Transcriptome and physiological responses to hydrogen peroxide of the facultatively phototrophic bacterium Rhodobacter sphaeroides

Journal of Bacteriology

Volumn 187, Issue 21, 2005, Pages 7232-7242

  Zeller, Tanja ^a   Moskvin, Oleg V ^b   Li, Kuanyu ^a   Klug, Gabriele ^a,c   Gomelsky, Mark ^b  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b UNIVERSITY OF WYOMING   (United States)

^c UNIVERSITY HOSPITAL GIESSEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; HYDROGEN PEROXIDE; IRON SULFUR PROTEIN; MESSENGER RNA; OXYGEN; PROTEIN APPA PPSR; PROTEIN FNRL; REPRESSOR PROTEIN; TETRAPYRROLE DERIVATIVE; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; DETOXIFICATION; DNA DAMAGE; DNA REPAIR; ELECTRON TRANSPORT; GENE EXPRESSION REGULATION; IRON STORAGE; IRON TRANSPORT; METABOLIC REGULATION; NONHUMAN; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PHOTOSYNTHESIS; PHOTOTROPHIC BACTERIUM; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; RELIABILITY; RHODOBACTER SPHAEROIDES;

ADAPTATION, PHYSIOLOGICAL; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CHEMOTAXIS; DNA REPAIR; FLAGELLA; FLAVOPROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; HYDROGEN PEROXIDE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIDATIVE STRESS; OXYGEN; POLYSACCHARIDES, BACTERIAL; RHODOBACTER SPHAEROIDES; RNA, BACTERIAL; RNA, MESSENGER; TETRAPYRROLES; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS); PHOTOBACTERIA; RHODOBACTER SPHAEROIDES;

EID: 27144476747     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.187.21.7232-7242.2005     Document Type: Article

References (58)

