Responses of the Rhodobacter sphaeroides transcriptome to blue light under semiaerobic conditions

Journal of Bacteriology

Volumn 186, Issue 22, 2004, Pages 7726-7735

  Braatsch, Stephan ^a,b   Moskvin, Oleg V ^b   Klug, Gabriele ^a,c   Gomelsky, Mark ^a,b  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b UNIVERSITY OF WYOMING   (United States)

^c Institut fur Mikrobiologie und Molekularbiologie   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; DEOXYRIBODIPYRIMIDINE PHOTOLYASE; GLUTATHIONE PEROXIDASE; OXIDOREDUCTASE; OXYGEN; PROTEIN APP A; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BLUE LIGHT; CONSENSUS SEQUENCE; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; GENE REPRESSION; GENETIC COMPLEMENTATION; NONHUMAN; OXIDATIVE STRESS; PHOTORECEPTOR; PHOTOSYNTHESIS; PRIORITY JOURNAL; PROMOTER REGION; RHODOBACTER SPHAEROIDES; UPREGULATION;

BACTERIAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; LIGHT; OXYGEN; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; PROTEOME; RHODOBACTER SPHAEROIDES; TRANSCRIPTION, GENETIC;

ANIMALIA; BACTERIA (MICROORGANISMS); NEGIBACTERIA; PROTEOBACTERIA; RHODOBACTER; RHODOBACTER SPHAEROIDES; RHODOPSEUDOMONAS;

EID: 7744242257     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.186.22.7726-7735.2004     Document Type: Article

References (67)

