Characterization and evolution of tetrameric Photosystem I from the thermophilic cyanobacterium Chroococcidiopsis sp TS-821

Plant Cell

Volumn 26, Issue 3, 2014, Pages 1230-1245

  Li, Meng ^a   Semchonok, Dmitry A ^b   Boekema, Egbert J ^b   Brucea, Barry D ^a  

^a UNIVERSITY OF TENNESSEE   (United States)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BIOPOLYMER; PHOTOSYSTEM I;

AMINO ACID SEQUENCE; CHEMISTRY; CIRCULAR DICHROISM; CYANOBACTERIUM; METABOLISM; MOLECULAR GENETICS; NATIVE POLYACRYLAMIDE GEL ELECTROPHORESIS; PHOTOSYSTEM I; SEQUENCE HOMOLOGY; TRANSMISSION ELECTRON MICROSCOPY;

AMINO ACID SEQUENCE; BIOPOLYMERS; CIRCULAR DICHROISM; CYANOBACTERIA; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; NATIVE POLYACRYLAMIDE GEL ELECTROPHORESIS; PHOTOSYSTEM I PROTEIN COMPLEX; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84899139307     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.120782     Document Type: Article

References (80)

1. Almog, O., Shoham, G., Michaeli, D., and Nechushtai, R. (1991). Monomeric and trimeric forms of photosystem I reaction center of Mastigocladus laminosus: Crystallization and preliminary characterization. Proc. Natl. Acad. Sci. USA 88: 5312-5316.
2. Amunts, A., and Nelson, N. (2008). Functional organization of a plant Photosystem I: Evolution of a highly efficient photochemical machine. Plant Physiol. Biochem. 46: 228-237.
3. Amunts, A., and Nelson, N. (2009). Plant photosystem I design in the light of evolution. Structure 17: 637-650.
4. Amunts, A., Toporik, H., Borovikova, A., and Nelson, N. (2010). Structure determination and improved model of plant photosystem I. J. Biol. Chem. 285: 3478-3486.
5. Aspinwall, C.L., Sarcina, M., and Mullineaux, C.W. (2004). Phycobilisome mobility in the cyanobacterium Synechococcus sp. PCC7942 is influenced by the trimerisation of Photosystem I. Photosynth. Res. 79: 179-187.
6. Baker, D.R., Manocchi, A.K., Lamicq, M.L., Li, M., Nguyen, K., Sumner, J.J., Bruce, B.D., and Lundgren, C.A. (2014). Comparative photoactivity and stability of isolated cyanobacterial monomeric and trimeric photosystem I. J. Physiol. Chem. B. 118: 2703-2711.
7. Ben-Shem, A., Frolow, F., and Nelson, N. (2003). Crystal structure of plant photosystem I. Nature 426: 630-635.
8. Ben-Shem, A., Frolow, F., and Nelson, N. (2004). Evolution of photosystem I-from symmetry through pseudo-symmetry to asymmetry. FEBS Lett. 564: 274-280.
9. 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.
10. 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.
11. Billi, D., Grilli Caiola, M., Paolozzi, L., and Ghelardini, P. (1998). A method for DNA extraction from the desert cyanobacterium chroococcidiopsis and its application to identification of ftsZ. Appl. Environ. Microbiol. 64: 4053-4056.
12. Boekema, E.J., Dekker, J.P., Vanheel, M.G., Rogner, M., Saenger, W., Witt, I., and Witt, H.T. (1987). Evidence for a trimeric organization of the photosystem I complex from the thermophilic cyanobacterium Synechococcus sp. FEBS Lett. 217: 283-286.
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. Boekema, E.J., Van Roon, H., Van Breemen, J.F., and Dekker, J.P. (1999). Supramolecular organization of photosystem II and its lightharvesting antenna in partially solubilized photosystem II membranes. Eur. J. Biochem. 266: 444-452.
15. Brecht, M., Hussels, M., Schlodder, E., and Karapetyan, N.V. (2012). Red antenna states of Photosystem I trimers from Arthrospira platensis revealed by single-molecule spectroscopy. Biochim. Biophys. Acta 1817: 445-452.
16. Cardona, T., Battchikova, N., Zhang, P.P., Stensjö, K., Aro, E.M., Lindblad, P., and Magnuson, A. (2009). Electron transfer protein complexes in the thylakoid membranes of heterocysts from the cyanobacterium Nostoc punctiforme. Biochim. Biophys. Acta 1787: 252-263.