1. Almiron, M., A. J. Link, D. Furlong, and R. Kolter. 1992. A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev. 6:2646-2654.
2. Boshoff, H. I., M. B. Reed, C. E. Barry III, and V. Mizrahi. 2003. DnaE2 polymerase contributes to in vivo survival and the emergence of drug resistance in Mycobacterium tuberculosis. Cell 113:183-193.
3. Braatsch, S., O. V. Moskvin, G. Klug, and M. Gomelsky. 2004. Reponses of the Rhodobacter sphaeroides transcriptome to blue light under semiaerobic conditions. J. Bacteriol. 186:7726-7735.
4. Braun, V. 2003. Iron uptake by Escherichia coli. Frontiers Biosci. 8:1409-1421.
5. Brown, O. R., E. Smyk-Randall, B. Draczynska-Lusiak, and J. A. Fee. 1995. Dihydroxy-acid dehydratasc, a [4Fe-4S] cluster-containing enzyme in Escherichia coli: effects of intracellular superoxide dismutase on its inactivation by oxidant stress. Arch. Biochem. Biophys. 319:10-22.
6. Calero, S., A. R. Fernandez de Henestrosa, and J. Barbe. 1994. Molecular cloning, sequence and regulation of expression of the recA gene of the phototrophic bacterium Rhodobacter sphaeroides. Mol. Gen. Genet. 242: 116-120.
7. Campos, É. G., M. Hermes-Lima, J. M. Smith, and R. K. Prichard. 1999. Characterisation of Fasciola hepatica cytochrome c peroxidase as an enzyme with potential antioxidant activity in vitro. Int. J. Parasitol. 29:655-662.
8. Chen, L., L. Keramati, and J. D. Helmann. 1995. Coordinate regulation of Bacillus subtilis peroxide stress genes by hydrogen peroxide and metal ions. Proc. Natl. Acad. Sci. USA 92:8190-8194.
9. Djaman, O., F. W. Outten, and J. A. Imlay. 2004. Repair of oxidized iron-sulfur clusters in Escherichia coli. J. Biol. Chem. 279:44590-44599.
10. Drews, G. 1983. Mikrobiologisches Praktikum. Springer Verlag, Heidelberg, Germany.
11. Flory, J. E., and T. J. Donohue. 1997. Transcriptional control of several aerobically induced cytochrome structural genes in Rhodobacter sphaeroides. Microbiology 143:3101-3110.
12. Gomelsky, M., and S. Kaplan. 1995a. Genetic evidence that PpsR from Rhodobacter sphaeroides 2.4.1 functions as a repressor of puc and bchF expression. J. Bacteriol. 177:1634-1637.
13. Gomelsky, M., and S. Kaplan. 1995b. 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.
14. Gomelsky, M., and S. Kaplan. 1997. Molecular genetic evidence suggesting interactions between AppA and PpsR in regulation of photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1. J. Bacteriol. 179:128-134.
15. 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.
16. Gonzalez-Flecha, B., and B. Demple. 1995. Metabolic sources of hydrogen peroxide in aerobically growing Escherichia coli. J. Biol. Chem. 270:13681-13687.
17. Helmann, J. D., M. F. Wu, A. Gaballa, P. A. Kobel, M. M. Morshedi, P. Fawcett, and C. Paddon. 2003. The global transcriptional response of Bacillus subtilis to peroxide stress is coordinated by three transcription factors. J. Bacteriol. 185:243-253.
18. 3+, and oxygen react with DNA-derived radicals formed during iron-mediated Fenton reactions. Biochemistry 35:12212-12219.
19. Higgins, V. J., N. Alic, G. W. Thorpe, M. Breitenbach, V. Larsson, and I. W. Dawes. 2002. Phenotypic analysis of gene deletant strains for sensitivity to oxidative stress. Yeast 19:203-214.
20. Imlay, J. A., and I. Fridovich. 1991. Assay of metabolic superoxide production in Escherichia coli. J. Biol. Chem. 266:6957-6965.
21. Irizarry, R. A., B. M. Bolstad, F. Collin, L. M. Cope, B. Hobbs, and T. P. Speed. 2003. Summaries of Aflymetrix GeneChip probe level data. Nucleic Acids Res. 31:e15.
22. Jude, F., T. Kohler, P. Branny, K. Perron, M. P. Mayer, R. Comte, and C. van Delden. 2003. Posttranscriptional control of quorum-sensing-dependent virulence genes by dksA in Pseudomonas aeruginosa. J. Bacteriol. 185:3558-3566.
23. Kiley, P. J., and H. Beinert. 2003. The role of Fe-S proteins in sensing and regulation in bacteria. Curr. Opin. Microbiol. 6:181-185.
24. Konola, J. T., K. E. Sargent, and J. B. Gow. 2000. Efficient repair of hydrogen peroxide-induced DNA damage by Escherichia coli requires SOS induction of RecA and RuvA proteins. Mutat. Res. 459:187-194.
25. Li, H., A. K. Singh, L. M. McIntyre, and L. A. Sherman. 2004. Differential gene expression in response to hydrogen peroxide and the putative PerR regulon of Synechocystis sp. strain PCC 6803. J. Bacteriol. 186:3331-3345.
26. Li, K., E. Haertig, and G. Klug. 2003. Thioredoxin 2 is involved in oxidative stress defence and redox-dependent expression of photosynthesis genes in Rhodobacter capsulatus. Microbiology 149:419-430.
27. Li, K., C. Pasternak, and G. Klug. 2003. Expression of the trxA gene for thioredoxin 1 in Rhodobacter sphaeroides during oxidatives stress. Arch. Microbiol. 180:484-489.
28. Li, K., S. Hein, W. Zou, and G. Klug. 2004. The glutathione-glutaredoxin system in Rhodobacter capsulatus: part of a complex regulatory network controlling defense against oxidative stress. J. Bacteriol. 186:6800-6808.
