Summary
Purple photosynthetic bacteria control numerous energy-generating and energy-utilizing processes in response to alterations in cellular redox, which is affected by environmental oxygen tension. The list of redox-regulated events includes synthesis of the pigmented and cytochrome components of the photosystem, enzymes for fixation of carbon and nitrogen, the synthesis of several terminal respiratory electron transport complexes, and synthesis of the energy-generating hydrogenase complex. Regulating synthesis of these components involves several well-characterized transcription factors including the sensor kinase RegB and its cognate response regulator RegA. Other redox-responding regulators include CrtJ and Fnr. Mechanisms of redox sensing by these transcription factors are discussed.
Access provided by Autonomous University of Puebla. Download to read the full chapter text
Chapter PDF
Similar content being viewed by others
Keywords
- Rhodobacter Sphaeroides
- Rhodobacter Capsulatus
- Redox Control
- Rhodopseudomonas Palustris
- Purple Photosynthetic Bacterium
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
Abbreviations
- B. :
-
Bradyrhizobium
- bp:
-
base pair(s)
- E. :
-
Escherichia
- NMR:
-
nuclear magnetic resonance
- P. :
-
Pseudomonas
- PAS:
-
Per-ARNT-Sim
- Rba. :
-
Rhodobacter
- Rps. :
-
Rhodopseudomonas
References
Armstrong GA, Schmidt A, Sandmann G and Hearst JE (1990) Genetic and biochemical characterization of carotenoid biosynthesis mutants of Rhodobacter capsulatus. J Biol Chem 265: 8329–8338
Bauer CE, Young DA and Marrs BL (1988) Analysis of the Rhodobacter capsulatus puf operon: Location of the oxygen regulatedpromoterregion and the identification of an additional puf encoded gene. J Biol Chem 263: 4820–4827
Bauer CE, Elsen S and Bird TH (1999) Mechanisms for redox control of gene expression. Ann Rev Microbiol 53: 495–523
Bauer E, Kaspar T, Fischer HM and Hennecke H (1998) Expression of the fixR-nifA operon in Bradyrhizobium japonicum depends on a new response regulator, RegR. J Bacteriol 180: 3853–3863
Bird TH, Du S and Bauer CE (1999) Autophosphorylation, phosphotransfer, and DNA-binding properties of the RegB/RegA two-component regulatory system in Rhodobacter capsulatus. J Biol Chem 274: 16343–16348
Bollivar DW, Suzuki JY, Beatty JT, Dobrowlski JD and Bauer CE (1994) Directed mutational analysis of bacteriochlorophyll a biosynthesis in Rhodobacter capsulatus. J Mol Biol 237: 622–640
Bolton JR (1978) Primary electron acceptor. In: Clayton RK and Sistrom WR (ed) The Photosynthetic Bacteria, pp 419–429. Plenum Press, New York
Bowman WC, Du S, Bauer CE and Kranz RG (1999) In vitro activation and repression of photosynthesis gene transcription in Rhodobacter capsulatus. Mol Microbiol 33: 429–437
Bratsch S, Gomelsky M, Kuphal S and Klug G (2002) A single flavoprotein, AppA, integrates both redox and light signals in Rhodobacter sphaeroides. Mol Microbiol 45: 827–836
Braatsch S, Bernstein JR, Lessner F, Morgan J, Liao JC, Harwood CS and Beatty JT (2006) Rhodopseudomonas palustris CGA009 has two functional ppsR genes, each of which encodes a repressor of photosynthesis gene expression. Biochemistry 45: 14441–14451
Braatsch S, Johnson JA, Noll K and Beatty JT (2007) The O2-responsive repressor PpsR2 but not PpsR1 transduces a light signal sensedby the BphP1 phytochrome in Rhodopseudomonas palustris CGA009. FEMS Microbiol Lett 272: 60–64
Buggy J and Bauer CE (1995). Cloning and characterization of senC, a gene involved in both aerobic respiration and photosynthesis gene expression in Rhodobacter capsulatus. J Bacteriol 177, 6958–6965
Chen W, Jager A and Klug G (2000) Correction of the DNA sequence of the regB gene of Rhodobacter capsulatus with implications for the membrane topology of the sensor kinase RegB. J Bacteriol 182: 818–820