17. Chitnis, V.P., Xu, Q., Yu, L., Golbeck, J.H., Nakamoto, H., Xie, D.L., and Chitnis, P.R. (1993). Targeted inactivation of the gene psaL encoding a subunit of photosystem I of the cyanobacterium Synechocystis sp. PCC 6803. J. Biol. Chem. 268: 11678-11684.
18. Criscuolo, A., and Gribaldo, S. (2011). Large-scale phylogenomic analyses indicate a deep origin of primary plastids within cyanobacteria. Mol. Biol. Evol. 28: 3019-3032.
19. Deusch, O., Landan, G., Roettger, M., Gruenheit, N., Kowallik, K.V., Allen, J.F., Martin, W., and Dagan, T. (2008). Genes of cyanobacterial origin in plant nuclear genomes point to a heterocyst-forming plastid ancestor. Mol. Biol. Evol. 25: 748-761.
20. El-Mohsnawy, E., Kopczak, M.J., Schlodder, E., Nowaczyk, M., Meyer, H.E., Warscheid, B., Karapetyan, N.V., and Rögner, M. (2010). Structure and function of intact photosystem 1 monomers from the cyanobacterium Thermosynechococcus elongatus. Biochemistry 49: 4740-4751.
21. Falcón, L.I., Magallón, S., and Castillo, A. (2010). Dating the cyanobacterial ancestor of the chloroplast. ISME J. 4: 777-783.
22. Fewer, D., Friedl, T., and Büdel, B. (2002). Chroococcidiopsis and heterocyst-differentiating cyanobacteria are each other's closest living relatives. Mol. Phylogenet. Evol. 23: 82-90.
23. Garczarek, L., van der Staay, G.W.M., Thomas, J.C., and Partensky, F. (1998). Isolation and characterization of Photosystem I from two strains of the marine oxychlorobacterium Prochlorococcus. Photosynth. Res. 56: 131-141.
24. Gardian, Z., Bumba, L., Schrofel, A., Herbstova, M., Nebesarova, J., and Vacha, F. (2007). Organisation of Photosystem I and Photosystem II in red alga Cyanidium caldarium: Encounter of cyanobacterial and higher plant concepts. Biochim. Biophys. Acta 1767: 725-731.
25. 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.
26. Gupta, R.S. (2009). Protein signatures (molecular synapomorphies) that are distinctive characteristics of the major cyanobacterial clades. Int. J. Syst. Evol. Microbiol. 59: 2510-2526.
27. Hackenberg, C., Kern, R., Hüge, J., Stal, L.J., Tsuji, Y., Kopka, J., Shiraiwa, Y., Bauwe, H., and Hagemann, M. (2011). Cyanobacterial lactate oxidases serve as essential partners in N2 fixation and evolved into photorespiratory glycolate oxidases in plants. Plant Cell 23: 2978-2990.
28. Hayashi, N.R., Peerapornpisal, Y., Nishihara, H., Ishii, M., Igarashi, Y., and Kodama, T. (1994). Isolation and cultivation of thermophilic cyanobacteria from hot springs of northern thailand. J. Ferment. Bioeng. 78: 179-181.
29. Heinemeyer, J., Eubel, H., Wehmhöner, D., Jänsch, L., and Braun, H.-P. (2004). Proteomic approach to characterize the supramolecular organization of photosystems in higher plants. Phytochemistry 65: 1683-1692.
30. Ihalainen, J.A., D'Haene, S., Yeremenko, N., van Roon, H., Arteni, A.A., Boekema, E.J., van Grondelle, R., Matthijs, H.C.P., and Dekker, J.P. (2005). Aggregates of the chlorophyll-binding protein IsiA (CP439) dissipate energy in cyanobacteria. Biochemistry 44: 10846-10853.
31. Ishida, T., Hasegawa, N., Hayashi, N.R., Peerapornpisal, Y., Ishii, M., Igarashi, Y., and Kodama, T. (1997). Growth characteristics and dense culture of a thermophilic cyanobacterium, Chroococcidiopsis sp. strain TS-821. J. Ferment. Bioeng. 83: 571-576.
32. Ivanov, A.G., Krol, M., Sveshnikov, D., Selstam, E., Sandström, S., Koochek, M., Park, Y.I., Vasil'ev, S., Bruce, D., Oquist, G., and Huner, N.P.A. (2006). Iron deficiency in cyanobacteria causes monomerization of photosystem I trimers and reduces the capacity for state transitions and the effective absorption cross section of photosystem I in vivo. Plant Physiol. 141: 1436-1445.
33. Iwamura, T., Nagai, H., and Ichimura, S.-E. (1970). Improved methods for determining contents of chlorophyll, protein, ribonucleic acid, and deoxyribonucleic acid in planktonic populations. Int. Revue ges. Hydrobiol. Hydrogr. 55: 131-147.
