Abstract
The crtEF, bchCA, and puf operons of the facultative phototrophic bacterium Rhodobacter capsulatus encode gene products that are necessary for the formation of various components of the photosynthetic apparatus. The crtEF operon encodes two enzymes involved in the biosynthesis of carotenoids, the bchCA operon codes for two enzymes of the bacteriochlorophyll biosynthetic pathway, and the puf operon encodes four pigment-binding polypeptides as well as two polypeptides with less well understood functions. These three operons are adjacent to one another on the chromosome and are transcribed in the same direction. We present the results of RNA blotting and S1 nuclease protection end-mapping experiments which provide direct evidence that the mRNA transcripts of these three operons overlap. Therefore, it is likely that the crtEF, bchCA, and puf operons can be expressed as a single transcriptional unit, although RNA polymerase may initiate transcription at any of several promoters.
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- Adams C. W., Forrest M. E., Cohen S. N., Beatty J. T. Structural and functional analysis of transcriptional control of the Rhodobacter capsulatus puf operon. J Bacteriol. 1989 Jan;171(1):473–482. doi: 10.1128/jb.171.1.473-482.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Armstrong G. A., Alberti M., Leach F., Hearst J. E. Nucleotide sequence, organization, and nature of the protein products of the carotenoid biosynthesis gene cluster of Rhodobacter capsulatus. Mol Gen Genet. 1989 Apr;216(2-3):254–268. doi: 10.1007/BF00334364. [DOI] [PubMed] [Google Scholar]
- Bauer C. E., Marrs B. L. Rhodobacter capsulatus puf operon encodes a regulatory protein (PufQ) for bacteriochlorophyll biosynthesis. Proc Natl Acad Sci U S A. 1988 Oct;85(19):7074–7078. doi: 10.1073/pnas.85.19.7074. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bauer C. E., Young D. A., Marrs B. L. Analysis of the Rhodobacter capsulatus puf operon. Location of the oxygen-regulated promoter region and the identification of an additional puf-encoded gene. J Biol Chem. 1988 Apr 5;263(10):4820–4827. [PubMed] [Google Scholar]
- Beatty J. T., Cohen S. N. Hybridization of cloned Rhodopseudomonas capsulata photosynthesis genes with DNA from other photosynthetic bacteria. J Bacteriol. 1983 Jun;154(3):1440–1445. doi: 10.1128/jb.154.3.1440-1445.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Chen C. Y., Beatty J. T., Cohen S. N., Belasco J. G. An intercistronic stem-loop structure functions as an mRNA decay terminator necessary but insufficient for puf mRNA stability. Cell. 1988 Feb 26;52(4):609–619. doi: 10.1016/0092-8674(88)90473-4. [DOI] [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]
- De Reuse H., Danchin A. The ptsH, ptsI, and crr genes of the Escherichia coli phosphoenolpyruvate-dependent phosphotransferase system: a complex operon with several modes of transcription. J Bacteriol. 1988 Sep;170(9):3827–3837. doi: 10.1128/jb.170.9.3827-3837.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Farchaus J. W., Gruenberg H., Oesterhelt D. Complementation of a reaction center-deficient Rhodobacter sphaeroides pufLMX deletion strain in trans with pufBALM does not restore the photosynthesis-positive phenotype. J Bacteriol. 1990 Feb;172(2):977–985. doi: 10.1128/jb.172.2.977-985.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
- Grundström T., Jaurin B. Overlap between ampC and frd operons on the Escherichia coli chromosome. Proc Natl Acad Sci U S A. 1982 Feb;79(4):1111–1115. doi: 10.1073/pnas.79.4.1111. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Holloway B. W., Morgan A. F. Genome organization in Pseudomonas. Annu Rev Microbiol. 1986;40:79–105. doi: 10.1146/annurev.mi.40.100186.000455. [DOI] [PubMed] [Google Scholar]
- Jaurin B., Grundström T., Edlund T., Normark S. The E. coli beta-lactamase attenuator mediates growth rate-dependent regulation. Nature. 1981 Mar 19;290(5803):221–225. doi: 10.1038/290221a0. [DOI] [PubMed] [Google Scholar]
- Johnson J. A., Wong W. K., Beatty J. T. Expression of cellulase genes in Rhodobacter capsulatus by use of plasmid expression vectors. J Bacteriol. 1986 Aug;167(2):604–610. doi: 10.1128/jb.167.2.604-610.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kiley P. J., Kaplan S. Molecular genetics of photosynthetic membrane biosynthesis in Rhodobacter sphaeroides. Microbiol Rev. 1988 Mar;52(1):50–69. doi: 10.1128/mr.52.1.50-69.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