Cho SH, Youn SH, Lee SR, Yim HS and Kang SO (2004) Redox property and regulation of PpsR, a transcriptional repressor of photosystem gene expression in Rhodobacter sphaeroides. Microbio 150: 697–706
Cohen-Bazire G, Sistrom WR and Stanier RY (1957) Kinetic studies of pigment synthesis by nonsulfur purple bacteria. J Cellular Comp Physiol 49: 25–68
Comolli JC and Donohue TJ (2002) Pseudomonas aeruginosa RoxR, are sponse regulator related to Rhodobacter sphaeroides PrrA, activates expression of the cyanide-insensitive terminal oxidase Mol Micro 45: 755–768
Dong C, Elsen S, Swem LR and Bauer CE (2002) AerR, a second aerobic repressor of photosynthesis gene expression in Rhodobacter capsulatus. J Bacteriol 184: 2805–2814
Du S, Bird TH and Bauer CE (1998) DNA binding characteristics of RegA. A constitutively active anaerobic activator of photosynthesis gene expression in Rhodobacter capsulatus. J Biol Chem 273: 18509–18513
Du S, Kouadio J-L K and Bauer CE (1999) Regulated expression of ahighly conserved regulatory gene cluster is necessary for controlling photosynthesis gene expression in response to anaerobiosis in Rhodobacter capsulatus. J Bacteriol 181: 4334–4341
Elsen S, Ponnampalam SN and Bauer CE (1998) CrtJ bound to distant binding sites interacts cooperatively to aerobically repress photopigment biosynthesis and light harvesting II gene expression in Rhodobacter capsulatus. J Biol Chem 273: 30762–30769
Elsen S, Dischert W, Colbeau A and Bauer CE (2000) Expression of uptake hydrogenase and molybdenum nitrogenase in Rhodobacter capsulatus is coregulated by the RegB-RegA two-component regulatory system. J Bact 182: 2831–2837
Elsen S, Swem LR, Swem DL and Bauer CE (2004) RegB/RegA, a highly conserved redox-responding global two-component regulatory system. Microbio Molec Biol Rev 68: 263–279
Elsen S, Jaubert M, Pignol D and Giraud F. (2005) PpsR: A multifaceted regulator of photosynthesis gene expression in purple bacteria. Mol Microbiol 57: 17–26
Emmerich R, Panglungtshang K, Strehler P, Hennecke H and Fischer H-M (1999) Phosphorylation, dephosphorylation and DNA-binding of the Bradyrhizobium japonicum RegSR two-component regulatory proteins. Eur J Biochem 263: 455–463
Emmerich R, Strehler P, Hennecke H and Fischer H-M (2000a) An imperfect inverted repeat is critical for DNA binding of the response regulator RegR of Bradyrhizobium japonicum. Nuc Acids Res 28: 4166–4171
Emmerich R, Hennecke H and Fischer H-M (2000b) Evidence for a functional similarity between the two-component regulatory systems RegSR, ActSR and RegBA (PrrBA) in α-proteobacteria. Arch Microbiol 174: 307–313
Eraso JM and Kaplan S (1994) prrA, a putative response regulator involved in oxygen regulation of photosynthesis gene expression in Rhodobacter sphaeroides. J Bacteriol 176: 32–43
Eraso JM and Kaplan S (1995) Oxygen-insensitive synthesis of the photosynthetic membranes of Rhodobacter sphaeroides: A mutant histidine kinase. J Bacteriol 177: 2695–2706
Eraso JM and Kaplan S (2000) From redox flow to gene regulation: Role of the PrrC protein of Rhodobacter sphaeroides 2.4.1. Biochem 39: 2052–2062
Giraud E, Fardoux J, Fourrier N, Hannibal L, Genty B, Bouyer P, Dreyfus B and Verméglio A (2002) Bacteriophytochrome controls photosystem synthesis in anoxygenic bacteria. Nature 417: 202–205
Giraud E, Zappa S, Jaubert M, Hannibal L, Fardoux J, Adriano JM, Bouyer P, Genty B, Pignol D and Verméglio A (2004) Bacteriophytochrome and regulation of the synthesis of the photosynthetic apparatus in Rhodopseudomonas palustris: Pitfalls of using laboratory strains. Photochem Photobiol Sci 3: 587–591
Gomelsky M and Kaplan S (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
Gomelsky M and Kaplan S (1995b). appA, a novel gene encoding a trans-acting factor involved in the regulation of photosynthesis gene expression in Rhodobacter sphaeroides. J Bacteriol 177: 4609–4618
