Role of the global transcriptional regulator PrrA in Rhodobacter sphaeroides 2.4.1: Combined transcriptome and proteome analysis

Journal of Bacteriology

Volumn 190, Issue 14, 2008, Pages 4831-4848

  Eraso, Jesus M ^a   Jung, Hyeob Roh ^a   Zeng, Xiaohua ^a   Callister, Stephen J ^b   Lipton, Mary S ^b   Kaplan, Samuel ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; ANTIBIOTIC AGENT; BETA GALACTOSIDASE; COMPLEMENTARY DNA; CYTIDINE TRIPHOSPHATE; DIMETHYL SULFOXIDE; GLUTATHIONE PEROXIDASE; KANAMYCIN; MESSENGER RNA; PHOSPHORUS 32; PROTEOME; RIBOSOME RNA; SPECTINOMYCIN; STREPTOMYCIN; TETRACYCLINE; TRANSCRIPTOME; TRIMETHOPRIM;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIUM CULTURE; BINDING SITE; CULTURE MEDIUM; DNA BINDING; DNA PROBE; ENZYME ASSAY; ESCHERICHIA COLI; FOURIER TRANSFORMATION; GENE EXPRESSION REGULATION; GENE TARGETING; GENETIC TRANSCRIPTION; ION CYCLOTRON RESONANCE MASS SPECTROMETRY; ISOTOPE LABELING; LIQUID CHROMATOGRAPHY; MICROARRAY ANALYSIS; NONHUMAN; NORTHERN BLOTTING; PHOTOSYNTHESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PRRA GENE; RHODOBACTER SPHAEROIDES; SOUTHERN BLOTTING; TANDEM MASS SPECTROMETRY; TRANSCRIPTION REGULATION;

ANAEROBIOSIS; ARTIFICIAL GENE FUSION; BACTERIAL PROTEINS; BETA-GALACTOSIDASE; DARKNESS; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REPORTER; KANAMYCIN RESISTANCE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEOME; RHODOBACTER SPHAEROIDES; RNA, BACTERIAL; RNA, MESSENGER;

RHODOBACTER SPHAEROIDES 2.4.1;

EID: 47249107417     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00301-08     Document Type: Article

References (79)

1. Adkins, J. N., M. E. Monroe, K. J. Auberry, Y. Shen, J. M. Jacobs, D. G. Camp II, F. Vitzthum, K. D. Rodland, R. C. Zangar, R. D. Smith, and J. G. Pounds. 2005. A proteomic study of the HUPO Plasma Proteome Project's pilot samples using an accurate mass and time tag strategy. Proteomics 5:3454-3466.
2. Arai, H., J. H. Roh, and S. Kaplan. 2008. Transcriptome dynamics during the transition from anaerobic photosynthesis to aerobic respiration in Rhodobacter sphaeroides 2.4.1. J. Bacteriol. 190:286-299.
3. Beattie, D. T., M. J. Mahan, and J. J. Mekalanos. 1993. Repressor binding to a regulatory site in the DNA coding sequence is sufficient to confer transcriptional regulation of the vir-repressed genes (vrg genes) in Bordetella pertussis. J. Bacteriol. 175:519-527.
4. Bourret, R. B., K. A. Borkovich, and M. I. Simon. 1991. Signal transduction pathways involving protein phosphorylation in prokaryotes. Annu. Rev. Biochem. 60:401-441.
5. Bradley, M. D., M. B. Beach, A. P. de Koning, T. S. Pratt, and R. Osuna. 2007. Effects of Fis on Escherichia coli gene expression during different growth stages. Microbiology 153:2922-2940.
6. Callister, S. J., R. C. Barry, J. N. Adkins, E. T. Johnson, W. J. Qian, B. J. M. Webb-Robertson, R. D. Smith, and M. S. Lipton. 2006. Normalization approaches for removing systematic biases associated with mass spectrometry and label-free proteomics. J. Proteome Res. 5:277-286.
