Abstract
Genes coding for putative CrtJ and AerR homologs were identified and characterized in the purple photosynthetic bacterium Rhodospirillum centenum (also known as Rhodocista centenaria), an organism that synthesizes photopigments even under highly aerated conditions. Mutational analysis indicated that in Rsp. centenum, genecrtJ codes for a repressor for photosynthesisgene expression as in Rhodobactercapsulatus, which exhibits a high level of oxygen repression of photosystem synthesis. In contrast to Rba. capsulatus, AerR in Rsp. centenum appears to be an aerobic activator; an aerR mutation resulted in significantly reduced levels of photopigment synthesis. Both aerR and crtJ mutants retained essentially normal levels of photosystem synthesis under anaerobic conditions, indicating that their activities are specific for aerobic photosystem synthesis. The readthrough transcript from crtE promoter, which is regulated by AerR and CrtJ, seems to be significant in maintaining the expression levels of the light harvesting I (puf) genes in Rsp. centenum. We suggest that AerR and CrtJ regulate aerobic photosystem synthesis primarily through controlling activity of the transcriptional readthrough.
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C. E. Bauer, S. Elsen, L. R. Swem, D. L. Swem and S., Masuda, Redox and light regulation of gene expression in photosynthetic prokaryotes Philos. Trans. R. Soc. London, Ser. B 2003 358 147–153
J. H. Zeilstra-Ryalls and S., Kaplan, Oxygen intervention in the regulation of gene expression: the photosynthetic bacterial paradigm Cell Mol. Life Sci. 2004 61 417–436
M. Doi, Y. Shioi, N. Gad’on, J. R. Golecki and G., Drews, Spectroscopical studies on the light-harvesting pigment-protein complex II from dark-aerobic and light-anaerobic grown cells of Rhodobacter sulfidophilus Biochim. Biophys. Acta 1991 1058 235–241
F. H. Yildiz, H. Gest and C. E., Bauer, Attenuated effect of oxygen on photopigment synthesis in Rhodospirillum centenum J. Bacteriol. 1991 173 5502–5506
G. E. Hagemann, E. K. Katsiou, H. Forkl, A. C. J. Steindorf and M. H., Tadros, Gene cloning and regulation of gene expression of the puc operon from Rhodovulum sulfidophilum Biochim. Biophys. Acta 1997 1351 341–358
S. Masuda, K. V. P. Nagashima, K. Shimada and K., Matsuura, Transcriptional control of expression of genes for photosynthetic reaction center and light-harvesting proteins in the purple bacterium Rhodovulum sulfidophilum J. Bacteriol. 2000 182 2778–2786
R. J. Penfold and J. M., Pemberton, Sequencing, chromosomal inactivation, and functional expression of ppsR a gene which represses carotenoid and bacteriochlorophyll synthesis in Rhodobacter sphaeroides J. Bacteriol. 1994 176 2869–2876
S. N. Ponnampalam, J. J. Buggy and C. E., Bauer, Characterization of an aerobic repressor that coordinately regulates bacteriochlorophyll, carotenoid, and light-harvesting-II expression in Rhodobacter capsulatus J. Bacteriol. 1995 177 2990–2997
C. Dong, S. Elsen, L. R. Swen and C. E., Bauer, AerR, a second aerobic repressor of photosynthesis gene expression in Rhodobacter capsulatus J. Bacteriol. 2002 184 2805–2814
L. Gomelsky, J. Sram, O. V. Moskvin, I. M. Horne, H. N. Dodd, J. M. Pemberton, A. G. McEwan, S. Kaplan and M., Gomelsky, Identification and in vivo characterization of PpaA, a regulator of photosystem formation in Rhodobacter sphaeroides Microbiology 2003 149 377–388
S. N. Ponnampalam and C. E., Bauer, DNA binding characteristics of CrtJ J. Biol. Chem. 1997 272 18391–18396
S. Masuda, C. Dong, D. Swem, A. T. Setterdahl, D. B. Knaff and C. E., Bauer, Repression of photosynthesis gene expression by formation of a disulfide bond in CrtJ Proc. Natl. Acad. Sci. USA 2002 99 7078–7083
S. Masuda and C. E., Bauer, AppA is a blue light photoreceptor that antirepresses photosynthesis gene expression in Rhodobacter sphaeroides Cell 2002 110 613–623
N. Igarashi, J. Harada, S. Nagashima, K. Matsuura, K. Shimada and K. V. P., Nagashima, Horizontal transfer of the photosynthesis gene cluster and operon rearrangement in purple bacteria J. Mol. Evol. 2001 52 333–341
E. Giraud, J. Fardoux, N. Fourrier, L. Hannibal, B. Genty, P. Bouyer, B. Dreyfus, A. Verméglio Bacteriophytochrome controls photosystem synthesis in anoxygenic bacteria Nature 2002 417 202–205
A. -S. Steunou, C. Astier and S., Ouchane, Regulation of photosynthesis genes in Rubrivivax gelatinosus: transcription factor PpsR is involved in both negative and positive control J. Bacteriol. 2004 186 3133–3142
S. Elsen, M. Jaubert, D. Pignol and E., Giraud, PpsR: a multifaceted regulator of photosynthesis gene expression in purple bacteria Mol. Microbiol. 2005 57 17–26
Á. T. Kovács, G. Rákhely, K. L. Kovács The PpsR regulator family Res. Microbiol. 2005 156 619–625
R. Stadtwald-Demchick, F. R. Turner and H., Gest, Physiological properties of the thermotolerant photosynthetic bacterium Rhodospirillum centenum FEMS Microbiol. Lett. 1990 67 139–144
R. Simon, U. Priefer and A., Puhler, A broad host range mobilization system for in vivo genetic engineering; transposon mutagenesis in Gram negative bacteria Biotechnology 1983 1 37–45
S. Masuda and C. E., Bauer, Null mutation of HvrA compensates for loss of an essential relA/spoT-like gene in Rhodobacter capsulatus J. Bacteriol. 2004 186 235–239
P. Gay, D. LeCoq, M. Steinmetz, T. Berkelman and C. I., Kado, Positive selection procedure for entrapment of insertion sequence elements in gram-negative bacteria J. Bacteriol. 1985 164 918–921
L. K. Lee and S., Kaplan, Transcriptional regulation of puc operon expression in Rhodobacter sphaeroides J. Biol. Chem. 1995 270 20453–20458
D. A. Young, C. E. Bauer, J. C. Williams and B. L., Marrs, Genetic evidence for superoperonal organization of genes for photosynthetic pigments and pigment binding proteins in Rhodobacter capsulatus Mol. Gen. Genet. 1989 218 1–12
J. F. Imhoff, Taxonomy and physiology of phototrophic purple bacteria and green sulfur bacteria in Anoxygenic Photosynthetic Bacteria, ed. R. E. Blankenship, M. T. Madigan and C. E. Bauer, Kluwer Academic Publishers, Dordrecht, The Netherlands, 1995, pp. 1-15
E. Giraud, A. Verméglio Bacteriophytochromes in anoxygenic photosynthetic bacteria Photosynth. Res. 2008 97 141–153
S. N. Ponnampalam, S. Elsen and C. E., Bauer, Aerobic repression of the Rhodobacter capsulatus bchC promoter involves cooperative interactions between CrtJ bound to neighboring palindromes J. Biol. Chem. 1998 273 30757–30761
S. Elsen, S. N. Ponnampalam and C. E., Bauer, 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. 1998 273 30762–30769
C. L. Wellington and J. T., Beatty, Overlapping mRNA transcripts of photosynthesis gene operons in Rhodobacter capsulatus J. Bacteriol. 1991 173 1432–1443
C. L. Wellington, A. K. P. Taggart and J. T., Beatty, Functional significance of overlapping transcrips of crtEF, bchCA, and puf photosynthesis gene operons in Rhodobacter capsulatus J. Bacteriol. 1991 173 2954–2961
S. Liotenberg, A. -S. Steunou, M. Picaud, F. Reiss-Husson, C. Astier and S., Ouchane, Organization and expression of photosynthesis genes and operons in anoxygenic photosynthetic proteobacteria Environ. Microbiol. 2008 10 2267–2276
F. H. Yildiz, H. Gest and C. E., Bauer, Conservation of the photosynthetic gene cluster in Rhodospirillum centenum Mol. Microbiol. 1992 6 2683–2691
G. W. Naylor, H. A. Addlesee, L. C. D. Gibson and C. N., Hunter, The photosynthesis gene cluster of Rhodobacter sphaeroides Photosynth. Res. 1999 62 121–139
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This paper was published as part of the themed issue of contributions from the 7th International Conference on Tetrapyrrole Photoreceptors in Photosynthetic Organisms held in Kyoto, December 2007.
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Masuda, S., Berleman, J., Hasselbring, B.M. et al. Regulation of aerobic photosystem synthesis in the purple bacterium Rhodospirillum centenum by CrtJ and AerR. Photochem Photobiol Sci 7, 1267–1272 (2008). https://doi.org/10.1039/b802365b
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DOI: https://doi.org/10.1039/b802365b