Transcriptome dynamics during the transition from anaerobic photosynthesis to aerobic respiration in Rhodobacter sphaeroides 2.4.1

Journal of Bacteriology

Volumn 190, Issue 1, 2008, Pages 286-299

  Arai, Hiroyuki ^a,b   Jung, Hyeob Roh ^a   Kaplan, Samuel ^a  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C OXIDASE; TRANSCRIPTOME;

AEROBIC METABOLISM; ANAEROBIC METABOLISM; ARTICLE; CARBOHYDRATE TRANSPORT; CELL COMPOSITION; DATA ANALYSIS; DNA MICROARRAY; ENERGY METABOLISM; GENE CLUSTER; GENE EXPRESSION REGULATION; HOMEOSTASIS; LIPID TRANSPORT; NONHUMAN; OXIDATION KINETICS; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; OXYGEN TENSION; PHOTOSYNTHESIS; PRIORITY JOURNAL; RHODOBACTER SPHAEROIDES; TIME SERIES ANALYSIS;

AEROBIOSIS; ANAEROBIOSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; KINETICS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXYGEN CONSUMPTION; PHOTOSYNTHESIS; RHODOBACTER SPHAEROIDES; RNA, BACTERIAL;

RHODOBACTER SPHAEROIDES 2.4.1;

EID: 37549018895     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01375-07     Document Type: Article

References (88)

