• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of jbacterPermissionsJournals.ASM.orgJournalJB ArticleJournal InfoAuthorsReviewers
J Bacteriol. Jan 1989; 171(1): 473–482.
PMCID: PMC209611

Structural and functional analysis of transcriptional control of the Rhodobacter capsulatus puf operon.

Abstract

We report data indicating that the Rhodobacter capsulatus puf operon promoter and the site for its oxygen regulation are located more than 700 base pairs upstream from the previously identified puf genes and have identified the nucleotide sequences that constitute these control signals. A model is proposed in which a polycistronic transcript at least 3.4 kilobases in length is initiated near the O2-regulated promoter and is processed posttranscriptionally by endonucleolytic cleavage at multiple sites, yielding discrete mRNA segments that are degraded at different rates. A newly identified gene (pufQ), which includes a hydrophobic domain having some similarity to domains of the products of the pufL and pufM genes, begins 313 nucleotides into the puf transcript and is located entirely within the most rapidly degraded segment of the transcript. A previously identified puf transcript segment encoding structural proteins for photosynthetic membrane complexes persists after degradation of the most 5' region of the transcript and is itself subject to segmentally specific degradation. Our results suggest a model in which differential expression of the multiple genes encoded by the puf operon is at least in part attributable to major differences in the rates of decay of the various segments of puf mRNA.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (2.4M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Images in this article

