Streptomyces coelicolor encodes a urate-responsive transcriptional regulator with homology to pecs from plant pathogens

Journal of Bacteriology

Volumn 195, Issue 21, 2013, Pages 4954-4965

  Huang, Hao ^a   Mackel, Brian J ^a   Grove, Anne ^a  

^a LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PECM PROTEIN; PECS PROTEIN; SPACER DNA; UNCLASSIFIED DRUG; URATE;

ARTICLE; BINDING SITE; CONTROLLED STUDY; GENE ACTIVITY; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; LIGAND BINDING; NONHUMAN; PLANT DISEASE; PRIORITY JOURNAL; PROTEIN BINDING; STREPTOMYCES COELICOLOR; UPREGULATION;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CLONING, MOLECULAR; DNA, INTERGENIC; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION, BACTERIAL; GENOMICS; MOLECULAR SEQUENCE DATA; PHYLOGENY; STREPTOMYCES COELICOLOR; TRANSCRIPTION FACTORS; URIC ACID;

EID: 84886040745     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00854-13     Document Type: Article

References (48)

1. Perera IC, Grove A. 2010. Molecular mechanisms of ligand-mediated attenuation of DNA binding by MarR family transcriptional regulators. J. Mol. Cell Biol. 2:243-254.
2. Grove A. 2013. MarR family transcription factors. Curr. Biol. 23:R142- R143.
3. Reverchon S, Nasser W, Robert-Baudouy J. 1994. pecS: a locus controlling pectinase, cellulase and blue pigment production in Erwinia chrysanthemi. Mol. Microbiol. 11:1127-1139.
4. Ariza RR, Cohen SP, Bachhawat N, Levy SB, Demple B. 1994. Repressor mutations in the marRAB operon that activate oxidative stress genes and multiple antibiotic resistance in Escherichia coli. J. Bacteriol. 176:143-148.
5. Perera IC, Grove A. 2011. MarR homologs with urate-binding signature. Protein Sci. 20:621-629.
6. Wilkinson SP, Grove A. 2004. HucR, a novel uric acid-responsive member of the MarR family of transcriptional regulators from Deinococcus radiodurans. J. Biol. Chem. 279:51442-51450.
7. Perera IC, Lee YH, Wilkinson SP, Grove A. 2009. Mechanism for attenuation of DNA binding by MarR family transcriptional regulators by small molecule ligands. J. Mol. Biol. 390:1019-1029.
8. Perera IC, Grove A. 2010. Urate is a ligand for the transcriptional regulator PecS. J. Mol. Biol. 402:539-551.
9. Grove A. 2010. Urate-responsive MarR homologs from Burkholderia. Mol. Biosyst. 6:2133-2142.
10. Bordelon T, Wilkinson SP, Grove A, Newcomer ME. 2006. The crystal structure of the transcriptional regulator HucR from Deinococcus radiodurans reveals a repressor preconfigured for DNA binding. J. Mol. Biol. 360:168-177.
11. Praillet T, Reverchon S, Nasser W. 1997. Mutual control of the PecS/ PecM couple, two proteins regulating virulence-factor synthesis in Erwinia chrysanthemi. Mol. Microbiol. 24:803-814.
12. Hommais F, Oger-Desfeux C, Van Gijsegem F, Castang S, Ligori S, Expert D, Nasser W, Reverchon S. 2008. PecS is a global regulator of the symptomatic phase in the phytopathogenic bacterium Erwinia chrysanthemi 3937. J. Bacteriol. 190:7508-7522.
13. Rouanet C, Nasser W. 2001. The PecM protein of the phytopathogenic bacterium Erwinia chrysanthemi, membrane topology and possible involvement in the efflux of the blue pigment indigoidine. J. Mol. Microbiol. Biotechnol. 3:309-318.
14. Sandalio LM, Fernandez VM, Ruperez FL, Del Rio LA. 1988. Superoxide free radicals are produced in glyoxysomes. Plant Physiol. 87:1-4.
15. Bolwell GP, Bindschedler LV, Blee KA, Butt VS, Davies DR, Gardner SL, Gerrish C, Minibayeva F. 2002. The apoplastic oxidative burst in response to biotic stress in plants: a three-component system. J. Exp. Bot. 53:1367-1376.
16. Yoshioka H, Bouteau F, Kawano T. 2008. Discovery of oxidative burst in the field of plant immunity: looking back at the early pioneering works and towards the future development. Plant Signal Behav. 3:153-155.
17. Huang H, Grove A. 2013. The transcriptional regulator TamR from Streptomyces coelicolor controls a key step in central metabolism during oxidative stress. Mol. Microbiol. 87:1151-1166.
18. Hodgson DA. 2000. Primary metabolism and its control in streptomycetes: a most unusual group of bacteria. Adv. Microb. Physiol. 42:47-238.
19. Laskaris P, Tolba S, Calvo-Bado L, Wellington EM. 2010. Coevolution of antibiotic production and counterresistance in soil bacteria. Environ. Microbiol. 12:783-796.
20. Haas D, Keel C. 2003. Regulation of antibiotic production in rootcolonizing Pseudomonas spp. and relevance for biological control of plant disease. Annu. Rev. Phytopathol. 41:117-153.
21. Slattery M, Rajbhandari I, Wesson K. 2001. Competition-mediated antibiotic induction in the marine bacterium Streptomyces tenjimariensis. Microb. Ecol. 41:90-96.
22. Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599.
23. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425.
24. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA. 2000. Practical Streptomyces genetics. John Innes Foundation, Norwich, United Kingdom.
25. Schmittgen TD, Livak KJ. 2008. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3:1101-1108.
26. Whitmore L, Wallace BA. 2004. DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res. 32:W668-W673.
27. Whitmore L, Wallace BA. 2008. Protein secondary structure analyses from circular dichroism spectroscopy: methods and reference databases. Biopolymers 89:392-400.
28. Sreerama N, Venyaminov SY, Woody RW. 1999. Estimation of the number of alpha-helical and beta-strand segments in proteins using circular dichroism spectroscopy. Protein Sci. 8:370-380.
29. Wilkinson SP, Grove A. 2005. Negative cooperativity of uric acid binding to the transcriptional regulator HucR from Deinococcus radiodurans. J. Mol. Biol. 350:617-630.
30. Zhou Z, Gu J, Li YQ, Wang Y. 2012. Genome plasticity and systems evolution in Streptomyces. BMC Bioinformatics 13(Suppl 10):S8.
31. Bignell DR, Huguet-Tapia JC, Joshi MV, Pettis GS, Loria R. 2010. What does it take to be a plant pathogen: genomic insights from Streptomyces species. Antonie Van Leeuwenhoek 98:179-194.
32. Lerat S, Simao-Beaunoir AM, Beaulieu C. 2009. Genetic and physiological determinants of Streptomyces scabies pathogenicity. Mol. Plant Pathol. 10:579-585.
33. Loria R, Kers J, Joshi M. 2006. Evolution of plant pathogenicity in Streptomyces. Annu. Rev. Phytopathol. 44:469-487.
34. Kirby R, Sangal V, Tucker NP, Zakrzewska-Czerwinska J, Wierzbicka K, Herron PR, Chu CJ, Chandra G, Fahal AH, Goodfellow M, Hoskisson PA. 2012. Draft genome sequence of the human pathogen Streptomyces somaliensis, a significant cause of actinomycetoma. J. Bacteriol. 194: 3544-3545.
35. Loria R, Bignell DR, Moll S, Huguet-Tapia JC, Joshi MV, Johnson EG, Seipke RF, Gibson DM. 2008. Thaxtomin biosynthesis: the path to plant pathogenicity in the genus Streptomyces. Antonie Van Leeuwenhoek 94: 3-10.
36. Guan D, Grau BL, Clark CA, Taylor CM, Loria R, Pettis GS. 2012. Evidence that thaxtomin C is a pathogenicity determinant of Streptomyces ipomoeae, the causative agent of Streptomyces soil rot disease of sweet potato. Mol. Plant Microbe Interact. 25:393-401.
37. Bukhalid RA, Chung SY, Loria R. 1998. nec1, a gene conferring a necrogenic phenotype, is conserved in plant-pathogenic Streptomyces spp. and linked to a transposase pseudogene. Mol. Plant Microbe Interact. 11:960- 967.
38. Takahashi H, Kumagai T, Kitani K, Mori M, Matoba Y, Sugiyama M. 2007. Cloning and characterization of a Streptomyces single module type non-ribosomal peptide synthetase catalyzing a blue pigment synthesis. J. Biol. Chem. 282:9073-9081.
39. Sardi P, Saracchi M, Quaroni S, Petrolini B, Borgonovi GE, Merli S. 1992. Isolation of endophytic Streptomyces strains from surface-sterilized roots. Appl. Environ. Microbiol. 58:2691-2693.
40. Tokala RK, Strap JL, Jung CM, Crawford DL, Salove MH, Deobald LA, Bailey JF, Morra MJ. 2002. Novel plant-microbe rhizosphere interaction involving Streptomyces lydicus WYEC108 and the pea plant (Pisum sativum). Appl. Environ. Microbiol. 68:2161-2171.
41. Razem FA, Bernards MA. 2003. Reactive oxygen species production in association with suberization: evidence for an NADPH-dependent oxidase. J. Exp. Bot. 54:935-941.
42. Sagi M, Davydov O, Orazova S, Yesbergenova Z, Ophir R, Stratmann JW, Fluhr R. 2004. Plant respiratory burst oxidase homologs impinge on wound responsiveness and development in Lycopersicon esculentum. Plant Cell 16:616-628.
43. Monshausen GB, Bibikova TN, Messerli MA, Shi C, Gilroy S. 2007. Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs. Proc. Natl. Acad. Sci. U. S. A. 104:20996- 21001.
44. Lehr NA, Schrey SD, Hampp R, Tarkka MT. 2008. Root inoculation with a forest soil streptomycete leads to locally and systemically increased resistance against phytopathogens in Norway spruce. New Phytol. 177:965-976.
45. Langlois P, Bourassa S, Poirier GG, Beaulieu C. 2003. Identification of Streptomyces coelicolor proteins that are differentially expressed in the presence of plant material. Appl. Environ. Microbiol. 69:1884-1889.
46. Alekshun MN, Levy SB, Mealy TR, Seaton BA, Head JF. 2001. The crystal structure of MarR, a regulator of multiple antibiotic resistance, at 2.3 A resolution. Nat. Struct. Biol. 8:710-714.
47. Saridakis V, Shahinas D, Xu X, Christendat D. 2008. Structural insight on the mechanism of regulation of the MarR family of proteins: highresolution crystal structure of a transcriptional repressor from Methanobacterium thermoautotrophicum. J. Mol. Biol. 377:655-667.
48. Kelley LA, Sternberg MJ. 2009. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4:363-371.