Gomelsky M and Klug G (2002) BLUF: A novel FAD-binding domain involved in sensory transduction in microorganisms. Trends Biochem. Sci. 27: 497–500
Gomelsky M, Horne IM, Lee HJ, Pemberton JM, McEwan AG, Kaplan S (2000) Domain structure, oligomeric state, and mutational analysis of PpsR, the Rhodobacter sphaeroides repressor of photosystem gene expression. J Bacteriol 182: 2253–2261
Han Y, Meyer MH, Keusgen M, Klug G (2007) A haem cofactor is required for redox and light signalling by the AppA protein of Rhodobacter sphaeroides. Mol Microbiol 64: 1090–1104
Hemschemeier SK, Ebel U, Jager A, Balzer A, Kirndorfer M and Klug G (2000) In vivo and in vitro analysis of RegA response regulator mutants of Rhodobacter capsulatus. J Mol Microbiol Biotech 2: 291–300
Inoue K, Mosley C, Kouadio J-L and Bauer C (1995) Isolation and in vitro phosphorylation of sensory transduction components controlling anaerobic induction of light harvesting and reaction center gene expression in R. capsulatus. Biochemistry 34: 391–396
Jaubert M, Zappa S, Fardoux J, Adriano J M, Hannibal L, Elsen S, Lavergne J, Verméglio A, Giraud E and Pignol D (2004) Light and redox control of photosynthesis gene expression in Bradyrhizobium: Dual roles of two PpsR. J Biol Chem 279: 44407–44416
Jones DF, Stenzel RA and Donohue TJ (2005) Mutational analysis of the C-terminal domain of the Rhodobacter sphaeroides response regulator PrrA. Microbiol 151: 4103–4110
Joshi HM and Tabita FR (1996) A global two component signal transduction system that integrates the control of photosynthesis, carbon dioxide assimilation, and nitrogen fixation. Proc Natl Acad Sci USA 93: 14515–14520
Kaplan S, Eraso J and Roh JH (2005) Interacting regulatory networks in the facultative photosynthetic bacterium, Rhodobacter sphaeroides 2.4.1. Biochem Soc Trans 33: 51–55
Kim, SK, Mason, JT, Knaff, DB, Bauer, CE and Setterdahl, AT (2006) Redox properties of the Rhodobacter sphaeroides transcriptional regulatory proteins PpsR and AppA. Photosynth Res 89: 89–98
Kovacs AT, Rakhely G and Kovacs KL (2005) The PpsR regulator family. Res Microbiol 156: 619–625
Laguri C, Phillips-Jones MK and Williamson MP (2003) Solution structure and DNA binding of the effector domain from the global regulator PrrA (RegA) from Rhodobacter sphaeroides: Insights into DNA binding specificity. Nucl Acids Res 31: 6778–6787
Laguri C, Stenzel RA, Donohue TJ, Phillips-Jones MK and Williamson MP (2006) Activation of the global gene regulator PrrA (RegA) from Rhodobacter sphaeroides. Biochem 45: 7872–7881
Laratta WP, Choi PS, Tosques IE and Shapleigh JP (2002) Involvement of the PrrB/PrrA two-component system in nitrite respiration in Rhodobacter sphaeroides 2.4.1: Evidence for transcriptional regulation. J Bact 184: 3521–3529
Madigan MT (1995) The microbiology of nitrogen fixation by anoxygenic photosynthetic bacteria, In: Blankenship RE, Madigan MT and Bauer CE (ed) Anoxygenic Photosynthetic Bacteria (Advances in Photosynthesis and Respiration, Vol 2), pp 915–928. Kluwer Academic Publishing, Dordrecht
Madigan MT and Gest H (1979) Growth of the photosynthetic bacterium Rhodopseudomonas capsulata chemoautotrophically in darkness with H2 as the energy source. J Bacteriol 137: 524–530
Mao L, Mackenzie C, Roh JH, Eraso JM, Kaplan S and Resat H (2005) Combining microarray and genomic data to predict DNA binding motifs. Microbiology 151: 3197–3213
Masuda S and Bauer CE (2002) AppA is a blue light photoreceptor that antirepresses photosynthesis gene expression in Rhodobacter sphaeroides. Cell 110: 613–623
Masuda S and Bauer CE (2005) The antirepressor AppA uses the novel flavin-binding BLUF domain as blue-light-absorbing photoreceptor to control photosystem synthesis. In: Briggs W and Spudich J (eds) Handbook of Photosensory Receptors, pp 433–446. Wiley-VCH publishing, Weinheim