1. Ahmad, M., and A. R. Cashmore. 1993. HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor. Nature 366:162-166.
2. B of Bacillus subtilis. J. Bacteriol. 183:1329-1338.
3. Baca, M., G. E. O. Borgstahl, M. Boissinot, P. M. Burke, D. R. Williams, K. A. Slater, and E. D. Getzoff. 1994. Complete chemical structure of photoactive yellow protein: novel thioester-linked 4-hydroxy-cinnamyl chromophore and photocycle chemistry. Biochemistry 33:14369-14377.
4. Bauer, C. E., S. Elsen, and T. H. Bird. 1999. Mechanisms for redox control of gene expression. Annu. Rev. Microbiol. 53:495-523.
5. Berrocal-Tito, G., L. Sametz-Baron, K. Eichenberg, B. A. Horwitz, and A. Herrera-Estrella. 1999. Rapid blue light regulation of a Trichoderma harzianum photolyase gene. J. Biol. Chem. 274:14288-14294.
6. Braatsch, S., and G. Klug. 2004. Blue light perception in bacteria. Photosynth. Res. 79:45-57.
7. Braatsch, S., and G. Klug. 2004. ORF90, a gene required for photoreactivation in Rhodobacter capsulatus SB1003 encodes a cyclobutane pyrimidine dimer photolyase. Photosynth. Res. 79:167-177.
8. Braatsch, S., M. Gomelsky, S. Kuphal, and G. Klug. 2002. A single flavoprotein, AppA, integrates both redox and light signals in Rhodobacter sphaeroides. Mol. Microbiol. 45:827-836.
9. Brudler, R., K. Hitomi, H. Daiyasu, H. Toh, K. I. Kucho, M. Ishiura, M. Kanehisa, V. A. Roberts, T. Todo, J. A. Tainer, and E. D. Getzoff. 2003. Identification of a new cryptochrome class: structure, function, and evolution. Mol. Cell 11:59-67.
10. Byrdin, M., A. P. Eker, M. H. Vos, and K. Brettel. 2003. Dissection of the triple tryptophan electron transfer chain in Escherichia coli DNA photolyase: Trp382 is the primary donor in photoactivation. Proc. Natl. Acad. Sci. USA 100:8676-8681.
11. Choudhary, M., and S. Kaplan. 2000. DNA sequence analysis of the photosynthesis region of Rhodobacter sphaeroides 2.4.1. Nucleic Acids Res. 28:862-867.
12. Christie, J. M., M. Salomon, K. Nozue, M. Wada, and W. R. Briggs. 1999. LOV (light, oxygen, or voltage) domains of the blue-light photoreceptor phototropin (nph1): binding sites for the chromophore flavin mononucleotide. Proc. Natl. Acad. Sci. USA 96:8779-8783.
13. Christie, J. M., P. Reymond, G. K. Powell, P. Bernasconi, A. A. Raibekas, E. Liscum, and W. R. Briggs. 1998. Arabidopsis NPH1: a flavoprotein with the properties of a photoreceptor for phototropism. Science 282:1698-1701.
14. Cohen-Bazire, G., W. R. Sistrom, and R. V. Stanier. 1957. Kinetic studies of pigment synthesis by non-sulfur bacteria. J. Cell. Comp. Physiol. 49:25-68.
15. Desikan, R., S. A.-H.-Mackerness, J. T. Hancock, and S. J. Neill. 2001. Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol. 127:159-172.
16. Gomelsky, L., J. Sram, O. V. Moskvin, I. M. Horne, H. N. Dodd, J. M. Pemperton, A. G. McEwan, S. Kaplan, and M. Gomelsky. 2003. Identification and in vivo characterization of PpaA, a regulator of photosystem formation in Rhodobacter sphaeroides. Microbiology 149:377-388.
17. Gomelsky, M., and G. Klug. 2002. BLUF: a novel FAD-binding domain involved in sensory transduction in microorganisms. Trends Biochem. Sci. 27:497-500.
18. Gomelsky, M., and S. Kaplan. 1995. appA, a novel gene encoding a transacting factor involved in the regulation of photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1. J. Bacteriol. 177:4609-4618.
19. Gomelsky, M., and S. Kaplan. 1995. Genetic evidence that PpsR from Rhodobacter sphaeroides 2.4.1 functions as a repressor of puc and bchF expression. J. Bacteriol. 177:1634-1637.
20. Gomelsky, M., and S. Kaplan. 1997. Molecular genetic analysis suggesting interactions between AppA and PpsR in regulation of photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1. J. Bacteriol. 179:128-134.
21. Gomelsky, M., and S. Kaplan. 1998. AppA, a redox regulator of photosystem formation in Rhodobacter sphaeroides 2.4.1, is a flavoprotein. Identification of a novel FAD binding domain. J. Biol. Chem. 273:35319-35325.
22. Gomelsky, M., I. M. Horne, H. J. Lee, J. M. Pemberton, A. G. McEwan, and S. Kaplan. 2000. Domain structure, oligomeric state, and mutational analysis of PpsR, the Rhodobacter sphaeroides repressor of photosystem gene expression. J. Bacteriol. 182:2253-2261.
