Transcriptional and preliminary functional analysis of the six genes located in divergence of phoR/phoP in Streptomyces lividans

Applied Microbiology and Biotechnology

Volumn 95, Issue 6, 2012, Pages 1553-1566

  Darbon, Emmanuelle ^a   Martel, Cécile ^a   Nowacka, Aleksandra ^a   Pegot, Sylvine ^a   Moreau, Patrice L ^b   Virolle, Marie Joëlle ^a  

^a UNIVERSITÉ PARIS SACLAY   (France)

^b AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

Oxidative stress; Pho regulon; Pi limitation; Streptomyces

Indexed keywords

CARBON AND NITROGEN; ENCODED PROTEINS; METALLO-PROTEINS; PHO REGULON; STREPTOMYCES; STREPTOMYCES LIVIDANS; TRANSCRIPTIONAL ANALYSIS; TWO COMPONENT SYSTEMS;

CONTRAST MEDIA; OXIDATIVE STRESS; PROTEINS;

GENE EXPRESSION;

BACTERIAL PROTEIN; PHOP PROTEIN; PROTEIN PHOR; PROTEIN PHOU; UNCLASSIFIED DRUG; PHOP PROTEIN, BACTERIA; PHOR PROTEIN, BACTERIA;

GENE EXPRESSION; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; OXIDATION; PROTEIN;

ARTICLE; BACTERIAL STRAIN; BACTERIUM CULTURE; GENETIC TRANSCRIPTION; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; POLYMERASE CHAIN REACTION; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULON; STREPTOMYCES LIVIDANS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS;

STREPTOMYCES; STREPTOMYCES LIVIDANS;

BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR SEQUENCE DATA; OXIDATIVE STRESS; REGULON; STREPTOMYCES LIVIDANS; TRANSCRIPTION, GENETIC;

EID: 84872028735     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-012-3995-2     Document Type: Article

References (78)