Masuda S, Matsumoto Y, Nagashima KVP, Shimada K, Inoue K, Bauer CE and Matsuura K (1999) Structural and functional analyses of photosynthetic regulatory genes regA and regB from Rhodovulum sulfidophilum, Roseobacter denitrificans, and Rhodobacter capsulatus. J Bacteriol 181: 4205–4215
Masuda S, Dong C, Swem D, Setterdahl AT, Knaff DB and Bauer CE (2002) Repression of photosynthesis gene expression by formation of a disulfide bond in CrtJ. Proc Natl Acad Sci USA 99: 7078–7083
McCleary WR and Stocks JB (1994) Acetyl phosphate and the activation of two-component response regulators. J Biol Chem 269: 31567–31572
Moskvin OV, Gomelsky L and Gomelsky M (2005) Transcriptome analysis of the Rhodobacter sphaeroides PpsR regulon: PpsR as a master regulator of photosystem development J Bacteriol 187: 2148–2156
Moskvin OV, Kaplan S, Gilles-Gonzalez MA and Gomelsky M (2007) Novel heme-based oxygen sensor with a revealing evolutionary history. J Biol Chem 282: 28740–28748
Mosley CS, Suzuki JY and Bauer CE (1994) Identification and molecular genetic characterization of a sensor kinase responsible for coordinately regulating light harvesting and reaction center gene expression in response to anaerobiosis. J Bacteriol 176: 7566–7573
Mouncey N J and Kaplan S (1998) Oxygen regulation of the ccoN gene encoding a component of the cbb 3 oxidase in Rhodobacter sphaeroides 2.4.1: Involvement of the FnrL protein. J Bacteriol 180: 2228–2231
Nowak E, Panjikar S, Konarev P, Svergun DI and Tucker PA (2006) The structural basis of signal transduction for the response regulator PrrA from Mycobacterium tuberculosis. J Biol Chem 281: 9659–9666
O’Gara JP and Kaplan S (1997) Evidence for the role of redox carriers in photosynthesis gene expression and carotenoid biosynthesis in Rhodobacter sphaeroides. 2.4.1. J Bacteriol 179: 1951–1961
Oh JI and Kaplan S (2000) Redox signaling: Globalization of gene expression EMBO J 19: 4237–4247
Ouchane S and Kaplan S (1999) Topological analysis of the membrane-localized redox-responsive sensor kinase PrrB from Rhodobacter sphaeroides 2.4.1. J Biol Chem 274: 17290–17296
Ouchane S, Picaud M, Therizols P, Reiss-Husson F and Astier C (2007) Global Regulation of Photosynthesis and Respiration by FnrL: The first two targets in the tetrapyrrole pathway. J Biol Chem 282: 7690–7699
Parkinson JS and Kofoid EC (1992) Communication modules in bacterial signaling proteins. Ann Rev Genet 26: 71–112
Parson W (1978) Quinones as secondary electron acceptor, In: RK Clayton and Sistrom WR (ed) The Photosynthetic Bacteria, pp 455–469. Plenum Press, New York
Penfold RJ and Pemberton JM (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
Pfenning N (1978) General physiology and ecology of photosynthetic bacteria, In: RK Clayton and Sistrom WR (ed) The Photosynthetic Bacteria, pp 1–18. Plenum Press, New York
Phillips-Jones MK and Hunter CN (1994) Cloning and nucleotide sequencing of RegA, a putative response regulator gene of Rhodobacter sphaeroides. FEMS Microbiol Lett 116: 269–275
Ponnampalam SN and Bauer CE (1997) DNA binding characteristics of CrtJ A redox-responding repressor of bacteriochlorophyll, carotenoid, and light harvesting-II gene expression in Rhodobacter capsulatus. J Biol Chem 272: 18391–18396
Ponnampalam SN, Buggy JJ, Bauer CE (1995) Characterization of an aerobic repressor that coordinately regulates bacteriochlorophyll, carotenoid, and light harvesting-II expression in Rhodobacter capsulatus. J Bacteriol 177: 2990–2997
Ponnampalam SN, Elsen S and Bauer CE (1998) Aerobic repression of the Rhodobacter capsulatus bchC promoter involves cooperative interactions between CrtJ bound to neighboring palindromes. J Biol Chem 273: 30757–30761