1. Aklujkar, M., R. C. Prince, and J. T. Beatty. 2005. The puhE gene of Rhodobacter capsulatus is needed for optimal transition from aerobic to photosynthetic growth and encodes a putative negative modulator of bacteriochlorophyll production. Arch. Biochem. Biophys. 437:186-198.
2. Aklujkar, M., R. C. Prince, and J. T. Beatty. 2005. The PuhB protein of Rhodobacter capsulatus functions in photosynthetic reaction center assembly with a secondary effect on light-harvesting complex 1. J. Bacteriol. 187:1334-1343.
3. Aklujkar, M., R. C. Prince, and J. T. Beatty. 2006. The photosynthetic deficiency due to puhC gene deletion in Rhodobacter capsulatus suggests a PuhC protein-dependent process of RC/LH1/PufX complex reorganization. Arch. Biochem. Biophys. 454:59-71.
4. Aldridge, P., and K. T. Hughes. 2002. Regulation of flagellar assembly. Curr. Opin. Microbiol. 5:160-165.
5. Andrews, S. C., A. K. Robinson, and F. Rodríguez- Quiñones. 2003. Bacterial iron homeostasis. FEMS Microbiol. Rev. 27:215-237.
6. Anthony, J. R., K. L. Warczak, and T. J. Donohue. 2005. A transcriptional response to singlet oxygen, a toxic byproduct of photosynthesis. Proc. Natl. Acad. Sci. USA 102:6502-6507.
7. Barras, F., L. Loiseau, and B. Py. 2005. How Escherichia coli and Saccharomyces cerevisiae build Fe/S proteins. Adv. Microb. Physiol. 50:41-101.
8. Beller, H. R., T. E. Letain, A. Chakicherla, S. R. Kane, T. C. Legler, and M. A. Coleman. 2006. Whole-genome transcriptional analysis of chemolitho-autotrophic thiosulfate oxidation by Thiobacillus denitrificans under aerobic versus denitrifying conditions. J. Bacteriol. 188:7005-7015.
9. Boes, N., K. Schreiber, E. Härtig, L. Jaensch, and M. Schobert. 2006. The Pseudomonas aeruginosa universal stress protein PA4352 is essential for surviving anaerobic energy stress. J. Bacteriol. 188:6529-6538.
10. 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.
11. Braatsch, S., O. V. Moskvin, G. Klug, and M. Gomelsky. 2004. Responses of the Rhodobacter sphaeroides transcriptome to blue light under semiaerobic conditions. J. Bacteriol. 186:7726-7735.
12. 2 structural gene. J. Bacteriol. 171:360-368.
13. 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.
14. 1 complex from Rhodobacter sphaeroides. Biochemistry 33:10207-10214.
15. Chilcott, G. S., and K. T. Hughes. 2000. Coupling of flagellar gene expression to flagellar assembly in Salmonella enterica serovar typhimurium and Escherichia coli. Microbiol. Mol. Biol. Rev. 64:694-708.
16. 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.
17. 3-type cytochrome c oxidases during respiratory growth of Rhodobacter sphaeroides. J. Bacteriol. 183:2013-2024.
18. D'Argenio, D. A., and S. I. Miller. 2004. Cyclic di-GMP as a bacterial second messenger. Microbiology 150:2497-2502.
19. Dasgupta, N., M. C. Wolfgang, A. L. Goodman, S. K. Arora, J. Jyot, S. Lory, and R. Ramphal. 2003. A four-tiered transcriptional regulatory circuit controls flagellar biogenesis in Pseudomonas aeruginosa. Mol. Microbiol. 50:809-824.
20. 2 deficient mutants of Rhodobacter sphaeroides. Biochemistry 27:1918-1925.
21. Donohue, T. J., P. J. Kiley, and S. Kaplan. 1988. The puf operon region of Rhodobacter sphaeroides. Photosynth. Res. 19:39-61.
22. 2 assimilation, nitrogen fixation, hydrogen metabolism and energy generation. FEMS Microbiol. Rev. 28:353-376.
23. 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.
24. 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.
25. 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.
26. 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.
27. 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.
28. Gomelsky, L., J. Sram, O. V. Moskvin, I. M. Horne, H. N. Dodd, J. M. Pemberton, 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.
29. Green, H. A., and T. J. Donohue. 2006. Activity of Rhodobacter sphaeroides RpoHII, a second member of the heat shock sigma factor family. J. Bacteriol. 188:5712-5721.
30. Hahn, F. M., L. M. Eubanks, C. A. Testa, B. S. Blagg, J. A. Baker, and C. D. Poulter. 2001. 1-Deoxy-D-xylulose 5-phosphate synthase, the gene product of open reading frame (ORF) 2816 and ORF 2895 in Rhodobacter capsulatus. J. Bacteriol. 183:1-11.
31. Hallenbeck, P. L., R. Lerchen, P. Hessler, and S. Kaplan. 1990. Roles of CfxA, CfxB, and external electron acceptors in regulation of ribulose 1,5-bisphosphate carboxylase/oxygenase expression in Rhodobacter sphaeroides. J. Bacteriol. 172:1736-1748.