23. Gregor, J., and G. Klug. 1999. Regulation of bacterial photosynthesis genes by oxygen and light. FEMS Microbiol. Lett. 179:1-9.
24. Gregor, J., and G. Klug. 2002. Oxygen-regulated expression of genes for pigment binding proteins in Rhodobacter capsulatus. J. Mol. Microbiol. Biotechnol. 4:249-253.
25. Hoff, W. D., I. H. Stokkum, M. E. van Brederode, A. M. Brouwer, J. C. Fitch, T. E. Meyer, R. van Grondelle, and K. J. Hellingwerf. 1994. Measurement and global analysis of the absorbance changes in the photocycle of the photoactive yellow protein from Ectothiorhodospira halophila. Biophys. J. 67:1691-1705.
26. Holland, M. J. 2002. Transcript abundance in yeast varies over six orders of magnitude. J. Biol. Chem. 277:14363-14366.
27. Irizarry, R. A., B. M. Bolstad, F. Collin, L. M. Cope, B. Hobbs, and T. P. Speed. 2003. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31:e15.
28. Jackson, J. B. 1988. Bacterial photosynthesis, p. 317-376. In C. Anthony (ed.), Bacterial energy transduction. Academic Press, Ltd., London, United Kingdom.
29. Jiang, Z. Y., L. R. Swem, B. G. Rushing, S. Devanathan, G. Tollin, and C. E. Bauer. 1999. Bacterial photoreceptor with similarity to photoactive yellow protein and plant phytochromes. Science 285:406-409.
30. Kalai, T., E. Hideg, I. Vass, and K. Hideg. 1998. Double (fluorescent and spin) sensors for detection of reactive oxygen species in the thylakoid membrane. Free Radic. Biol. Med. 24:649-652.
31. Kanai, S., R. Kikuno, H. Toh, H. Ryo, and T. Todo. 1997. Molecular evolution of the photolyase-blue-light photoreceptor family. J. Mol. Evol. 45:535-548.
32. Laan, W., M. A. van der Horst, I. H. van Stokkum, and K. J. Hellingwerf. 2003. Initial characterization of the primary photochemistry of AppA, a blue-light-using flavin adenine dinucleotide-domain containing transcriptional antirepressor protein from Rhodobacter sphaeroides: a key role for reversible intramolecular proton transfer from the flavin adenine dinucleotide chromophore to a conserved tyrosine? Photochem. Photobiol. 78:290-297.
33. Lee, J. M., S. Zhang, S. Saha, S. Santa Anna, C. Jiang, and J. Perkins. 2001. RNA expression analysis using an antisense Bacillus subtilis genome array. J. Bacteriol. 183:7371-7380.
34. Lei, X. G. 2001. Glutathione peroxidase-1 gene knockout on body antioxidant defense in mice. Biofactors 14:93-99.
35. Leichert, L., C. Scharf, and M. Hecker. 2003. Global characterization of disulfide stress in Bacillus subtilis. J. Bacteriol. 185:1967-1975.
36. Losi, A., E. Polverini, B. Quest, and W. Gartner. 2002. First evidence for phototropin-related blue-light receptors in prokaryotes. Biophys. J. 82:2627-2634.
37. MacGregor, B. J., R. K. Karls, and T. J. Donohue. 1998. Transcription of the Rhodobacter sphaeroides cycA P1 promoter by alternative RNA polymerase holoenzymes. J. Bacteriol. 180:1-9.
38. Malhotra, K., S. T. Kim, A. Batschauer, L. Dawut, and A. Sancar. 1995. Putative blue-light photoreceptors from Arabidopsis thaliana and Sinapis alba with a high degree of sequence homology to DNA photolyase contain the two photolyase cofactors but lack DNA repair activity. Biochemistry 34:6892-6899.
39. Masuda, S., and C. E. Bauer. 2002. AppA is a blue light photoreceptor that antirepresses photosynthesis gene expression in Rhodobacter sphaeroides. Cell 110:613-623.
40. McEwan, A. G. 1994. Photosynthetic electron transport and anaerobic metabolism in purple non-sulfur bacteria. Antonie Leeuwenhoek 66:151-164.
41. Meyer, T. E. 1985. Isolation and characterization of soluble cytochromes, ferredoxins, and other chromophoric proteins from the halophilic phototrophic bacterium Ectothiorhodospira halophila. Biochim. Biophys. Acta 806:175-183.
42. Mitani, H., N. Uchida, and A. Shima. 1996. Induction of cyclobutane pyrimidine dimer photolyase in cultured fish cells by UVA and blue light. Photochem. Photobiol. 64:943-948.
43. Newman, J. D., L. C. Anthony, and T. J. Donohue. 2001. The importance of zinc-binding to the function of Rhodobacter sphaeroides ChrR as an anti-sigma factor. J. Mol. Biol. 313:495-499.
44. E, and the target promoters cycA P3 and rpoE P1. J. Mol. Biol. 294:307-320.
