The NblAl protein from the filamentous cyanobacterium Tolypothrix PCC 7601: Regulation of its expression and interactions with phycobilisome components

Molecular Microbiology

Volumn 50, Issue 3, 2003, Pages 1043-1054

  Luque, Ignacio ^a,b   De Ochoa Alda, Jesús A G ^a,c   Richaud, Catherine ^a   Zabulon, Gérald ^a   Thomas, Jean Claude ^a   Houmard, Jean ^a  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b Campus de San Vicente de Raspeig   (Spain)

^c Facultad de CC Biologicas   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOPHYCOCYANIN; BACTERIAL PROTEIN; MESSENGER RNA; NITROGEN; PHYCOBILIPROTEIN; PHYCOCYANIN; PHYCOERYTHRIN; POLYPEPTIDE; PROTEIN NBLAL; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CYANOBACTERIUM; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PHOTOSYNTHESIS; PHYCOBILISOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RED LIGHT; TOLYPOTHRIX; TRANSCRIPTION INITIATION SITE;

BACTERIA (MICROORGANISMS); CYANOBACTERIA; NEGIBACTERIA; PROKARYOTA; TOLYPOTHRIX; TOLYPOTHRIX SP. PCC 7601;

EID: 0242690137     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2003.03768.x     Document Type: Article

References (50)