7. Callister, S. J., M. A. Dominguez, C. D. Nicora, X. Zeng, C. L. Tavano, S. Kaplan, T. J. Donohue, R. D. Smith, and M. S. Lipton. 2006. Application of the accurate mass and time tag approach to the proteome analysis of subcellular fractions obtained from Rhodobacter sphaeroides 2.4.1. Aerobic and photosynthetic cell cultures. J. Proteome Res. 5:1940-1947.
8. Callister, S. J., C. D. Nicora, X. Zeng, J. H. Roh, M. A. Dominguez, C. L. Tavano, M. E. Monroe, S. Kaplan, T. J. Donohue, R. D. Smith, and M. S. Lipton. 2006. Comparison of aerobic and photosynthetic Rhodobacter sphaeroides 2.4.1 proteomes. J. Microbiol. Methods 67:424-436.
9. 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.
10. Cohen-Bazire, G., W. R. Sistrom, and R. Y. Stanier. 1957. Kinetic studies of pigment synthesis by non-sulfur purple bacteria. J. Cell. Physiol. 49:25-68.
11. 2 gene P2 promoter by the response regulator PrrA. J. Bacteriol. 184:390-399.
12. Condon, C. 2007. Maturation and degradation of RNA in bacteria. Curr. Opin. Microbiol. 10:271-278.
13. Conway, T., and G. K. Schoolnik. 2003. Microarray expression profiling: capturing a genome-wide portrait of the transcriptome. Mol. Microbiol. 47:879-889.
14. - mutant of Rhodobacter sphaeroides. J. Bacteriol. 170:320-329.
15. Delany, I., G. Spohn, R. Rappuoli, and V. Scarlato. 2002. In vitro selection of high affinity HspR-binding sites within the genome of Helicobacter pylori. Gene 283:63-69.
16. Ditta, G., S. Stanfield, D. Corbin, and D. R. Helinski. 1980. Broad host range DNA cloning system for gram-negative bacteria: construction of a gene bank of Rhizobium meliloti. Proc. Natl. Acad. Sci. USA 77:7347-7351.
17. Dryden, S. C., and S. Kaplan. 1990. Localization and structural analysis of the ribosomal RNA operons of Rhodobacter sphaeroides. Nucleic Acids Res. 18:7267-7277.
18. Dubbs, J. M., and F. R. Tabita. 2003. Interactions of the cbbII promoter-operator region with CbbR and RegA (PrrA) regulators indicate distinct mechanisms to control expression of the two cbb operons of Rhodobacter sphaeroides. J. Biol. Chem. 278:16443-16450.
19. 2 assimilation, nitrogen fixation, hydrogen metabolism and energy generation. FEMS Microbiol. Rev. 28:353-376.
20. Elsen, S., W. Dischert, A. Colbeau, and C. E. Bauer. 2000. Expression of uptake hydrogenase and molybdenum nitrogenase in Rhodobacter capsulatus is coregulated by the RegB-RegA two-component regulatory system. J. Bacteriol. 182:2831-2837.
21. Elsen, S., L. R. Swem, D. L. Swem, and C. E. Bauer. 2004. RegB/RegA, a highly conserved redox-responding global two-component regulatory system. Microbiol. Mol. Biol. Rev. 68:263-279.
22. Eraso, J. M., and S. Kaplan. 1995. Oxygen-insensitive synthesis of the photosynthetic membranes of Rhodobacter sphaeroides: a mutant histidine kinase. J. Bacteriol. 177:2695-2706.
23. Eraso, J. M., and S. Kaplan. 1994. PrrA, a putative response regulator involved in oxygen regulation of photosynthesis gene expression in Rhodobacter sphaeroides. J. Bacteriol. 176:32-43.
24. Eraso, J. M., and S. Kaplan. 2002. Redox flow as an instrument of gene regulation. Methods Enzymol. 348:216-229.
25. Gomelsky, M., and S. Kaplan. 1995. appA, a novel gene encoding a trans-acting factor involved in the regulation of photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1. J. Bacteriol. 177:4609-4618.
26. 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.
27. Halbeisen, R. E., A. Galgano, T. Scherrer, and A. P. Gerber. 2008. Post-transcriptional gene regulation: from genome-wide studies to principles. Cell. Mol. Life Sci. 65:798-813.
28. Hemschemeier, S. K., U. Ebel, A. Jager, A. Balzer, M. Kirndorfer, and G. Klug. 2000. In vivo and in vitro analysis of RegA response regulator mutants of Rhodobacter capsulatus. J. Mol. Microbiol. Biotechnol. 2:291-300.
29. Kang, Y., K. D. Weber, Y. Qiu, P. J. Kiley, and F. R. Blattner. 2005. Genome-wide expression analysis indicates that FNR of Escherichia coli K-12 regulates a large number of genes of unknown function. J. Bacteriol. 187:1135-1160.
30. Kaplan, S., J. Eraso, and J. H. Roh. 2005. Interacting regulatory networks in the facultative photosynthetic bacterium, Rhodobacter sphaeroides 2.4.1. Biochem. Soc. Trans. 33:51-55.
31. Karls, R. K., J. R. Wolf, and T. J. Donohue. 1999. Activation of the cycA P2 promoter for the Rhodobacter sphaeroides cytochrome c2 gene by the photosynthesis response regulator. Mol. Microbiol. 34:822-835.
32. Keen, N. T., S. Tamaki, D. Kobayashi, and D. Trollinger. 1988. Improved broad-host-range plasmids for DNA cloning in gram-negative bacteria. Gene 70:191-197.
33. Kelly, A., M. D. Goldberg, R. K. Carroll, V. Danino, J. C. Hinton, and C. J. Dorman. 2004. A global role for Fis in the transcriptional control of metabolism and type III secretion in Salmonella enterica serovar Typhimurium. Microbiology 150:2037-2053.
34. Kiley, P. J., and S. Kaplan. 1988. Molecular genetics of photosynthetic membrane biosynthesis in Rhodobacter sphaeroides. Microbiol. Rev. 52:50-69.
35. Labes, M., A. Puhler, and R. Simon. 1990. A new family of RSF1010-derived expression and lac-fusion broad-host-range vectors for gram-negative bacteria. Gene 89:37-46.
36. Laguri, C., R. A. Stenzel, T. J. Donohue, M. K. Phillips-Jones, and M. P. Williamson. 2006. Activation of the global gene regulator PrrA (RegA) from Rhodobacter sphaeroides. Biochemistry 45:7872-7881.
37. Laub, M. T., S. L. Chen, L. Shapiro, and H. H. McAdams. 2002. Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle. Proc. Natl. Acad. Sci. USA 99:4632-4637.
38. Lee, J. K., and S. Kaplan. 1992. Isolation and characterization of trans-acting mutations involved in oxygen regulation of puc operon transcription in Rhodobacter sphaeroides. J. Bacteriol. 174:1158-1171.
39. Lee, J. K., and S. Kaplan. 1995. Transcriptional regulation of puc operon expression in Rhodobacter sphaeroides. Analysis of the cis-acting downstream regulatory sequence. J. Biol. Chem. 270:20453-20458.
40. Lee, J. K., P. J. Kiley, and S. Kaplan. 1989. Posttranscriptional control of puc operon expression of B800-850 light-harvesting complex formation in Rhodobacter sphaeroides. J. Bacteriol. 171:3391-3405.
41. Li, C., and W. H. Wong. 2001. Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc. Natl. Acad. Sci. USA 98:31-36.
42. Li, K., C. Pasternak, E. Hartig, K. Haberzettl, A. Maxwell, and G. Klug. 2004. Thioredoxin can influence gene expression by affecting gyrase activity. Nucleic Acids Res. 32:4563-4575.
