Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1987 Jun;169(6):2675–2684. doi: 10.1128/jb.169.6.2675-2684.1987

Isolation and characterization of light-regulated phycobilisome linker polypeptide genes and their transcription as a polycistronic mRNA.

T L Lomax, P B Conley, J Schilling, A R Grossman
PMCID: PMC212156  PMID: 3108238

Abstract

Several cyanobacteria adjust both the phycobiliprotein and linker protein composition of the phycobilisome, a light-harvesting complex in cyanobacteria and some eucaryotic algae, to maximize absorption of prevalent wavelengths of light. This process is called complementary chromatic adaptation. We sequenced the amino terminus of a linker polypeptide which is associated with phycocyanin and accumulates to high levels during growth of the cyanobacterium Fremyella diplosiphon in red light. A mixed oligonucleotide encoding a region of this amino terminus was synthesized and used to identify a fragment of F. diplosiphon genomic DNA encoding the linker polypeptide. This linker gene was located between two other linker genes and contiguous to the red-light-induced phycocyanin gene set. Sequences of all three linker genes are presented. These genes were transcribed together onto a large polycistronic mRNA which also encoded the red-light-induced phycocyanin subunits. The relationship of this transcript to the biogenesis of the phycobilisome when F. diplosiphon is grown under different conditions of illumination is discussed.

