine:2-deoxy-scyllo-inosose aminotransferase genes. J Antibiot (Tokyo) 55:1016-1018 (Pubitemid 35423168)
67. Thomas L, Hodgson DA, Wentzel A, Nieselt K, Ellingsen TE, Moore J, Morrissey ER, Legaie R, The STREAM Consortium, Rodríguez-García A, Martín JF, Burroughs NJ, Wellington EM, SmithMC (2012)Metabolic switches and adaptations deduced from the proteomes of Streptomyces coelicolor wild type and phoP mutant grown in batch culture. Mol Cell Proteomics 11:M111.013797
68. Tiffert Y, Supra P,Wurm R,Wohlleben W,Wagner R, 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)
69. Uesugi Y, Hatanaka T (2009) Phospholipase D mechanism using Streptomyces PLD. Biochim Biophys Acta 1791:962-969
70. VanBogelen RA, Olson ER, Wanner BL, Neidhardt FC (1996) Global analysis of proteins synthesized during phosphorus restriction in Escherichia coli. J Bacteriol 178:4344-4366 (Pubitemid 26262219)
71. Vining LC (1992) Secondary metabolism, inventive evolution and biochemical diversity-a review. Gene 115:135-140
72. Wanner BL (1996) Phosphorus assimilation and control of the phosphate regulon. In: Neidhardt FC, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (eds) Escherichia coli and Salmonella, 2nd edn. American Society for Microbiology, Washington, pp 1357-1381
73. Wösten MM, Parker CT, van Mourik A, Guilhabert MR, van Dijk L, van Putten JP (2006) The Campylobacter jejuni PhosS/PhosR operon represents a non-classical phosphate-sensitive twocomponent system. Mol Microbiol 62:278-291 (Pubitemid 44386566)
74. Wray LV, Fisher SH (1993) The Streptomyces coelicolor glnR gene encodes a protein similar to other bacterial response regulators. Gene 130:145-150
75. Yamane T, Okamura H, Ikeguchi M, Nishimura Y, Kidera A (2008) Water-mediated interactions between DNA and PhoB DNAbinding/ transactivation domain: NMR-restrained molecular dynamics in explicit water environment. Proteins 71:1970-1983 (Pubitemid 351732949)
76. 2+-dependent phospholipase D. Protein Sci 11:2958-2968
77. Yuan ZC, Zaheer R, Morton R, Finan TM (2006) Genome prediction of PhoB regulated promoters in Sinorhizobium meliloti and twelve proteobacteria. Nucleic Acids Res 34:2686-2697 (Pubitemid 43985631)