45. Oh, J. I., and S. Kaplan. 2000. Redox signaling: globalization of gene expression. EMBO J. 19:4237-4247.
46. Pappas, C. T., J. Sram, O. V. Moskvin, P. S. Ivanov, R. C. Mackenzie, M. Choudhary, M. L. Land, F. W. Larimer, S. Kaplan, and M. Gomelsky. 2004. Construction and validation of the Rhodobacter sphaeroides 2.4.1 DNA microarray: transcriptome flexibility at diverse growth modes. J. Bacteriol. 186: in press.
47. Penfold, R. J., and J. M. Pemberton. 1991. A gene from the photosynthetic cluster of Rhodobacter sphaeroides induces trans suppression of bacteriochlorophyll and carotenoid levels in R. sphaeroides and R. capsulatus. Curr. Microbiol. 23:259-263.
48. Penfold, R. J., and J. M. Pemberton. 1994. Sequencing, chromosomal inactivation, and functional expression in Escherichia coli of ppsR, a gene which represses carotenoid and bacteriochlorophyll synthesis in Rhodobacter sphaeroides. J. Bacteriol. 176:2869-2876.
49. Raivio, T. L., and T. J. Silhavy. 2001. Periplasmic stress and ECF sigma factors. Annu. Rev. Microbiol. 55:591-624.
50. Sancar, A. 2003. Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors. Chem. Rev. 103:2203-2237.
51. Schilke, B. A., and T. J. Donohue. 1995. ChrR positively regulates transcription of the Rhodobacter sphaeroides cytochrome c2 gene. J. Bacteriol. 177:1929-1937.
52. Schneider, T. D., and R. M. Stephens. 1990. Sequence logos: a new way to display consensus sequences. Nucleic Acids Res. 18:6097-6100.
53. Shimada, H., K. Iba, and K. Takamiya. 1992. Blue-light irradiation reduces the expression of puf and puc operons of Rhodobacter sphaeroides under semi-aerobic conditions. Plant Cell Physiol. 33:471-475.
54. Sprenger, W. W., W. D. Hoff, J. P. Armitage, and K. J. Hellingwerf. 1993. The eubacterium Ectothiorhodospira halophila is negatively phototactic, with a wavelength dependence that fits the absorption spectrum of the photoactive yellow protein. J. Bacteriol. 175:3096-3104.
55. Storz, G., and J. A. Imlay. 1999. Oxidative stress. Curr. Opin. Microbiol. 2:188-194.
56. Storz, G., and M. Zheng. 2000. Oxidative stress, p. 47-59. In G. Storz and R. Hengge-Aronis (ed.), Bacterial stress responses. ASM Press, Washington, D.C.
57. Suwanto, A., and S. Kaplan. 1989. Physical and genetic mapping of the Rhodobacter sphaeroides 2.4.1 genome: genome size, fragment identification, and gene localization. J. Bacteriol. 171:5850-5859.
58. Wosten, M. M. 1998. Eubacterial sigma-factors. FEMS Microbiol. Rev. 22: 127-150.
59. Worthington, E. N., I. H. Kavakli, G. Berrocal-Tito, B. E. Bondo, and A. Sancar. 2003. Purification and characterization of three members of the photolyase/cryptochrome family blue-light photoreceptors from Vibrio cholerae. J. Biol. Chem. 278:39143-39154.
60. Yang, H., A. Sasarman, H. Inokuchi, and J. Adler. 1996. Non-iron porphyrins cause tumbling to blue light by an Escherichia coli mutant defective in hemG. Proc. Natl. Acad. Sci. USA 93:2459-2463.
61. Yang, H., H. Inokuchi, and J. Adler. 1995. Phototaxis away from blue light by an Escherichia coli mutant accumulating protoporphyrin IX. Proc. Natl. Acad. Sci. USA 92:7332-7336.
62. Yasuhira, S., H. Mitani, and A. Shima. 1991. Enhancement of photorepair of ultraviolet-damage by preillumination with fluorescent light in cultured fish cells. Photochem. Photobiol. 53:211-215.
63. Yuen, T., E. Wurmbach, R. L. Pfeffer, B. J. Ebersole, and S. C. Sealfon. 2002. Accuracy and calibration of commercial oligonucleotide and custom cDNA microarrays. Nucleic Acids Res. 30:E48.
64. Zeilstra-Ryalls, J. H., and S. Kaplan. 2004. Oxygen intervention in the regulation of gene expression: the photosynthetic bacterial paradigm. Cell Mol. Life Sci. 61:417-436.
65. Zeilstra-Ryalls, J. H., M. Gomelsky, A. A. Yeliseev, J. M. Eraso, and S. Kaplan. 1998. Transcriptional regulation of photosynthesis operons in Rhodobacter sphaeroides 2.4.1. Methods Enzymol. 297:151-166.
66. Zeng, X., M. Choudhary, and S. Kaplan. 2003. A second and unusual pucBA operon of Rhodobacter sphaeroides 2.4.1: genetics and function of the encoded polypeptides. J. Bacteriol. 185:6171-6184.
67. Zheng, M., X. Wang, L. J. Templeton, D. R. Smulski, R. A. LaRossa, and G. Storz. 2001. DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J. Bacteriol. 183:4562-4570.