32. Happ, H. N., S. Braatsch, V. Broschek, L. Osterloh, and G. Klug. 2005. Light-dependent regulation of photosynthesis genes in Rhodobacter sphaeroides 2.4.1 is coordinately controlled by photosynthetic electron transport via the PrrBA two-component system and the photoreceptor AppA. Mol. Microbiol. 58:903-914.
33. Hondorp, E. R., and R. G. Matthews. 2004. Oxidative stress inactivates cobalamin-independent methionine synthase (MetE) in Escherichia coli. PLoS Biol. 2:e336.
34. Jäger, A., S. Braatsch, K. Haberzettl, S. Metz, L. Osterloh, Y. Han, and G. Klug. 2007. The AppA and PpsR proteins from Rhodobacter sphaeroides can establish a redox-dependent signal chain but fail to transmit blue-light signals in other bacteria. J. Bacteriol. 189:2274-2282.
35. Jones, H. M., and R. P. Gunsalus. 1987. Regulation of Escherichia coli fumarate reductase (frdABCD) operon expression by respiratory electron acceptors and the fnr gene product. J. Bacteriol. 169:3340-3349.
36. Kalir, S., J. McClure, K. Pabbaraju, C. Southward, M. Ronen, S. Leibler, M. G. Surette, and U. Alon. 2001. Ordering genes in a flagella pathway by analysis of expression kinetics from living bacteria. Science 292:2080-2083.
37. Kaplan, S., B. D. Cain, T. J. Donohue, W. D. Shepherd, and G. S. Yen. 1983. Biosynthesis of the photosynthetic membranes of Rhodopseudomonas sphaeroides. J. Cell. Biochem. 22:15-29.
38. 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.
39. Kiley, P. J., and S. Kaplan. 1987. Cloning, DNA sequence, and expression of the Rhodobacter sphaeroides light-harvesting B800-850-α and B800-850-β genes. J. Bacteriol. 169:3268-3275.
40. Kiley, P. J., and S. Kaplan. 1988. Molecular genetics of photosynthetic membrane biosynthesis in Rhodobacter sphaeroides. Microbiol. Rev. 52:50-69.
41. 3 oxidase in the regulation of photosynthesis gene expression through the PrrBA system in Rhodobacter sphaeroides 2.4.1. J. Bacteriol. 189:5617-5625.
42. Krieger-Liszkay, A. 2005. Singlet oxygen production in photosynthesis. J. Exp. Bot. 56:337-346.
43. 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.
44. Lee, J. K., and S. Kaplan. 1992. cis-acting regulatory elements involved in oxygen and light control of puc operon transcription in Rhodobacter sphaeroides. J. Bacteriol. 174:1146-1157.
45. Leichert, L. I., and U. Jakob. 2004. Protein thiol modifications visualized in vivo. PLoS Biol. 2:e333.
46. 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.
47. Mackenzie, C., M. Choudhary, F. W. Larimer, P. F. Predki, S. Stilwagen, J. P. Armitage, R. D. Barber, T. J. Donohue, J. P. Hosler, J. E. Newman, J. P. Shapleigh, R. E. Sockett, J. Zeilstra-Ryalls, and S. Kaplan. 2001. The home stretch, a first analysis of the nearly completed genome of Rhodobacter sphaeroides 2.4.1. Photosynth. Res. 70:19-41.
48. 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.
49. Martin, A. C., M. Gould, E. Byles, M. A. Roberts, and J. P. Armitage. 2006. Two chemosensory operons of Rhodobacter sphaeroides are regulated independently by sigma 28 and sigma 54. J. Bacteriol. 188:7932-7940.
50. 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.
51. Meijer, W. G., and F. R. Tabita. 1992. Isolation and characterization of the nifUSVW-rpoN gene cluster from Rhodobacter sphaeroides. J. Bacteriol. 174:3855-3866.
52. Meinhardt, S. W., P. J. Kiley, S. Kaplan, A. R. Crofts, and S. Harayama. 1985. Characterization of light-harvesting mutants of Rhodopseudomonas sphaeroides. I. Measurement of the efficiency of energy transfer from light-harvesting complexes to the reaction center. Arch. Biochem. Biophys. 236:130-139.
53. 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.
54. T: involvement of the FnrL protein. J. Bacteriol. 180:2228-2231.
55. T: identification and characterization of genes encoding quinol oxidases. FEMS Microbiol. Lett. 192:205-210.
56. y from Rhodobacter sphaeroides is functional in respiratory but not in photosynthetic electron transfer. Proc. Natl. Acad. Sci. USA 96:4348-4353.
57. Oh, J. I., and S. Kaplan. 2000. Redox signaling: globalization of gene expression. EMBO J. 19:4237-4247.
58. Oh, J. I., and S. Kaplan. 2001. Generalized approach to the regulation and integration of gene expression. Mol. Microbiol. 39:1116-1123.
59. Oh, J. I., I. J. Ko, and S. Kaplan. 2003. Digging deeper: uncovering genetic loci which modulate photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1. Microbiology 149:949-960.
60. Østerås, M., and U. Jenal. 2000. Regulatory circuits in Caulobacter. Curr. Opin. Microbiol. 3:171-176.
61. 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.