29. Masuda, S., and C. Bauer. 2002. AppA is a blue light photoreceptor that antirepresses photosynthesis gene expression in Rhodobacter sphaeroides. Cell 110:613-623.
30. Messner, K. R., and J. A. Imlay. 1999. The identification of primary sites of superoxide and hydrogen peroxide formation in the aerobic respiratory chain and sulfite reductase complex of Escherichia coli. J. Biol. Chem. 274:10119-10128.
31. Mogull, S. A., L. J. Runyen-Janecky, M. Hong, and S. M. Payne. 2001. dksA is required for intercellular spread of Shigella flexneri via an RpoS-independent mechanism. Infect. Immun. 69:5742-5751.
32. Moskvin, O. V., L. Gomelsky, and M. Gomelsky. 2005. Transcriptome analysis of the Rhodobacter sphaeroides PpsR regulon: PpsR as a master regulator of photosystem development. J. Bacteriol. 187:2148-2156.
33. T: involvement of the FnrL protein. J. Bacteriol. 180:2228-2231.
34. Oh, J. I., and S. Kaplan. 1999. The cbb3 terminal oxidase of Rhodobacter sphaeroides 2.4.1: structural and functional implications for the regulation of spectral complex formation. Biochemistry 38:2688-2696.
35. Oh, J. I., J. M. Eraso, and S. Kaplan. 2000. Interacting regulatory circuits involved in orderly control of photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1. J. Bacteriol. 182:3081-3087.
36. 3-PrrBA signal transduction pathway in vitro. Biochemistry 43:7915-7923.
37. Palma, M., D. DeLuca, S. Worgall, and L. E. N. Quadri. 2004. Transcriptome analysis of the response of Pseudomonas aeruginosa to hydrogen peroxide. J. Bacteriol. 186:248-252.
38. 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. 186:4748-4758.
39. Paul, B. J., W. Ross, T. Gaal, and R. L. Gourse. 2004. rRNA transcription in Eschenchia coli. Annu. Rev. Genet. 38:749-770.
40. Porwollik, S., J. Frye, L. D. Florea, F. Blackmer, and M. McClelland. 2003. A non-redundant microarray of genes for two related bacteria. Nucleic Acids Res. 31:1869-1876.
41. Ringeling, P. L., S. L. Davy, F. A. Monkara, C. Hunt, D. P. Dickson, A. G. McEwan, and G. R. Moore. 1994. Iron metabolism in Rhodobacter capsulatus. Characterisation of bacterioferritin and formation of non-haem iron particles in intact cells. Eur. J. Biochem. 223:847-855.
42. Roh, J. H., and S. Kaplan. 2000. Genetic and phenotypic analyses of the rdx locus of Rhodobacter sphaeroides 2.4.1. J. Bacteriol. 182:3475-3481.
43. Roh, J. H., and S. Kaplan. 2002. Interdependent expression of the cco-NOQP-rdxBHIS loci in Rhodobacter sphaeroides 2.4.1. J. Bacteriol. 184:5330-5338.
44. Roh, J. H., W. E. Smith, and S. Kaplan. 2004. Effects of oxygen and light intensity on transcriptome expression in Rhodobacter sphaeroides 2.4.1 Redox active gene expression profile. J. Biol. Chem. 279:9146-9155.
45. Samoilenko, I. I., E. I. Vasil'eva, I. B. Pavlova, and M. A. Tumanian. 1983. Mechanisms of the bactericidal action of hydrogen peroxide. Z. Mikrobiol. Epidemiol. Immunobiol. 12:30-33.
46. Schweikert, C., A. Liszkay, and P. Schopfer. 2002. Polysaccharide degradation by Fenton reaction- or peroxidase-generated hydroxyl radicals in isolated plant cell walls. Phytochemistry 61:31-35.
47. Seaver, L. C., and J. A. Imlay. 2001. Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J. Bacteriol. 183:7173-7181.
48. Seaver, L. C., and J. A. Imlay. 2004. Are respiratory enzymes the primary sources of intracellular hydrogen peroxide? J. Biol. Chem. 279:48742-48750.
49. Seib, K. L., H. J. Tseng, A. G. McEwan, M. A. Apicella, and M. P. Jennings. 2004. Defences against oxidative stress in Neisseria gonorrhoeae and Neisseria meningitidis: distinctive systems for different lifestyles. J. Infect. Dis. 190: 136-147.
50. 2+ cluster of FNR from Escherichia coli. Biochemistry 43:791-798.
51. Tapias, A., S. Campoy, and J. Barbe. 2000. Analysis of the expression of the Rhodobacter sphaeroides lexA gene. Mol. Gen. Genet. 2636:957-965.
52. Volkert, M. R., and P. Landini. 2001. Transcriptional responses to DNA damage. Curr. Opin. Microbiol. 4:178-185.
53. von Gabain, A., J. G. Belasco, J. L. Schottel, A. C. Y. Chang, and S. N. Cohen. 1983. Decay of mRNA in Escherichia coli: investigation of the fate of specific segments of transcripts. Proc. Natl. Acad. Sci. USA 80:653-657.
54. 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.
55. Zeilstra-Ryalls, J. H., and S. Kaplan. 1995. Aerobic and anaerobic regulation in Rhodobacter sphaeroides 2.4.1: the role of the fnrL gene. J. Bacteriol. 177:6422-6431.
56. Zeilstra-Ryalls, J. H., and S. Kaplan. 1998. Role of the fnrL gene in photosystem gene expression and photosynthetic growth of Rhodobacter sphaeroides. J. Bacteriol. 180:1496-1503.
57. Zeller, T., and G. Klug. 2004. Detoxification of hydrogen peroxide and expression of catalase genes in Rhodobacter. Microbiology 150:3451-3462.
58. 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.