1. Allen, M.M., and Smith, A.J. (1969) Nitrogen chlorosis in blue-green algae. Arch Mikrobiol 69: 114-120.
2. Ausubel, P.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., and Struhl, K. (1999) Short Protocols in Molecular Biology. New York: John Wiley & Sons.
3. Baier, K., Nicklisch, S., Grundner, C., Reinecke, J., and Lockau, W. (2001) Expression of two nblA-homologous genes is required for phycobilisome degradation in nitrogen-starved Synechocystis sp. PCC6803. FEMS Microbiol Lett 195: 35-39.
4. Bennett, A., and Bogorad, L. (1973) Complementary chromatic adaptation in a filamentous blue-green alga. J Cell Biol 58: 419-435.
5. Burkhard, P., Kammerer, R.A., Steinmetz, M.O., Bourenkov, G.P., and Aebi, U. (2000) The coiled-coil trigger site of the rod domain of cortexillin I unveils a distinct network of interhelical and intrahelical salt bridges. Structure Fold Des 8: 223-230.
6. Burkhard, P., Stetefeld, J., and Strelkov, S.V. (2001) Coiled coils: a highly versatile protein folding motif. Trends Cell Biol 11: 82-88.
7. Campbell, D. (1996) Complementary chromatic adaptation alters photosynthetic strategies in the cyanobacterium Calothrix. Microbiology 142: 1255-1263.
8. Collier, J.L., and Grossman, A.R. (1994) A small polypeptide triggers complete degradation of light-harvesting phycobiliproteins in nutrient-deprived cyanobacteria. EMBO J 13: 1039-1347.
9. Collier, J.L., Herbert, S.K., Fork, D.C., and Grossman, A.R. (1994) Changes in the cyanobacterial photosynthetic apparatus in response to macronutrient deprivation. Photosyn Res 42: 173-183.
10. Csiszàr, K., Houmard, J., Damerval, T., and Tandeau de Marsac, N. (1987) Transcriptional analysis of the cyanobacterial gvpABC operon in differentiated cells: occurrence of an antisense RNA complementary to three overlapping transcripts. Gene 60: 29-37.
11. Dolganov, N., and Grossman, A.R. (1999) A polypeptide with similarity to phycocyanin alpha-subunit phycocyanobilin lyase involved in degradation of phycobilisomes. J Bacteriol 181: 610-617.
12. Garcia-Dominguez, M., Reyes, J.C., and Florencio, F.J. (2000) NtcA represses transcription of gifA and gifB, genes that encode inhibitors of glutamine synthetase type I from Synechocystis sp. PCC 6803. Mol Microbiol 35: 1192-1201.
13. Glazer, A.N. (1989) Light guides. Directional energy transfer in a photosynthetic antenna. J Biol Chem 264: 1-4.
14. Görl, M., Sauer, J., Baier, T., and Forchhammer, K. (1998) Nitrogen-starvation-induced chlorosis in Synechococcus PCC 7942: adaptation to long-term survival. Microbiology 144: 2449-2458.
15. Grossman, A.R., Bhaya, D., and He, Q. (2001) Tracking the light environment by cyanobacteria and the dynamic nature of light harvesting. J Biol Chem 276: 11449-11452.
16. Herrero, A., Muro-Pastor, A.M., and Flores, E. (2001) Nitrogen control in cyanobacteria. J Bacteriol 183: 411-425.
17. Kahn, K., Mazel, D., Houmard, J., Tandeau de Marsac, N., and Schaefer, M.R. (1997) A role for cpeYZ in cyanobacterial phycoerythrin biosynthesis. J Bacteriol 179: 998-1006.
18. Laurière, M. (1993) A semidry electroblotting system efficiently transfers both high- and low-molecular-weight proteins separated by SDS-PAGE. Anal Biochem 212: 206-211.
19. Li, H., and Sherman, L.A. (2002) Characterization of Synechocystis sp. strain PCC 6803 and Δnbl mutants under nitrogen-deficient conditions. Arch Microbiol 178: 256-266.
20. Lupas, A. (1996) Coiled coils: new structures and new functions. Trends Biochem Sci 21: 375-382.
21. Luque, I., Zabulon, G., Contreras, A., and Houmard, J. (2001) Convergence of two global transcriptional regulators on nitrogen induction of the stress-acclimation gene nblA in the cyanobacterium Synechococcus sp. PCC 7942. Mol Microbiol 41: 937-947.
22. Lynn, M.E., Bantle, J.A., and Ownby, J.D. (1986) Estimation of gene expression in heterocysts of Anabaena variabilis by using DNA-RNA hybridization. J Bacteriol 167: 940-946.
23. MacKinney, G. (1941) Absorption of light by chorophyll solutions. J Biol Chem 140: 315-322.
24. Mazel, D., Guglielmi, G., Houmard, J., Sidler, W., Bryant, D.A., and Tandeau de Marsac, N. (1986) Green light induces transcription of the phycoerythrin operon in the cyanobacterium Calothrix PCC 7601. Nucleic Acids Res 14: 8279-8290.
25. Mazel, D., Houmard, J., Castets, A.-M., and Tandeau de Marsac, N. (1990) Highly repetitive DNA sequences in cyanobacterial genomes. J Bacteriol 172: 2755-2761.
26. Meeks, J.C., and Elhai, J. (2002) Regulation of cellular differentiation in filamentous cyanobacteria in free-living and plant-associated symbiotic growth states. Microbiol Mol Biol Rev 66: 94-121.
27. Mehrani, T., Wu, K.C., Morasso, M.I., Bryan, J.T., Marekov, L.N., Parry, D.A., and Steinert, P.M. (2001) Residues in the 1A rod domain segment and the linker L2 are required for stabilizing the A11 molecular alignment mode in keratin intermediate filaments. J Biol Chem 276: 2088-2097.
28. Newman, J.R., Wolf, E., and Kim, P.S. (2000) From the cover: a computationally directed screen identifying interacting coiled coils from Saccharomyces cerevisiae. Proc Natl Acad Sci USA 97: 13203-13208.
29. Noubir, S., Luque, I., Ochoa de Alda, J.A.G., Perewoska, I., Tandeau de Marsac, N., Cobley, J.G., and Houmard, J. (2002) Coordinated expression of phycobiliprotein operons in the chromatically adapting cyanobacterium Calothrix PCC 7601: a role for RcaD and RcaG. Mol Microbiol 43: 749-762.
30. Ochoa de Alda, J.A.G., Tapia, M.I., Llama, M.J., and Serra, J.L. (1996) Bioenergetic processes are modified during nitrogen starvation and recovery in Phormidium laminosum (Cyanophyceae). J Phycol 32: 258-265.
31. Ray, S., Zozulya, S., Niemi, G.A., Flaherty, K.M., Brolley, D., Dizhoor, A.M., et al. (1992) Cloning, expression, and crystallization of recoverin, a calcium sensor in vision. Proc Natl Acad Sci USA 89: 5705-5709.
32. Richaud, C., Zabulon, G., Joder, A., and Thomas, J.-C. (2001) Nitrogen or sulfur starvation differentially affects phycobilisome degradation and expression of the nblA gene in Synechocystis strain PCC 6803. J Bacteriol 183: 2989-2994.
33. Rippka, R., and Herdman, M. (1992) Pasteur culture collection of cyanobacterial strains in axenic culture. In Catalogue and Taxonomic Handbook. Paris: Institut Pasteur.
34. Sauer, J., Schreiber, U., Schmid, R., Volker, U., and Forchhammer, K. (2001) Nitrogen starvation-induced chlorosis in Synechococcus PCC 7942. Low-level photosynthesis as a mechanism of long-term survival. Plant Physiol 126: 233-243.
35. Schagger, H., and von Jagow, G. (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166: 368-379.
36. Schwarz, R., and Grossman, A.R. (1998) A response regulator of cyanobacteria integrates diverse environmental signals and is critical for survival under extreme conditions. Proc Natl Acad Sci USA 95: 11008-11013.
37. Sobczyk, A., Schyns, G., Tandeau de Marsac, N., and Houmard, J. (1993) Transduction of the light signal during complementary chromatic adaptation in the cyanobacterium Calothrix sp. PCC 7601: DNA-binding proteins and modulation by phosphorylation. EMBO J 12: 997-1004.
38. Steinert, P.M. (1990) The two-chain coiled-coil molecule of native epidermal keratin intermediate filaments is a type I-type II heterodimer. J Biol Chem 265: 8766-8774.
39. Steinmetz, M.O., Stock, A., Schulthess, T., Landwehr, R., Lustig, A., Faix, J., et al. (1998) A distinct 14 residue site triggers coiled-coil formation in cortexillin I. EMBO J 17: 1883-1891.
40. Strauss, H., Misselwitz, R., Labudde, D., Nicklisch, S., and Baier, K. (2002) NblA from Anabaena sp. PCC 7120 is a mostly alpha-helical protein undergoing reversible trimerization in solution. Eur J Biochem 269: 4617-4624.
41. Swerdlow, P.S., Finley, D., and Varshavsky, A. (1986) Enhancement of immunoblot sensitivity by heating of hydrated filters. Anal Biochem 156: 147-153.
42. Tandeau de Marsac, N., and Houmard, J. (1993) Adaptation of cyanobacteria to environmental stimuli: new steps towards molecular mechanisms. FEMS Microbiol Rev 104: 119-190.
43. Thomas, J.-C., and Passaquet, C. (1999) Characterization of a phycoerythrin without alpha-subunits from a unicellular red alga. J Biol Chem 274: 2472-2482.
44. Tooley, A.J., and Glazer, A.N. (2002) Biosynthesis of the cyanobacterial light-harvesting polypeptide phycoerythrocyanin holo-subunit in a heterologous host. J Bacteriol 184: 4666-4671.
45. Vioque, A. (1992) Analysis of the gene encoding the RNA subunit of ribonuclease P from cyanobacteria. Nucleic Acids Res 20: 6331-6337.
46. van Waasbergen, L.G., Dolganov, N., and Grossman, A.R. (2002) nblS, a gene involved in controlling photosynthesis-related gene expression during high light and nutrient stress in Synechococcus elongatus PCC 7942. J Bacteriol 184: 2481-2490.
47. Wawersik, M., Paladini, R.D., Noensie, E., and Coulombe, P.A. (1997) A Proline Residue in the α-Helical Rod Domain of Type I Keratin16 Destabilizes Keratin Heterotetramers. J Biol Chem 272: 32557-32565.
48. Wolk, C.P. (1996) Heterocyst formation. Annu Rev Genet 30: 59-78.
49. Yeliseev, A.A., and Kaplan, S. (1995) A sensory transducer homologous to the mammalian peripheral-type benzodiazepine receptor regulates photosynthetic membrane complex formation in Rhodobacter sphaeroides 2.4.1. J Biol Chem 270: 21167-21175.
50. Yeliseev, A.A., and Kaplan, S. (1999) A novel mechanism for the regulation of photosynthesis gene expression by the TspO outer membrane protein of Rhodobacter sphaeroides 2.4.1. J Biol Chem 274: 21234-21243.