62. Partridge, J. D., C. Scott, Y. Tang, R. K. Poole, and J. Green. 2006. Escherichia coli transcriptome dynamics during the transition from anaerobic to aerobic conditions. J. Biol. Chem. 281:27806-27815.
63. Partridge, J. D., G. Sanguinetti, D. P. Dibden, R. E. Roberts, R. K. Poole, and J. Green. 2007. Transition of Escherichia coli from aerobic to microaerobic conditions involves fast and slow reacting regulatory components. J. Biol. Chem. 282:11230-11237.
64. 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.
65. 54 factors of Rhodobacter sphaeroides are not functionally interchangeable. Mol. Microbiol. 46:75-85.
66. Poggio, S., A. Osorio, G. Dreyfus, and L. Camarena. 2005. The flagellar hierarchy of Rhodobacter sphaeroides is controlled by the concerted action of two enhancer-binding proteins. Mol. Microbiol. 58:969-983.
67. Poggio, S., A. Osorio, G. Dreyfus, and L. Camarena. 2006. Transcriptional specificity of RpoN1 and RpoN2 involves differential recognition of the promoter sequences and specific interaction with the cognate activator proteins. J. Biol. Chem. 281:27205-27215.
68. Poggio, S., C. Abreu-Goodger, S. Fabela, A. Osorio, G. Dreyfus, P. Vinuesa, and L. Camarena. 2007. A complete set of flagellar genes acquired by horizontal transfer coexists with the endogenous flagellar system in Rhodobacter sphaeroides. J. Bacteriol. 189:3208-3216.
69. 28-dependent flagellar gene transcription hierarchy of Vibrio cholerae. Mol. Microbiol. 39:1595-1609.
70. Prüß, B. M., and P. Matsumura. 1997. Cell cycle regulation of flagellar genes. J. Bacteriol. 179:5602-5604.
71. 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.
72. Römling, U., M. Gomelsky, and M. Y. Galperin. 2005. C-di-GMP: the dawning of a novel bacterial signalling system. Mol. Microbiol. 57:629-639.
73. Schreiber, K., N. Boes, M. Eschbach, L. Jaensch, J. Wehland, T. Bjarnsholt, M. Givskov, M. Hentzer, and M. Schobert. 2006. Anaerobic survival of Pseudomonas aeruginosa by pyruvate fermentation requires an Usp-type stress protein. J. Bacteriol. 188:659-668.
74. Shapiro, L., and R. Losick. 2000. Dynamic spatial regulation in the bacterial cell. Cell 100:89-98.
75. Unden, G., and J. Schirawski. 1997. The oxygen-responsive transcriptional regulator FNR of Escherichia coli: the search for signals and reactions. Mol. Microbiol. 25:205-210.
76. Wood, B. J. B., B. W. Nichols, and A. T. James. 1965. The lipids and fatty acid metabolism of photosynthetic bacteria. Biochim. Biophys. Acta 106:261-273.
77. Yeliseev, A. A., and S. Kaplan. 1995. A sensory transducer homologous to the mammalian peripheral-type benzodiazepine receptor regulates photosynthetic membrane complex formation in Rhodobacter sphaeroides 2.4.1. J. Biol. Chem. 270:21167-21175.
78. Yeliseev, A. A., and S. Kaplan. 1999. A novel mechanism for the regulation of photosynthesis gene expression by the TspO outer membrane protein of Rhodobacter sphaeroides 2.4.1. J. Biol. Chem. 274:21234-21243.
79. Yeliseev, A. A., and S. Kaplan. 2000. TspO of Rhodobacter sphaeroides. A structural and functional model for the mammalian peripheral benzodiazepine receptor. J. Biol. Chem. 275:5657-5667.
80. Young, C. S., and J. T. Beatty. 1998. Topological model of the Rhodobacter capsulatus light-harvesting complex 1 assembly protein LhaA (previously known as ORF1696). J. Bacteriol. 180:4742-4745.
81. Young, C. S., R. C. Reyes, and J. T. Beatty. 1998. Genetic complementation and kinetic analyses of Rhodobacter capsulatus ORF1696 mutants indicate that the ORF1696 protein enhances assembly of the light-harvesting I complex. J. Bacteriol. 180:1759-1765.
82. 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.
83. Zeilstra-Ryalls, J., M. Gomelsky, J. M. Eraso, A. Yeliseev, J. O'Gara, and S. Kaplan. 1998. Control of photosystem formation in Rhodobacter sphaeroides. J. Bacteriol. 180:2801-2809.
84. 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.
85. Zeilstra-Ryalls, J. H., and K. L. Schornberg. 2006. Analysis of hemF gene function and expression in Rhodobacter sphaeroides 2.4.1. J. Bacteriol. 188:801-804.
86. Zeller, T., O. V. Moskvin, K. Li, G. Klug, and M. Gomelsky. 2005. Transcriptome and physiological responses to hydrogen peroxide of the facultatively phototrophic bacterium Rhodobacter sphaeroides. J. Bacteriol. 187:7232-7342.
87. 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.
88. Zhu, Y. S., P. J. Kiley, T. J. Donohue, and S. Kaplan. 1986. Origin of the mRNA stoichiometry of the puf operon in Rhodobacter sphaeroides. J. Biol. Chem. 261:10366-10374.