1. Alix E, Blanc-Potard AB (2009) Hydrophobic peptides: novel regulators within bacterial membrane. Mol Microbiol 72:5-11
2. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389-3402
3. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373-399
4. 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
5. Baek JH, Lee SY (2006) Novel gene members in the Pho regulon of Escherichia coli. FEMS Microbiol Lett 264:104-109
6. Baltz RH (2008) Renaissance in antibacterial discovery from actinomycetes. Curr Opin Pharmacol 8:557-563
7. Bentley SD, Chater KF, Cerdeno-Tarraga AM, Challis GL, Thomson NR, James KD, Harris DE, Quail MA, Kieser H, Harper D, Bateman A, Brown S, Chandra G, Chen CW, Collins M, Cronin A, Fraser A, Goble A, Hidalgo J, Hornsby T, Howarth S, Huang CH, Kieser T, Larke L, Murphy L, Oliver K, O'Neil S, Rabbinowitsch E, Rajandream MA, Rutherford K, Rutter S, Seeger K, Saunders D, Sharp S, Squares R, Squares S, Taylor K, Warren T, Wietzorrek A, Woodward J, Barrell BG, Parkhill J, Hopwood DA (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141-147
8. Blondelet-Rouault MH, Weiser J, Lebrihi A, Branny P, Pernodet JL (1997) Antibiotic resistance gene cassettes derived from the omega interposon for use in E. coli and Streptomyces. Gene 190:315-317
9. Bogel G, Schrempf H, de Orue O, Lucana D (2009) The heme-binding protein HbpS regulates the activity of the Streptomyces reticuli iron-sensing histidine kinase SenS in a redox-dependent manner. Amino Acids 37:681-691
10. Buelow DR, Raivio TL (2010) Three (and more) component regulatory systems - auxiliary regulators of bacterial histidine kinases. Mol Microbiol 75:547-566
11. Capdevila M, Atrian S (2011) Metallothionein protein evolution: a miniassay. J Biol Inorg Chem 16:977-989
12. Challis GL (2008a) Genome mining for novel natural product discovery. J Med Chem 51:2618-2628
13. Challis GL (2008b) Mining microbial genomes for new natural products and biosynthetic pathways. Microbiology 154:1555-1569
14. Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 81:1991-1995
15. Coyle P, Philcox JC, Carey LC, Rofe AM (2002) Metallothionein: the multipurpose protein. Cell Mol Life Sci 59:627-647
16. Crepin S, Chekabab SM, Le Bihan G, Bertrand N, Dozois CM, Harel J (2011) The Pho regulon and the pathogenesis of Escherichia coli. Vet Microbiol 153:82-88
17. den Hengst CD, Buttner MJ (2008) Redox control in actinobacteria. Biochim Biophys Acta 1780:1201-1216
18. Diaz M, Esteban A, Fernandez-Abalos JM, Santamaria RI (2005) The high-affinity phosphate-binding protein PstS is accumulated under high fructose concentrations and mutation of the corresponding gene affects differentiation in Streptomyces lividans. Microbiology 151:2583-2592
19. Doumith M, Weingarten P, Wehmeier UF, Salah-Bey K, Benhamou B, Capdevila C, Michel JM, Piepersberg W, Raynal MC (2000) Analysis of genes involved in 6-deoxyhexose biosynthesis and transfer in Saccharopolyspora erythraea. Mol Gen Genet 264:477-485
20. Dwyer DJ, Kohanski MA, Collins JJ (2009) Role of reactive oxygen species in antibiotic action and resistance. Curr Opin Microbiol 12:482-489
21. Fenton HJH (1986) Oxidation of tartaric acid in the presence of iron. J Chem Soc 65:899-910
22. Flardh K, Buttner MJ (2009) Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium. Nat Rev Microbiol 7:36-49
23. 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
24. Glaser L, Loewy A (1979a) Control of teichoic acid synthesis during phosphate limitation. J Bacteriol 137:327-331
25. Glaser L, Loewy A (1979b) Regulation of teichoic acid synthesis during phosphate limitation. J Biol Chem 254:2184-2186
26. Goto Y, Li B, Claesen J, Shi Y, Bibb MJ, van der Donk WA (2010) Discovery of unique lanthionine synthetases reveals new mechanistic and evolutionary insights. PLoS Biol 8:e1000339
27. Guillemet ML, Moreau PL (2008) Fur-dependent detoxification of organic acids by rpoS mutants during prolonged incubation under aerobic, phosphate starvation conditions. J Bacteriol 190:5567-5575
28. 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
29. Hassett DJ, Imlay JA (2007) Bactericidal antibiotics and oxidative stress: a radical proposal. ACS Chem Biol 2:708-710
30. Hobbs G, Frazer CM, Gardner DCJ, Cullum JA, Oliver SG (1989) Dispersed growth of Streptomyces in liquid culture. Appl Microbiol Biotechnol 31:272-277
31. Hopwood DA, Kieser T, Wright HM, Bibb MJ (1983) Plasmids, recombination and chromosome mapping in Streptomyces lividans 66. J Gen Microbiol 129:2257-2269
32. Hsieh YJ, Wanner BL (2010) Global regulation by the seven-component Pi signaling system. Curr Opin Microbiol 13:198-203
33. Hulett FM (1996) The signal-transduction network for Pho regulation in Bacillus subtilis. Mol Microbiol 19:933-939
34. Imlay JA (2003) Pathways of oxidative damage. Annu Rev Microbiol 57:395-418
35. Karray F (2005) Etude de la biosynthèse de l'antibiotique spiramycine par Streptomyces ambofaciens. Université Paris sud 11, Orsay, France
36. Kehrer JP (2000) The Haber-Weiss reaction and mechanisms of toxicity. Toxicology 149:43-50
37. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA (2000) Practical Streptomyces Genetics. In: Foundation TJI (ed), Norwich, UK, pp. 248
38. Kosower NS, Kosower EM (1995) Diamide: an oxidant probe for thiols. Methods Enzymol 251:123-133
39. Liu J, Lou Y, Yokota H, Adams PD, Kim R, Kim SH (2005) Crystal structure of a PhoU protein homologue: a new class of metalloprotein containing multinuclear iron clusters. J Biol Chem 280:15960-15966
40. Makino K, Amemura M, Kim SK, Nakata A, Shinagawa H (1993) Role of the sigma 70 subunit of RNA polymerase in transcriptional activation by activator protein PhoB in Escherichia coli. Genes Dev 7:149-160
41. Marchler-Bauer A, Anderson JB, Cherukuri PF, DeWeese-Scott C, Geer LY, Gwadz M, He S, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Liebert CA, Liu C, Lu F, Marchler GH, Mullokandov M, Shoemaker BA, Simonyan V, Song JS, Thiessen PA, Yamashita RA, Yin JJ, Zhang D, Bryant SH (2005) CDD: a Conserved Domain Database for protein classification. Nucleic Acids Res 33:D192-D196