Potter CA, Ward A, Laguri C, Williamson MP, Henderson PJ and Phillips-Jones MK (2002) Expression, purification and characterization of full-length histidine protein kinase RegB from Rhodobacter sphaeroides. J Mol Biol 320: 201–213
Qian, Y and Tabita FR (1996) A global signal transduction system regulates aerobic and anaerobic CO2 fixation in Rhodobacter sphaeroides. J Bact 178: 12–18
Roh JH and Kaplan S (2000) Genetic and phenotypic analyses of the rdx locus of Rhodobacter sphaeroides 2.4.1. J Bacteriol 182: 3475–3481
Sganga MW and Bauer CE (1992) Regulatory factors controlling photosynthetic reaction center and light-harvesting gene expression in Rhodobacter capsulatus. Cell 68: 945–954
Smart JL, Willett JW and Bauer CE (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
Steunou AS, Astier C and Ouchane S (2004) Regulation of photosynthesis genes in Rubrivivax gelatinosus: Transcription factor PpsR is involved in both negative and positive control. J Bacteriol 186: 3133–3142
Swem DL and Bauer CE (2002) Coordination of ubiquinol oxidase and cytochrome cbb 3 oxidase expression by multiple regulators in Rhodobacter capsulatus. J Bacteriol 184: 2815–2820
Swem LR, Elsen S, Bird TH, Swem DL, Koch HG, Myllykallio H, Daldal F and Bauer CE (2001) The RegB/RegA two-component regulatory system controls synthesis of photosynthesis and respiratory electron transfer components in Rhodobacter capsulatus. J Mol Biol 309: 121–138
Swem LR, Kraft BJ, Swem DL, Setterdahl AT, Masuda S, Knaff DB, Zaleski JM and Bauer CE (2003) Signal transduction by the global regulator RegB is mediated by a redox-active cysteine. EMBO J 22: 4699–4708
Swem LR, Gong X, Yu CA and Bauer CE (2006) Identification of a ubiquinone-binding site that affects autophosphorylation of the sensor kinase RegB. J Biol Chem 281: 6768–6775
Tabita FR (1995) The biochemistry and metabolic regulation of carbon metabolism and CO2 fixation in purple bacteria. In: Blankenship RE, Madigan MT and Bauer CE (ed) Anoxygenic Photosynthetic Bacteria (Advances in Photosynthesis and Respiration, Vol 2), pp 885–914. Kluwer Academic Publishing, Dordrecht
Tiwari RP, Reeve WG, Dilworth MJ and Glenn AR (1996) Acid tolerance in Rhizobium meliloti strain WSM419 involves a two-component sensor-regulator system Microbiol 142: 1693–1704
Vichivanives P, Bird TH, Bauer CE and Tabita FR (2000) Multiple regulators and their interactions in vivo and in vitro with the cbb regulons of Rhodobacter capsulatus. J Mol Biol 300: 1079–1099
Willett J, Smart JL and Bauer CE (2007) RegA controls synthesis of bacteriochlorophyll and carotenoid photopigments in Rhodobacter capsulatus. J Bacteriol, In Press
Zeilstra-Ryalls JH, Gabbert K, Mouncey NJ, Kaplan S and Kranz RG (1997) Analysis of the fnrL gene and its function in Rhodobacter capsulatus. J Bacteriol 179: 7264–7273
Zeilstra-Ryalls JH and Kaplan S (1995) Aerobic and anaerobic regulation in Rhodobacter sphaeroides 2.4.1: The role of the fiirL gene. J Bacteriol 177: 6422–6431
Zeilstra-Ryalls JH and Kaplan S (1998) Role of the fnrL gene in photosystem gene expression and photosynthetic growth of Rhodobacter sphaeroides 2.4.1. J Bacteriol 180: 1496–1503
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2009 Springer Science + Business Media B.V
About this chapter
Cite this chapter
Bauer, C.E., Setterdahl, A., Wu, J., Robinson, B.R. (2009). Regulation of Gene Expression in Response to Oxygen Tension. In: Hunter, C.N., Daldal, F., Thurnauer, M.C., Beatty, J.T. (eds) The Purple Phototrophic Bacteria. Advances in Photosynthesis and Respiration, vol 28. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-8815-5_35
Download citation
DOI: https://doi.org/10.1007/978-1-4020-8815-5_35
Publisher Name: Springer, Dordrecht
Print ISBN: 978-1-4020-8814-8
Online ISBN: 978-1-4020-8815-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)