Abstract
The regulation of the photosynthetic genes by DNA supercoiling in Rhodobacter capsulatus has been studied by using gyrase inhibitors in vivo and by measurement of mRNA levels of more than a dozen genes. The results demonstrate that the levels of mRNA for light-harvesting (I, II) and reaction center (L, M, H) proteins, bacteriochlorophyll biosynthetic enzymes, ribulose-bisphosphate carboxylase (EC 4.1.1.39), and the mRNAs from the open reading frames Q and R decreased immediately and dramatically upon addition of novobiocin and coumermycin. In contrast, the mRNAs for carotenoid biosynthetic enzymes, the cytochrome bc1 complex, and constitutively expressed mRNA under aerobic conditions for light-harvesting I and for reaction center (L, M) proteins are less sensitive to the inhibitors. In accordance with these results, the biosynthesis of bacteriochlorophyll is markedly repressed by gyrase inhibitors novobiocin, coumermycin, nalidixic acid, and oxolinic acid either under anaerobic conditions or during a shift from aerobic to anaerobic conditions. The synthesis of light-harvesting (I, II) bacteriochlorophyll complexes is also inhibited by novobiocin and coumermycin. The kinetics of specific mRNA changes and the differential sensitivity of anaerobic and aerobic genes to the gyrase inhibitors strongly suggest that DNA supercoiling is involved in the differential expression of photosynthetic genes in response to the level of oxygen in R. capsulatus.
Full text
PDF




Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Belasco J. G., Beatty J. T., Adams C. W., von Gabain A., Cohen S. N. Differential expression of photosynthesis genes in R. capsulata results from segmental differences in stability within the polycistronic rxcA transcript. Cell. 1985 Jan;40(1):171–181. doi: 10.1016/0092-8674(85)90320-4. [DOI] [PubMed] [Google Scholar]
- Biel A. J., Marrs B. L. Transcriptional regulation of several genes for bacteriochlorophyll biosynthesis in Rhodopseudomonas capsulata in response to oxygen. J Bacteriol. 1983 Nov;156(2):686–694. doi: 10.1128/jb.156.2.686-694.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- COHEN-BAZIRE G., SISTROM W. R., STANIER R. Y. Kinetic studies of pigment synthesis by non-sulfur purple bacteria. J Cell Physiol. 1957 Feb;49(1):25–68. doi: 10.1002/jcp.1030490104. [DOI] [PubMed] [Google Scholar]
- Chory J., Kaplan S. The in vitro transcription-translation of DNA and RNA templates by extracts of Rhodopseudomonas sphaeroides. Optimization and comparison of template specificity with Escherichia coli extracts and in vivo synthesis. J Biol Chem. 1982 Dec 25;257(24):15110–15121. [PubMed] [Google Scholar]
- Clark W. G., Davidson E., Marrs B. L. Variation of levels of mRNA coding for antenna and reaction center polypeptides in Rhodopseudomonas capsulata in response to changes in oxygen concentration. J Bacteriol. 1984 Mar;157(3):945–948. doi: 10.1128/jb.157.3.945-948.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Drews G., Oelze J. Organization and differentiation of membranes of phototrophic bacteria. Adv Microb Physiol. 1981;22:1–92. doi: 10.1016/s0065-2911(08)60325-2. [DOI] [PubMed] [Google Scholar]
- Gabellini N., Harnisch U., McCarthy J. E., Hauska G., Sebald W. Cloning and expression of the fbc operon encoding the FeS protein, cytochrome b and cytochrome c1 from the Rhodopseudomonas sphaeroides b/c1 complex. EMBO J. 1985 Feb;4(2):549–553. doi: 10.1002/j.1460-2075.1985.tb03663.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gellert M. DNA topoisomerases. Annu Rev Biochem. 1981;50:879–910. doi: 10.1146/annurev.bi.50.070181.004311. [DOI] [PubMed] [Google Scholar]
- Gorchein A. Control of magnesium-protoporphyrin chelatase activity in Rhodopseudomonas spheroides. Role of light, oxygen, and electron and energy transfer. Biochem J. 1973 Aug;134(4):833–845. doi: 10.1042/bj1340833d. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Klug G., Kaufmann N., Drews G. Gene expression of pigment-binding proteins of the bacterial photosynthetic apparatus: Transcription and assembly in the membrane of Rhodopseudomonas capsulata. Proc Natl Acad Sci U S A. 1985 Oct;82(19):6485–6489. doi: 10.1073/pnas.82.19.6485. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kranz R. G., Haselkorn R. Anaerobic regulation of nitrogen-fixation genes in Rhodopseudomonas capsulata. Proc Natl Acad Sci U S A. 1986 Sep;83(18):6805–6809. doi: 10.1073/pnas.83.18.6805. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lascelles J. The regulation of heme and chlorophyll synthesis in bacteria. Ann N Y Acad Sci. 1975 Apr 15;244:334–347. doi: 10.1111/j.1749-6632.1975.tb41540.x. [DOI] [PubMed] [Google Scholar]
- Marrs B., Gest H. Regulation of bacteriochlorophyll synthesis by oxygen in respiratory mutants of Rhodopseudomonas capsulata. J Bacteriol. 1973 Jun;114(3):1052–1057. doi: 10.1128/jb.114.3.1052-1057.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Menzel R., Gellert M. Modulation of transcription by DNA supercoiling: a deletion analysis of the Escherichia coli gyrA and gyrB promoters. Proc Natl Acad Sci U S A. 1987 Jun;84(12):4185–4189. doi: 10.1073/pnas.84.12.4185. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Menzel R., Gellert M. Regulation of the genes for E. coli DNA gyrase: homeostatic control of DNA supercoiling. Cell. 1983 Aug;34(1):105–113. doi: 10.1016/0092-8674(83)90140-x. [DOI] [PubMed] [Google Scholar]
- Muller E. D., Chory J., Kaplan S. Cloning and characterization of the gene product of the form II ribulose-1,5-bisphosphate carboxylase gene of Rhodopseudomonas sphaeroides. J Bacteriol. 1985 Jan;161(1):469–472. doi: 10.1128/jb.161.1.469-472.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Novak P. D., Maier R. J. Inhibition of hydrogenase synthesis by DNA gyrase inhibitors in Bradyrhizobium japonicum. J Bacteriol. 1987 Jun;169(6):2708–2712. doi: 10.1128/jb.169.6.2708-2712.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Otter R., Cozzarelli N. R. Escherichia coli DNA gyrase. Methods Enzymol. 1983;100:171–180. doi: 10.1016/0076-6879(83)00053-1. [DOI] [PubMed] [Google Scholar]
- Smith G. R. DNA supercoiling: another level for regulating gene expression. Cell. 1981 Jun;24(3):599–600. doi: 10.1016/0092-8674(81)90085-4. [DOI] [PubMed] [Google Scholar]
- Stirdivant S. M., Crossland L. D., Bogorad L. DNA supercoiling affects in vitro transcription of two maize chloroplast genes differently. Proc Natl Acad Sci U S A. 1985 Aug;82(15):4886–4890. doi: 10.1073/pnas.82.15.4886. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thompson R. J., Mosig G. Stimulation of a Chlamydomonas chloroplast promoter by novobiocin in situ and in E. coli implies regulation by torsional stress in the chloroplast DNA. Cell. 1987 Jan 30;48(2):281–287. doi: 10.1016/0092-8674(87)90431-4. [DOI] [PubMed] [Google Scholar]
- Wang J. C. DNA topoisomerases. Annu Rev Biochem. 1985;54:665–697. doi: 10.1146/annurev.bi.54.070185.003313. [DOI] [PubMed] [Google Scholar]
- Weaver P. F., Wall J. D., Gest H. Characterization of Rhodopseudomonas capsulata. Arch Microbiol. 1975 Nov 7;105(3):207–216. doi: 10.1007/BF00447139. [DOI] [PubMed] [Google Scholar]
- Yamamoto N., Droffner M. L. Mechanisms determining aerobic or anaerobic growth in the facultative anaerobe Salmonella typhimurium. Proc Natl Acad Sci U S A. 1985 Apr;82(7):2077–2081. doi: 10.1073/pnas.82.7.2077. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Youvan D. C., Bylina E. J., Alberti M., Begusch H., Hearst J. E. Nucleotide and deduced polypeptide sequences of the photosynthetic reaction-center, B870 antenna, and flanking polypeptides from R. capsulata. Cell. 1984 Jul;37(3):949–957. doi: 10.1016/0092-8674(84)90429-x. [DOI] [PubMed] [Google Scholar]
- Zhu Y. S., Cook D. N., Leach F., Armstrong G. A., Alberti M., Hearst J. E. Oxygen-regulated mRNAs for light-harvesting and reaction center complexes and for bacteriochlorophyll and carotenoid biosynthesis in Rhodobacter capsulatus during the shift from anaerobic to aerobic growth. J Bacteriol. 1986 Dec;168(3):1180–1188. doi: 10.1128/jb.168.3.1180-1188.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhu Y. S., Hearst J. E. Regulation of expression of genes for light-harvesting antenna proteins LH-I and LH-II; reaction center polypeptides RC-L, RC-M, and RC-H; and enzymes of bacteriochlorophyll and carotenoid biosynthesis in Rhodobacter capsulatus by light and oxygen. Proc Natl Acad Sci U S A. 1986 Oct;83(20):7613–7617. doi: 10.1073/pnas.83.20.7613. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhu Y. S., Kaplan S. 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. 1985 Jun;162(3):925–932. doi: 10.1128/jb.162.3.925-932.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhu Y. S., Kiley P. J., Donohue T. J., Kaplan S. Origin of the mRNA stoichiometry of the puf operon in Rhodobacter sphaeroides. J Biol Chem. 1986 Aug 5;261(22):10366–10374. [PubMed] [Google Scholar]