42. Martin 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
43. Marzan LW, Shimizu K (2011) Metabolic regulation of Escherichia coli and its phoB and phoR genes knockout mutants under phosphate and nitrogen limitations as well as at acidic condition. Microb Cell Fact 10:39
44. Moreau PL (2004) Diversion of the metabolic flux from pyruvate dehydrogenase to pyruvate oxidase decreases oxidative stress during glucose metabolism in nongrowing Escherichia coli cells incubated under aerobic, phosphate starvation conditions. J Bacteriol 186:7364-7368
45. Moreau PL, Gerard F, Lutz NW, Cozzone P (2001) Non-growing Escherichia coli cells starved for glucose or phosphate use different mechanisms to survive oxidative stress. Mol Microbiol 39:1048-1060
46. Muth G, Nussbaumer B, Wohlleben W, Pühler A (1989) A vector system with temperature-sensitive replication for gene disruption and mutational cloning in streptomycetes. Mol Gen Genet 219:341-348
47. Nguyen HC, Karray F, Lautru S, Gagnat J, Lebrihi A, Huynh TD, Pernodet JL (2010) Glycosylation steps during spiramycin biosynthesis in Streptomyces ambofaciens: involvement of three glycosyltransferases and their interplay with two auxiliary proteins. Antimicrob Agents Chemother 54:2830-2839
48. Oganesyan V, Oganesyan N, Adams PD, Jancarik J, Yokota HA, Kim R, Kim SH (2005) Crystal structure of the "PhoU-like" phosphate uptake regulator from Aquifex aeolicus. J Bacteriol 187:4238-4244
49. Ortiz de Orue Lucana D, Zou P, Nierhaus M, Schrempf H (2005) Identification of a novel two-component system SenS/SenR modulating the production of the catalase-peroxidase CpeB and the haem-binding protein HbpS in Streptomyces reticuli. Microbiology 151:3603-3614
50. Ortiz de Orue Lucana D, Bogel G, Zou P, Groves MR (2009) The oligomeric assembly of the novel haem-degrading protein HbpS is essential for interaction with its cognate two-component sensor kinase. J Mol Biol 386:1108-1122
51. Ortiz de Orue Lucana D, Groves MR (2009) The three-component signalling system HbpS-SenS-SenR as an example of a redox sensing pathway in bacteria. Amino Acids 37:479-486
52. Raynal A, Karray F, Tuphile K, Darbon-Rongere E, Pernodet JL (2006) Excisable cassettes: new tools for functional analysis of Streptomyces genomes. Appl Environ Microbiol 72:4839-4844
53. Redenbach M, Kieser HM, Denapaite D, Eichner A, Cullum J, Kinashi H, Hopwood DA (1996) A set of ordered cosmids and a detailed genetic and physical map for the 8 Mb Streptomyces coelicolor A3(2) chromosome. Mol Microbiol 21:77-96
54. Rice CD, Pollard JE, Lewis ZT, McCleary WR (2009) Employment of a promoter-swapping technique shows that PhoU modulates the activity of the PstSCAB2 ABC transporter in Escherichia coli. Appl Environ Microbiol 75:573-582
55. Robinson NJ, Whitehall SK, Cavet JS (2001) Microbial metallothioneins. Adv Microb Physiol 44:183-213
56. 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 ΔphoP mutant. Proteomics 7:2410-2429
57. 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
58. Russwurm M, Koesling D (2004) Guanylyl cyclase: NO hits its target. Biochem Soc Symp: 51-63
59. Sambrook J, Russel DW 2001 Molecular Cloning: a Laboratory Manual, Third edition edn., pp. Pages.
60. Sanchez R, Riddle M, Woo J, Momand J (2008) Prediction of reversibly oxidized protein cysteine thiols using protein structure properties. Protein Sci 17:473-481
61. Santos-Beneit F, Rodriguez-Garcia A, Franco-Dominguez E, Martin JF (2008) Phosphate-dependent regulation of the low- and high-affinity transport systems in the model actinomycete Streptomyces coelicolor. Microbiology 154:2356-2370
62. 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
63. 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
64. Santos-Beneit F, Barriuso-Iglesias M, Fernandez-Martinez LT, Martinez-Castro M, Sola-Landa A, Rodriguez-Garcia A, Martin 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 77:7586-7594
65. Sharma RSRT (1996) Preparation of electrocompetent E. coli using salt-free growth medium. Biotechniques 20:42-44
66. Siedenburg G, Groves MR, de Orue O, Lucana D (2012) Novel redox-sensing modules: accessory protein- and nucleic Acid-mediated signaling. Antioxid Redox Signal 16:668-677
67. 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
68. 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
69. 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
70. Steed PM, Wanner BL (1993) Use of the rep technique for allele replacement to construct mutants with deletions of the pstSCAB-phoU operon: evidence of a new role for the PhoU protein in the phosphate regulon. J Bacteriol 175:6797-6809
71. Taschner NP, Yagil E, Spira B (2004) A differential effect of sigmaS on the expression of the PHO regulon genes of Escherichia coli. Microbiology 150:2985-2992
72. Thompson CJ, Ward JM, Hopwood DA (1980) DNA cloning in Streptomyces: resistance genes from antibiotic-producing species. Nature 286:525-527
73. Touati D (2000) Iron and oxidative stress in bacteria. Arch Biochem Biophys 373:1-6
74. Vazquez-Torres A (2012) Redox active thiol sensors of oxidative and nitrosative stress. Antioxid Redox Signal (in press)
75. Wang S, He YX, Bao R, Teng YB, Ye BP, Zhou CZ (2008) Cloning, expression, purification, crystallization and preliminary X-ray diffraction analysis of hypothetical protein SCO4226 from Streptomyces coelicolor A3(2). Acta Crystallogr Sect F Struct Biol Cryst Commun 64:847-850
76. Willey JM, van der Donk WA (2007) Lantibiotics: peptides of diverse structure and function. Annu Rev Microbiol 61:477-501
77. Yu D, Ellis HM, Lee EC, Jenkins NA, Copeland NG, Court DL (2000) An efficient recombination system for chromosome engineering in Escherichia coli. Proc Natl Acad Sci USA 97:5978-5983
78. Yuan ZC, Zaheer R, Finan TM (2005) Phosphate limitation induces catalase expression in Sinorhizobium meliloti, Pseudomonas aeruginosa and Agrobacterium tumefaciens. Mol Microbiol 58:877-894