Full text

PDF
2679

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bacon D. J., Anderson W. F. Multiple sequence alignment. J Mol Biol. 1986 Sep 20;191(2):153–161. doi: 10.1016/0022-2836(86)90252-4. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Belknap W. R., Haselkorn R. Cloning and light regulation of expression of the phycocyanin operon of the cyanobacterium Anabaena. EMBO J. 1987 Apr;6(4):871–884. doi: 10.1002/j.1460-2075.1987.tb04833.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Benton W. D., Davis R. W. Screening lambdagt recombinant clones by hybridization to single plaques in situ. Science. 1977 Apr 8;196(4286):180–182. doi: 10.1126/science.322279. [DOI] [PubMed] [Google Scholar]
  5. Bryant D. A., Cohen-Bazire G. Effects of chromatic illumination on cyanobacterial phycobilisomes. Evidence for the specific induction of a second pair of phycocyanin subunits in Pseudanabaena 7409 grown in red light. Eur J Biochem. 1981 Oct;119(2):415–424. doi: 10.1111/j.1432-1033.1981.tb05624.x. [DOI] [PubMed] [Google Scholar]
  6. Bryant D. A. The photoregulated expression of multiple phycocyanin species. A general mechanism for the control of phycocyanin synthesis in chromatically adapting cyanobacteria. Eur J Biochem. 1981 Oct;119(2):425–429. doi: 10.1111/j.1432-1033.1981.tb05625.x. [DOI] [PubMed] [Google Scholar]
  7. Clary D. O., Wolstenholme D. R. The ribosomal RNA genes of Drosophila mitochondrial DNA. Nucleic Acids Res. 1985 Jun 11;13(11):4029–4045. doi: 10.1093/nar/13.11.4029. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Conley P. B., Lemaux P. G., Grossman A. R. Cyanobacterial light-harvesting complex subunits encoded in two red light-induced transcripts. Science. 1985 Nov 1;230(4725):550–553. doi: 10.1126/science.3931221. [DOI] [PubMed] [Google Scholar]
  9. Conley P. B., Lemaux P. G., Lomax T. L., Grossman A. R. Genes encoding major light-harvesting polypeptides are clustered on the genome of the cyanobacterium Fremyella diplosiphon. Proc Natl Acad Sci U S A. 1986 Jun;83(11):3924–3928. doi: 10.1073/pnas.83.11.3924. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Darley-Usmar V. M., Fuller S. D. Mr-values of mature subunits I and III of beef heart cytochrome c oxidase in relationship to nucleotide sequences of their genes. FEBS Lett. 1981 Nov 30;135(1):164–166. doi: 10.1016/0014-5793(81)80968-4. [DOI] [PubMed] [Google Scholar]
  11. Egelhoff T., Grossman A. Cytoplasmic and chloroplast synthesis of phycobilisome polypeptides. Proc Natl Acad Sci U S A. 1983 Jun;80(11):3339–3343. doi: 10.1073/pnas.80.11.3339. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Frischauf A. M., Lehrach H., Poustka A., Murray N. Lambda replacement vectors carrying polylinker sequences. J Mol Biol. 1983 Nov 15;170(4):827–842. doi: 10.1016/s0022-2836(83)80190-9. [DOI] [PubMed] [Google Scholar]
  14. Füglistaller P., Suter F., Zuber H. Linker polypeptides of the phycobilisome from the cyanobacterium Mastigocladus laminosus: amino-acid sequences and relationships. Biol Chem Hoppe Seyler. 1985 Oct;366(10):993–1001. doi: 10.1515/bchm3.1985.366.2.993. [DOI] [PubMed] [Google Scholar]
  15. Glazer A. N. Light harvesting by phycobilisomes. Annu Rev Biophys Biophys Chem. 1985;14:47–77. doi: 10.1146/annurev.bb.14.060185.000403. [DOI] [PubMed] [Google Scholar]
  16. Glazer A. N., Lundell D. J., Yamanaka G., Williams R. C. The structure of a "simple" phycobilisome. Ann Microbiol (Paris) 1983 Jul-Aug;134B(1):159–180. doi: 10.1016/s0769-2609(83)80103-3. [DOI] [PubMed] [Google Scholar]
  17. Glazer A. N. Phycobilisomes: structure and dynamics. Annu Rev Microbiol. 1982;36:173–198. doi: 10.1146/annurev.mi.36.100182.001133. [DOI] [PubMed] [Google Scholar]
  18. Glazer A. N., Yeh S. W., Webb S. P., Clark J. H. Disk-to-Disk Transfer as the Rate-Limiting Step for Energy Flow in Phycobilisomes. Science. 1985 Jan 25;227(4685):419–423. doi: 10.1126/science.227.4685.419. [DOI] [PubMed] [Google Scholar]
  19. Grossman A. R., Lemaux P. G., Conley P. B. Regulated synthesis of phycobilisome components. Photochem Photobiol. 1986 Dec;44(6):827–837. doi: 10.1111/j.1751-1097.1986.tb05543.x. [DOI] [PubMed] [Google Scholar]
  20. HUGHES E. O., GORHAM P. R., ZEHNDER A. Toxicity of a unialgal culture of Microcystis aeruginosa. Can J Microbiol. 1958 Jun;4(3):225–236. doi: 10.1139/m58-024. [DOI] [PubMed] [Google Scholar]
  21. Henikoff S. Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene. 1984 Jun;28(3):351–359. doi: 10.1016/0378-1119(84)90153-7. [DOI] [PubMed] [Google Scholar]