43. Li, K., C. Pasternak, and G. Klug. 2003. Expression of the trxA gene for thioredoxin 1 in Rhodobacter sphaeroides during oxidative stress. Arch. Microbiol. 180:484-489.
44. Liu, X., and P. De Wulf. 2004. Probing the ArcA-P modulon of Escherichia coli by whole genome transcriptional analysis and sequence recognition profiling. J. Biol. Chem. 279:12588-12597.
45. Mackenzie, C., J. M. Eraso, M. Choudhary, J. H. Roh, X. Zeng, P. Bruscella, A. Puskas, and S. Kaplan. 2007. Postgenomic adventures with Rhodobacter sphaeroides. Annu. Rev. Microbiol. 61:283-307.
46. Maniatis, T., J. Sambrook, and E. F. Fritsch. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
47. Mao, L., C. Mackenzie, J. H. Roh, J. M. Eraso, S. Kaplan, and H. Resat. 2005. Combining microarray and genomic data to predict DNA binding motifs. Microbiology 151:3197-3213.
48. McClure, W. R., D. K. Hawley, P. Youderian, and M. M. Susskind. 1983. DNA determinants of promoter selectivity in Escherichia coli. Cold Spring Harbor Symp. Quant. Biol. 47:477-481.
49. Monroe, M. E., N. Tolic, N. Jaitly, J. L. Shaw, J. N. Adkins, and R. D. Smith. 2007. VIPER: an advanced software package to support high-throughput LC-MS peptide identification. Bioinformatics 23:2021-2023.
50. 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.
51. Norbeck, A. D., M. E. Monroe, J. N. Adkins, K. K. Anderson, D. S. Daly, and R. D. Smith. 2005. The utility of accurate mass and LC elution time information in the analysis of complex proteomes. J. Am. Soc. Mass Spectrom. 16:1239-1249.
52. 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.
53. Oh, J. I., and S. Kaplan. 2001. Generalized approach to the regulation and integration of gene expression. Mol. Microbiol. 39:1116-1123.
54. Ouchane, S., M. Picaud, P. Therizols, F. Reiss-Husson, and C. Astier. 2007. Global regulation of photosynthesis and respiration by FnrL. The first two targets in the tetrapyrrole pathway. J. Biol. Chem. 282:7690-7699.
55. 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.
56. Patten, C. L., M. G. Kirchhof, M. R. Schertzberg, R. A. Morton, and H. E. Schellhorn. 2004. Microarray analysis of RpoS-mediated gene expression in Escherichia coli K-12. Mol. Genet. Genomics 272:580-591.
57. 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.
58. Peter, B. J., J. Arsuaga, A. M. Breier, A. B. Khodursky, P. O. Brown, and N. R. Cozzarelli. 2004. Genomic transcriptional response to loss of chromosomal supercoiling in Escherichia coli. Genome Biol. 5:R87.
59. Pilkis, S. J., E. Fox, L. Wolfe, L. Rothbarth, A. Colosia, H. B. Stewart, and M. R. el-Maghrabi. 1986. Hormonal modulation of key hepatic regulatory enzymes in the gluconeogenic/glycolytic pathway. Ann. N. Y. Acad. Sci. 478:1-19.
60. Qian, W. J., T. Liu, M. E. Monroe, E. F. Strittmatter, J. M. Jacobs, L. J. Kangas, K. Petritis, D. G. Camp II, and R. D. Smith. 2005. Probability-based evaluation of peptide and protein identifications from tandem mass spectrometry and SEQUEST analysis: the human proteome. J. Proteome Res. 4:53-62.
61. Rahman, M., M. R. Hasan, T. Oba, and K. Shimizu. 2006. Effect of rpoS gene knockout on the metabolism of Escherichia coli during exponential growth phase and early stationary phase based on gene expressions, enzyme activities and intracellular metabolite concentrations. Biotechnol. Bioeng. 94:585-595.
62. Reckinger, A. R., K. S. Jeong, A. B. Khodursky, and H. Hiasa. 2007. RecA can stimulate the relaxation activity of topoisomerase I: molecular basis of topoisomerase-mediated genome-wide transcriptional responses in Escherichia coli. Nucleic Acids Res. 35:79-86.
63. 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.
64. Schneider, R., A. Travers, T. Kutateladze, and G. Muskhelishvili. 1999. A DNA architectural protein couples cellular physiology and DNA topology in Escherichia coli. Mol. Microbiol. 34:953-964.
65. Sganga, M. W., and C. E. Bauer. 1992. Regulatory factors controlling photosynthetic reaction center and light-harvesting gene expression in Rhodobacter capsulatus. Cell 68:945-954.
66. Simon, R., U. Priefer, and A. Puhler. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Bio/Technology 1:37-45.
67. Smart, J. L., J. W. Willett, and C. E. Bauer. 2004. Regulation of hem gene expression in Rhodobacter capsulatus by redox and photosystem regulators RegA, CrtJ, FnrL, and AerR. J. Mol. Biol. 342:1171-1186.
68. Smith, R. D., G. A. Anderson, M. S. Lipton, L. Pasa-Tolic, Y. Shen, T. P. Conrads, T. D. Veenstra, and H. R. Udseth. 2002. An accurate mass tag strategy for quantitative and high-throughput proteome measurements. Proteomics 2:513-523.
69. Tai, T. N., W. A. Havelka, and S. Kaplan. 1988. A broad-host-range vector system for cloning and translational lacZ fusion analysis. Plasmid 19:175-188.
70. Tao, R., J. S. Karliner, U. Simonis, J. Zheng, J. Zhang, N. Honbo, and C. C. Alano. 2007. Pyrroloquinoline quinone preserves mitochondrial function and prevents oxidative injury in adult rat cardiac myocytes. Biochem. Biophys. Res. Commun. 363:257-262.
71. Tatusov, R. L., N. D. Fedorova, J. D. Jackson, A. R. Jacobs, B. Kiryutin, E. V. Koonin, D. M. Krylov, R. Mazumder, S. L. Mekhedov, A. N. Nikolskaya, B. S. Rao, S. Smirnov, A. V. Sverdlov, S. Vasudevan, Y. I. Wolf, J. J. Yin, and D. A. Natale. 2003. The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4:41.
72. van Niel, C. B. 1944. The culture, general physiology, and classification of the non-sulfur purple and brown bacteria. Bacteriol. Rev. 8:1-118.
73. Vieira, J., and J. Messing. 1982. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene 19:259-268.
74. s-dependent genes, promoters, and sigma factor selectivity. J. Bacteriol. 187:1591-1603.
75. Zeilstra-Ryalls, J., and S. Kaplan. 1998. Role of the fnrL gene in photosystem gene expression and photosynthetic growth of Rhodobacter sphaeroides 2.4.1. J. Bacteriol. 180:1496-1503.
76. 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.
77. Zeng, X., J. H. Roh, S. J. Callister, C. L. Tavano, T. J. Donohue, M. S. Lipton, and S. Kaplan. 2007. Proteomic characterization of the Rhodobacter sphaeroides 2.4.1 photosynthetic membrane: identification of new proteins. J. Bacteriol. 189:7464-7474.
78. Zheng, M., X. Wang, B. Doan, K. A. Lewis, T. D. Schneider, and G. Storz. 2001. Computation-directed identification of OxyR DNA binding sites in Escherichia coli. J. Bacteriol. 183:4571-4579.
79. Zhu, Y. S., and S. Kaplan. 1985. Effects of light, oxygen, and substrates on steady-state levels of mRNA coding for ribulose-1,5-bisphosphate carboxylase and light-harvesting and reaction center polypeptides in Rhodopseudomonas sphaeroides. J. Bacteriol. 162:925-932.