- Leidigh B. J., Wheelis M. L. The clustering on the Pseudomonas putida chromosome of genes specifying dissimilatory functions. J Mol Evol. 1973 Nov 27;2(4):235–242. doi: 10.1007/BF01654092. [DOI] [PubMed] [Google Scholar]
- Roberts J. W. Phage lambda and the regulation of transcription termination. Cell. 1988 Jan 15;52(1):5–6. doi: 10.1016/0092-8674(88)90523-5. [DOI] [PubMed] [Google Scholar]
- Schmidhauser T. J., Helinski D. R. Regions of broad-host-range plasmid RK2 involved in replication and stable maintenance in nine species of gram-negative bacteria. J Bacteriol. 1985 Oct;164(1):446–455. doi: 10.1128/jb.164.1.446-455.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schumacher A., Drews G. Effects of light intensity on membrane differentiation in Rhodopseudomonas capsulata. Biochim Biophys Acta. 1979 Sep 11;547(3):417–428. doi: 10.1016/0005-2728(79)90022-7. [DOI] [PubMed] [Google Scholar]
- Schumacher A., Drews G. The formation of bacteriochlorophyll.protein complexes of the photosynthetic apparatus of Rhodopseudomonas capsulata during early stages of development. Biochim Biophys Acta. 1978 Feb 9;501(2):183–194. doi: 10.1016/0005-2728(78)90025-7. [DOI] [PubMed] [Google Scholar]
- Scolnik P. A., Marrs B. L. Genetic research with photosynthetic bacteria. Annu Rev Microbiol. 1987;41:703–726. doi: 10.1146/annurev.mi.41.100187.003415. [DOI] [PubMed] [Google Scholar]
- Scolnik P. A., Zannoni D., Marrs B. L. Spectral and functional comparisons between the carotenoids of the two antenna complexes of Rhodopseudomonas capsulata. Biochim Biophys Acta. 1980 Dec 3;593(2):230–240. doi: 10.1016/0005-2728(80)90061-4. [DOI] [PubMed] [Google Scholar]
- Sockett R. E., Donohue T. J., Varga A. R., Kaplan S. Control of photosynthetic membrane assembly in Rhodobacter sphaeroides mediated by puhA and flanking sequences. J Bacteriol. 1989 Jan;171(1):436–446. doi: 10.1128/jb.171.1.436-446.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Solioz M., Marrs B. The gene transfer agent of Rhodopseudomonas capsulata. Purification and characterization of its nucleic acid. Arch Biochem Biophys. 1977 May;181(1):300–307. doi: 10.1016/0003-9861(77)90508-2. [DOI] [PubMed] [Google Scholar]
- Taylor D. P., Cohen S. N., Clark W. G., Marrs B. L. Alignment of genetic and restriction maps of the photosynthesis region of the Rhodopseudomonas capsulata chromosome by a conjugation-mediated marker rescue technique. J Bacteriol. 1983 May;154(2):580–590. doi: 10.1128/jb.154.2.580-590.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tichy H. V., Oberlé B., Stiehle H., Schiltz E., Drews G. Genes downstream from pucB and pucA are essential for formation of the B800-850 complex of Rhodobacter capsulatus. J Bacteriol. 1989 Sep;171(9):4914–4922. doi: 10.1128/jb.171.9.4914-4922.1989. [DOI] [PMC free article] [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]
- Wellington C. L., Beatty J. T. Promoter mapping and nucleotide sequence of the bchC bacteriochlorophyll biosynthesis gene from Rhodobacter capsulatus. Gene. 1989 Nov 30;83(2):251–261. doi: 10.1016/0378-1119(89)90111-x. [DOI] [PubMed] [Google Scholar]
- Wheelis L. The genetics of dissimilarity pathways in Pseudomonas. Annu Rev Microbiol. 1975;29:505–524. doi: 10.1146/annurev.mi.29.100175.002445. [DOI] [PubMed] [Google Scholar]
- Yen H. C., Marrs B. Map of genes for carotenoid and bacteriochlorophyll biosynthesis in Rhodopseudomonas capsulata. J Bacteriol. 1976 May;126(2):619–629. doi: 10.1128/jb.126.2.619-629.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Young D. A., Bauer C. E., Williams J. C., Marrs B. L. Genetic evidence for superoperonal organization of genes for photosynthetic pigments and pigment-binding proteins in Rhodobacter capsulatus. Mol Gen Genet. 1989 Jul;218(1):1–12. doi: 10.1007/BF00330558. [DOI] [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]
- Youvan D. C., Ismail S. Light-harvesting II (B800-B850 complex) structural genes from Rhodopseudomonas capsulata. Proc Natl Acad Sci U S A. 1985 Jan;82(1):58–62. doi: 10.1073/pnas.82.1.58. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zucconi A. P., Beatty J. T. Posttranscriptional regulation by light of the steady-state levels of mature B800-850 light-harvesting complexes in Rhodobacter capsulatus. J Bacteriol. 1988 Feb;170(2):877–882. doi: 10.1128/jb.170.2.877-882.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- von Gabain A., Belasco J. G., Schottel J. L., Chang A. C., Cohen S. N. Decay of mRNA in Escherichia coli: investigation of the fate of specific segments of transcripts. Proc Natl Acad Sci U S A. 1983 Feb;80(3):653–657. doi: 10.1073/pnas.80.3.653. [DOI] [PMC free article] [PubMed] [Google Scholar]