Click on the image to see a larger version.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Aliabadi Z, Warren F, Mya S, Foster JW. Oxygen-regulated stimulons of Salmonella typhimurium identified by Mu d(Ap lac) operon fusions. J Bacteriol. 1986 Mar;165(3):780–786. [PMC free article] [PubMed]
  • Allen JP, Feher G, Yeates TO, Rees DC, Deisenhofer J, Michel H, Huber R. Structural homology of reaction centers from Rhodopseudomonas sphaeroides and Rhodopseudomonas viridis as determined by x-ray diffraction. Proc Natl Acad Sci U S A. 1986 Nov;83(22):8589–8593. [PMC free article] [PubMed]
  • Bauer CE, Marrs BL. 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. [PMC free article] [PubMed]
  • Bauer CE, Young DA, Marrs BL. 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]
  • Beck E, Bremer E. Nucleotide sequence of the gene ompA coding the outer membrane protein II of Escherichia coli K-12. Nucleic Acids Res. 1980 Jul 11;8(13):3011–3027. [PMC free article] [PubMed]
  • Belasco JG, Beatty JT, Adams CW, von Gabain A, Cohen SN. 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. [PubMed]
  • Berk AJ, Sharp PA. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell. 1977 Nov;12(3):721–732. [PubMed]
  • Cannon M, Hill S, Kavanaugh E, Cannon F. A molecular genetic study of nif expression in Klebsiella pneumoniae at the level of transcription, translation and nitrogenase activity. Mol Gen Genet. 1985;198(2):198–206. [PubMed]
  • Chen CY, Beatty JT, Cohen SN, Belasco JG. 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. [PubMed]
  • Clark WG, Davidson E, Marrs BL. 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. [PMC free article] [PubMed]
  • COHEN-BAZIRE G, SISTROM WR, STANIER RY. Kinetic studies of pigment synthesis by non-sulfur purple bacteria. J Cell Physiol. 1957 Feb;49(1):25–68. [PubMed]
  • Davidson E, Daldal F. Primary structure of the bc1 complex of Rhodopseudomonas capsulata. Nucleotide sequence of the pet operon encoding the Rieske cytochrome b, and cytochrome c1 apoproteins. J Mol Biol. 1987 May 5;195(1):13–24. [PubMed]
  • Drews G, Oelze J. Organization and differentiation of membranes of phototrophic bacteria. Adv Microb Physiol. 1981;22:1–92. [PubMed]
  • Hawley DK, McClure WR. Compilation and analysis of Escherichia coli promoter DNA sequences. Nucleic Acids Res. 1983 Apr 25;11(8):2237–2255. [PMC free article] [PubMed]
  • Henikoff S. Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene. 1984 Jun;28(3):351–359. [PubMed]
  • Hui A, Hayflick J, Dinkelspiel K, de Boer HA. Mutagenesis of the three bases preceding the start codon of the beta-galactosidase mRNA and its effect on translation in Escherichia coli. EMBO J. 1984 Mar;3(3):623–629. [PMC free article] [PubMed]
  • Johnson JA, Wong WK, Beatty JT. Expression of cellulase genes in Rhodobacter capsulatus by use of plasmid expression vectors. J Bacteriol. 1986 Aug;167(2):604–610. [PMC free article] [PubMed]
  • Klug G, Adams CW, Belasco J, Doerge B, Cohen SN. Biological consequences of segmental alterations in mRNA stability: effects of deletion of the intercistronic hairpin loop region of the Rhodobacter capsulatus puf operon. EMBO J. 1987 Nov;6(11):3515–3520. [PMC free article] [PubMed]
  • Kranz RG, Haselkorn R. Anaerobic regulation of nitrogen-fixation genes in Rhodopseudomonas capsulata. Proc Natl Acad Sci U S A. 1986 Sep;83(18):6805–6809. [PMC free article] [PubMed]
  • Kunkel TA. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc Natl Acad Sci U S A. 1985 Jan;82(2):488–492. [PMC free article] [PubMed]
  • Marrs B. Genetic recombination in Rhodopseudomonas capsulata. Proc Natl Acad Sci U S A. 1974 Mar;71(3):971–973. [PMC free article] [PubMed]
  • Maxam AM, Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. [PubMed]
  • Messing J. New M13 vectors for cloning. Methods Enzymol. 1983;101:20–78. [PubMed]
  • Moss B. 5' end labeling of RNA with capping and methylating enzymes. Gene Amplif Anal. 1981;2:253–266. [PubMed]
  • Prentki P, Krisch HM. In vitro insertional mutagenesis with a selectable DNA fragment. Gene. 1984 Sep;29(3):303–313. [PubMed]
  • Schmidhauser TJ, Helinski DR. 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. [PMC free article] [PubMed]
  • Shaw DJ, Rice DW, Guest JR. Homology between CAP and Fnr, a regulator of anaerobic respiration in Escherichia coli. J Mol Biol. 1983 May 15;166(2):241–247. [PubMed]
  • Smith AJ. DNA sequence analysis by primed synthesis. Methods Enzymol. 1980;65(1):560–580. [PubMed]
  • von Gabain A, Belasco JG, Schottel JL, Chang AC, Cohen SN. 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. [PMC free article] [PubMed]
  • Weaver PF, Wall JD, Gest H. Characterization of Rhodopseudomonas capsulata. Arch Microbiol. 1975 Nov 7;105(3):207–216. [PubMed]
  • Wilbur WJ, Lipman DJ. Rapid similarity searches of nucleic acid and protein data banks. Proc Natl Acad Sci U S A. 1983 Feb;80(3):726–730. [PMC free article] [PubMed]
  • Williams JC, Steiner LA, Feher G. Primary structure of the reaction center from Rhodopseudomonas sphaeroides. Proteins. 1986 Dec;1(4):312–325. [PubMed]
  • Wilson HR, Chan PT, Turnbough CL., Jr Nucleotide sequence and expression of the pyrC gene of Escherichia coli K-12. J Bacteriol. 1987 Jul;169(7):3051–3058. [PMC free article] [PubMed]
  • Winkelman JW, Clark DP. Anaerobically induced genes of Escherichia coli. J Bacteriol. 1986 Jul;167(1):362–367. [PMC free article] [PubMed]
  • Youvan DC, Bylina EJ, Alberti M, Begusch H, Hearst JE. 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. [PubMed]
  • Youvan DC, 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. [PMC free article] [PubMed]
  • Zhu YS, Hearst JE. 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. [PMC free article] [PubMed]
  • Zoller MJ, Smith M. Oligonucleotide-directed mutagenesis of DNA fragments cloned into M13 vectors. Methods Enzymol. 1983;100:468–500. [PubMed]
  • Zucconi AP, Beatty JT. 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. [PMC free article] [PubMed]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

Formats:

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...