  22. Holschuh K., Bottomley W., Whitfeld P. R. Structure of the spinach chloroplast genes for the D2 and 44 kd reaction-centre proteins of photosystem II and for tRNASer (UGA). Nucleic Acids Res. 1984 Dec 11;12(23):8819–8834. doi: 10.1093/nar/12.23.8819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Houmard J., Mazel D., Moguet C., Bryant D. A., Tandeau de Marsac N. Organization and nucleotide sequence of genes encoding core components of the phycobilisomes from Synechococcus 6301. Mol Gen Genet. 1986 Dec;205(3):404–410. doi: 10.1007/BF00338074. [DOI] [PubMed] [Google Scholar]
  24. Hunkapiller M. W., Lujan E., Ostrander F., Hood L. E. Isolation of microgram quantities of proteins from polyacrylamide gels for amino acid sequence analysis. Methods Enzymol. 1983;91:227–236. doi: 10.1016/s0076-6879(83)91019-4. [DOI] [PubMed] [Google Scholar]
  25. Lemaux P. G., Grossman A. R. Major light-harvesting polypeptides encoded in polycistronic transcripts in a eukaryotic alga. EMBO J. 1985 Aug;4(8):1911–1919. doi: 10.1002/j.1460-2075.1985.tb03870.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lemaux P. G., Grossman A. Isolation and characterization of a gene for a major light-harvesting polypeptide from Cyanophora paradoxa. Proc Natl Acad Sci U S A. 1984 Jul;81(13):4100–4104. doi: 10.1073/pnas.81.13.4100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Lundell D. J., Glazer A. N. Molecular architecture of a light-harvesting antenna. Quaternary interactions in the Synechococcus 6301 phycobilisome core as revealed by partial tryptic digestion and circular dichroism studies. J Biol Chem. 1983 Jul 25;258(14):8708–8713. [PubMed] [Google Scholar]
  28. Lundell D. J., Williams R. C., Glazer A. N. Molecular architecture of a light-harvesting antenna. In vitro assembly of the rod substructures of Synechococcus 6301 phycobilisomes. J Biol Chem. 1981 Apr 10;256(7):3580–3592. [PubMed] [Google Scholar]
  29. Mazel D., Guglielmi G., Houmard J., Sidler W., Bryant D. A., Tandeau de Marsac N. Green light induces transcription of the phycoerythrin operon in the cyanobacterium Calothrix 7601. Nucleic Acids Res. 1986 Nov 11;14(21):8279–8290. doi: 10.1093/nar/14.21.8279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Messing J. New M13 vectors for cloning. Methods Enzymol. 1983;101:20–78. doi: 10.1016/0076-6879(83)01005-8. [DOI] [PubMed] [Google Scholar]
  31. Nicholson B. J., Hunkapiller M. W., Grim L. B., Hood L. E., Revel J. P. Rat liver gap junction protein: properties and partial sequence. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7594–7598. doi: 10.1073/pnas.78.12.7594. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Redlinger T., Gantt E. A M(r) 95,000 polypeptide in Porphyridium cruentum phycobilisomes and thylakoids: Possible function in linkage of phycobilisomes to thylakoids and in energy transfer. Proc Natl Acad Sci U S A. 1982 Sep;79(18):5542–5546. doi: 10.1073/pnas.79.18.5542. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Redlinger T., Gantt E. Phycobilisome Structure of Porphyridium cruentum: POLYPEPTIDE COMPOSITION. Plant Physiol. 1981 Dec;68(6):1375–1379. doi: 10.1104/pp.68.6.1375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Saraste M. Location of haem-binding sites in the mitochondrial cytochrome b. FEBS Lett. 1984 Jan 30;166(2):367–372. doi: 10.1016/0014-5793(84)80114-3. [DOI] [PubMed] [Google Scholar]
  35. Schirmer T., Bode W., Huber R., Sidler W., Zuber H. X-ray crystallographic structure of the light-harvesting biliprotein C-phycocyanin from the thermophilic cyanobacterium Mastigocladus laminosus and its resemblance to globin structures. J Mol Biol. 1985 Jul 20;184(2):257–277. doi: 10.1016/0022-2836(85)90379-1. [DOI] [PubMed] [Google Scholar]
  36. Singer B. S., Gold L., Shinedling S. T., Colkitt M., Hunter L. R., Pribnow D., Nelson M. A. Analysis in vivo of translational mutants of the rIIB cistron of bacteriophage T4. J Mol Biol. 1981 Jul 5;149(3):405–432. doi: 10.1016/0022-2836(81)90479-4. [DOI] [PubMed] [Google Scholar]
  37. Thomas P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. doi: 10.1073/pnas.77.9.5201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Williams R. C., Gingrich J. C., Glazer A. N. Cyanobacterial phycobilisomes. Particles from Synechocystis 6701 and two pigment mutants. J Cell Biol. 1980 Jun;85(3):558–566. doi: 10.1083/jcb.85.3.558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. de Marsac N. T., Cohen-bazire G. Molecular composition of cyanobacterial phycobilisomes. Proc Natl Acad Sci U S A. 1977 Apr;74(4):1635–1639. doi: 10.1073/pnas.74.4.1635. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES