Supramolecular organization and dual function of the IsiA chlorophyll-binding protein in cyanobacteria

Biochemistry

Volumn 43, Issue 32, 2004, Pages 10308-10313

  Yeremenko, Nataliya ^a   Kouřil, Roman ^b   Ihalainen, Janne A ^c   D'Haene, Sandrine ^c   Van Oosterwijk, Niels ^b   Andrizhiyevskaya, Elena G ^c   Keegstra, Wilko ^b   Dekker, Henk L ^d   Hagemann, Martin ^e   Boekema, Egbert J ^b   Matthijs, Hans C P ^a   Dekker, Jan P ^c  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c VU UNIVERSITY AMSTERDAM   (Netherlands)

^d UNIVERSITY OF AMSTERDAM   (Netherlands)

^e UNIVERSITY OF ROSTOCK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BIOSYNTHESIS; CHLOROPHYLL; FLUORESCENCE; MONOMERS; OCEANOGRAPHY; PROTEINS; SUPRAMOLECULAR CHEMISTRY;

CYANOBACTERIA; SUPRAMOLECULAR OPTIMIZATION;

BIOCHEMISTRY;

BINDING PROTEIN; CHLOROPHYLL; CHLOROPHYLL BINDING PROTEIN; IRON; ISIA PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; CYANOBACTERIUM; ELECTRON MICROSCOPY; FLUORESCENCE SPECTROSCOPY; GENE EXPRESSION; LIGHT HARVESTING SYSTEM; MASS SPECTROMETRY; NONHUMAN; OPERON; PHOTOOXIDATION; PHOTOSYSTEM I; PHOTOSYSTEM II; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; SYNECHOCYSTIS;

BACTERIAL PROTEINS; CHLOROPHYLL; CYANOBACTERIA; FLUORESCENCE; IRON; LIGHT-HARVESTING PROTEIN COMPLEXES; MUTATION; PROTEIN BINDING;

BACTERIA (MICROORGANISMS); CYANOBACTERIA; SYNECHOCYSTIS; SYNECHOCYSTIS SP. PCC 6803;

EID: 4043070560     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048772l     Document Type: Article

References (38)

1. Martin, J. H., Coale, K. H., Johnson, K. S., Fitzwater, S. E., Gordon, R. M., Tanner, S. J., Hunter, C. N., Elrod, V. A., Nowicki, J. L., Coley, T. L., et al. (1994) Testing the iron hypothesis in ecosystems of the equatorial pacific ocean, Nature 371, 123-129.
2. De Baar, H. J. W., de Jong, J. T. M., Bakker, D. C. E., Loscher, B. M., Veth, C., Bathmann, U., and Smetacek, V. (1995) Importance of iron for plankton blooms and carbon-dioxide drawdown in the southern ocean, Nature 373, 412-415.
3. Falkowski, P. G., Barber, R. T., and Smetacek, V. (1998) Biogeochemical controls and feedbacks on ocean primary production, Science 281, 200-206.
4. Behrenfeld, M. J., and Kolber, Z. S. (1999) Widespread iron limitation of phytoplankton in the South Pacific Ocean, Science 283, 840-843.
5. Ting, C. S., Rocap, G., King, J., and Chisholm, S. W. (2002) Cyanobacterial photosynthesis in the oceans: the origins and significance of divergent light-harvesting strategies, Trends Microbiol. 10, 134-142.
6. Burnap, R. L., Troyan, T., and Sherman, L. A. (1993) The highly abundant chlorophyll-protein of iron-deficient Synechococcus sp. PCC 7942 (CP43′) is encoded by the isiA gene, Plant Physiol. 103, 893-902.
7. Jordan, P., Fromme, P., Witt, H. T., Klukas, O., Saenger, W., and Krauss, N. (2001) Three-dimensional structure of phoyosystem I at 2.5 Å resolution, Nature 411, 909-917.
8. Fromme, P., Melkozernov, A., Jordan, P., and Krauss, N. (2003) Structure and function of photosystem I: interaction with its soluble electron carriers and external antenna systems, FEBS Lett. 555, 40-44.
9. Falk, S., Samson, G., Bruce, D., Huner, N. P. A., and Laudenbach, D. E. (1995) Functional analysis of the iron-stress induced CP43′ polypeptide of PS II in the cyanobacterium Synechococcus sp. PCC 7942, Photosynth. Res. 45, 51-60.
10. Sandström, S., Park, Y. I., Öquist, G., and Gustafsson, P. (2001) CP437prime;, the isiA gene product, functions as an excitation energy dissipator in the cyanobacterium Synechococcus sp. PCC 7942, Photochem. Photobiol. 74, 431-437.
11. Green, B. R. (2003) The evolution of light-harvesting antennas, in Light-Harvesting Antennas in Photosynthesis (Green, B. R., and Parson, W. W., Eds.) pp 129-168, Kluwer Academic Publishers, Dordrecht, The Netherlands.
12. Bibby, T. S., Nield, J., and Barber, J. (2001) Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria, Nature 412, 743-745.
13. Boekema, E. J., Hifney, A., Yakushevska, A. E., Piotrowski, M., Keegstra, W., Berry, S., Michel, K. P., Pistorius, E. K., and Kruip, J. (2001) A giant chlorophyll-protein complex induced by iron-deficiency in cyanobacteria, Nature 412, 745-748.
14. Ferreira, K. N., Iverson, T. M., Maghlaoui, K., Barber, J., and Iwata, S. (2004) Architecture of the photosynthetic oxygen-evolving center, Science 303, 1831-1838.
15. Van Amerongen, H., and Dekker, J. P. (2003) Light-harvesting in photosystem II, in Light-Harvesting Antennas in Photosynthesis (Green, B. R., and Parson, W. W., Eds.) pp 219-251, Kluwer Academic Publishers, Dordrecht, The Netherlands.
16. Bibby, T. S., Nield, J., Chen, M., Larkum, A. W. D., and Barber, J. (2003) Structure of a photosystem II supercomplex isolated from Prochloron didemni retaining its chlorophyll a/b light-harvesting system, Proc. Natl. Acad. Sci. U.S.A. 100, 9050-9054.
17. Bibby, T. S., Mary, I., Nield, J., Partensky, F., and Barber, J. (2003) Low-light-adapted Prochlorococcus species possess specific antennae for each photosystem, Nature 424, 1051-1054.
18. Bibby, T. S., Nield, J., Partensky, F., and Barber, J. (2001) Oxyphotobacteria: Antenna ring around PS1, Nature 413, 590.
19. Andrizhiyevskaya, E. G., Schwabe, T. M. E., Germano, M., D'Haene, S., Kruip, J., van Grondelle, R., and Dekker, J. P. (2002) Spectroscopic properties of PSI-IsiA supercomplexes of the cyanobacterium Synechococcus PCC 7942, Biochim. Biophys. Acta 1556, 265-272.
20. Melkozernov, A. N., Bibby, T. S., Lin, S., Barber, J., and Blankenship, R. E. (2003) Time-resolved absorption and emission show that the CP43′ antenna ring of iron-stressed Synechocystis sp. PCC 6803 is efficiently coupled to the photosystem I reaction center core, Biochemistry 42, 3893-3903.
21. Andrizhiyevskaya, E. G., Frolov, D., van Grondelle, R., and Dekker, J. P. (2004) Energy transfer and trapping in the photosystem I complex of Synechococcus PCC 7942 and in its supercomplex with IsiA, Biochim. Biophys. Acta 1656, 104-113.
22. Park, Y. I., Sandström, S., Gustafsson, P., and Öquist, G. (1999) Expression of the isiA gene is essential for the survival of the cyanobacterium Synechococcus sp PCC7942 by protecting photosystem II from excess light under iron limitation, Mol. Microbiol. 32, 123-129.
23. Michel, K. P., and Pistorius, E. K. (2004) Adaptation of the photosynthetic electron transport chain in cyanobacteria to iron deficiency: The function of IdiA and IsiA, Physiol. Plant. 120, 36-50.
24. Sandström, S., Ivanov, A. G., Park, Y. I., Öquist, G., and Gustafsson, P. (2002) Iron stress responses in the cyanobacterium Synechocystis sp. PCC 7942, Physiol. Plant. 116, 255-263.
25. Singh, A. K., McIntyre, L. M., and Sherman, L. A. (2003) Microarray analysis of the genome-wide response to iron deficiency and iron reconstitution in the cyanobacterium Synechocystis sp. PCC 6803, Plant Physiol. 132, 1825-1839.
26. Jeanjean, R., Zuther, E., Yeremenko, N., Havaux, M., Matthijs, H. C. P., and Hagemann, M. (2003) A photosystem I psaFJ-null mutant of the cyanobacterium Synechocystis PCC 6803 expresses the isiAB operon under iron replete conditions, FEBS Lett. 549, 52-56.
27. Scholts, M. J. C., Aardewijn, P., and van Walraven, H. S. (1996) Membrane vesicles from Synechocystis 6803 showing proton and electron transport and high ATP synthase activities, Photosynth. Res. 47, 301-305.
28. Kouril, R., Yeremenko, N., D'Haene, S., Yakushevska, A. E., Keegstra, W., Matthijs, H. C. P., Dekker, J. P., and Boekema, E. J. (2003) Photosystem I trimers from Synechocystis PCC 6803 lacking the PsaF and PsaJ subunits bind an IsiA ring of 17 units, Biochim. Biophys. Acta 1607, 1-4.
29. Schägger, 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.
30. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins from silver stained polyacrylamide gels, Anal. Chem. 68, 850-858.
31. Harauz, G., Boekema, E. J., and van Heel, M. (1988) Statistical image analysis of electron micrographs of ribosomal subunits, Methods Enzymol. 164, 35-49.
32. Penczek, P., Radermacher, M., and Frank, J. (1992) Three-dimensional reconstruction of single particles embedded in ice, Ultramicroscopy 40, 33-53.
33. Karapetyan, N. V., Holzwarth, A. R., and Rögner, M. (1999) The photosystem I trimer of cyanobacteria: molecular organization, excitation dynamics and physiological significance, FEBS Lett. 460, 395-400.
34. Boekema, E. J., van Roon, H., Calkoen, F., Bassi, R., and Dekker, J. P. (1999) Multiple types of association of photosystem II and its light-harvesting antenna in partially solubilized photosystem II membranes, Biochemistry 38, 2233-2239.
35. Gobets, B., van Stokkum, I. H. M., Rögner, M., Kruip, J., Schlodder, E., Karapetyan, N. V., Dekker, J. P., and van Grondelle, R. (2001) Time-resolved fluorescence emission measurements of photosystem I particles of various cyanobacteria: A unified compartmental model, Biophys. J. 81, 407-424.
36. Ben-Shem, A., Frolow, F., and Nelson, N. (2003) Crystal structure of plant photosystem I, Nature 426, 630-635.
37. Liu, Z., Yan, H., Wang, K., Kuang, T., Zhang, J., Gui, L., An, X., and Chang, W. (2004) Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution, Nature 428, 287-292.
38. Ruban, A. V., Wentworth, M., Yakushevska, A. E., Andersson, J., Lee, P. J., Keegstra, W., Dekker, J. P., Boekema, E. J., Jansson, S., and Horton, P. (2003) Plants lacking the main light-harvesting complex retain photosystem II macro-organization, Nature 421, 648-652.