34. Iwuchukwu, I.J., Vaughn, M., Myers, N., O'Neill, H., Frymier, P., and Bruce, B.D. (2010). Self-organized photosynthetic nanoparticle for cell-free hydrogen production. Nat. Nanotechnol. 5: 73-79.
35. Jordan, P., Fromme, P., Witt, H.T., Klukas, O., Saenger, W., and Krauss, N. (2001). Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution. Nature 411: 909-917.
36. Karapetyan, N.V., Dorra, D., Schweitzer, G., Bezsmertnaya, I.N., and Holzwarth, A.R. (1997). Fluorescence spectroscopy of the longwave chlorophylls in trimeric and monomeric photosystem I core complexes from the cyanobacterium Spirulina platensis. Biochemistry 36: 13830-13837.
37. Keeling, P.J. (2004). Diversity and evolutionary history of plastids and their hosts. Am. J. Bot. 91: 1481-1493.
38. Kern, R., Bauwe, H., and Hagemann, M. (2011). Evolution of enzymes involved in the photorespiratory 2-phosphoglycolate cycle from cyanobacteria via algae toward plants. Photosynth. Res. 109: 103-114.
39. Kiley, P., Zhao, X., Vaughn, M., Baldo, M.A., Bruce, B.D., and Zhang, S. (2005). Self-assembling peptide detergents stabilize isolated photosystem I on a dry surface for an extended time. PLoS Biol. 3: e230.
40. Kitmitto, A., Mustafa, A.O., Holzenburg, A., and Ford, R.C. (1998). Three-dimensional structure of higher plant photosystem I determined by electron crystallography. J. Biol. Chem. 273: 29592-29599.
41. Kouřil, R., Arteni, A.A., Lax, J., Yeremenko, N., D'Haene, S., Rögner, M., Matthijs, H.C.P., Dekker, J.P., and Boekema, E.J. (2005b). Structure and functional role of supercomplexes of IsiA and Photosystem I in cyanobacterial photosynthesis. FEBS Lett. 579: 3253-3257.
42. Kouril, R., van Oosterwijk, N., Yakushevska, A.E., and Boekema, E.J. (2005). Photosystem I: A search for green plant trimers. Photochem. Photobiol. Sci. 4: 1091-1094.
43. Kouřil, R., Wientjes, E., Bultema, J.B., Croce, R., and Boekema, E.J. (2013). High-light vs. low-light: Effect of light acclimation on photosystem II composition and organization in Arabidopsis thaliana. Biochim. Biophys. Acta 1827: 411-419.
44. Kouřil, R., Yeremenko, N., D'Haene, S., Oostergetel, G.T., Matthijs, H.C.P., Dekker, J.P., and Boekema, E.J. (2005a). Supercomplexes of IsiA and Photosystem I in a mutant lacking subunit PsaL. Biochim. Biophys. Acta 1706: 262-266.
45. Kouřil, 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.
46. Kruip, J., Bald, D., Boekema, E., and Rögner, M. (1994). Evidence for the existence of trimeric and monomeric Photosystem I complexes in thylakoid membranes from cyanobacteria. Photosynth. Res. 40: 279-286.
47. Kruip, J., Boekema, E.J., Bald, D., Boonstra, A.F., and Rögner, M. (1993). Isolation and structural characterization of monomeric and trimeric photosystem I complexes (P700. FA/FB and P700. FX) from the cyanobacterium Synechocystis PCC 6803. J. Biol. Chem. 268: 23353-23360.
48. Kruip, J., Chitnis, P.R., Lagoutte, B., Rögner, M., and Boekema, E.J. (1997). Structural organization of the major subunits in cyanobacterial photosystem 1. Localization of subunits PsaC,-D,-E,-F, and-J. J. Biol. Chem. 272: 17061-17069.
49. LeBlanc, G., Chen, G., Jennings, G.K., and Cliffel, D.E. (2012). Photoreduction of catalytic platinum particles using immobilized multilayers of Photosystem I. Langmuir 28: 7952-7956.
50. Mangels, D., Kruip, J., Berry, S., Rögner, M., Boekema, E.J., and Koenig, F. (2002). Photosystem I from the unusual cyanobacterium Gloeobacter violaceus. Photosynth. Res. 72: 307-319.
51. Mareš, J., Hrouzek, P., Kaňa, R., Ventura, S., Strunecký, O., and Komárek, J. (2013). The primitive thylakoid-less cyanobacterium gloeobacter is a common rock-dwelling organism. PLoS ONE 8: e66323.
52. Mershin, A., Matsumoto, K., Kaiser, L., Yu, D., Vaughn, M., Nazeeruddin, M.K., Bruce, B.D., Graetzel, M., and Zhang, S. (2012). Self-assembled photosystem-I biophotovoltaics on nanostructured TiO(2)and ZnO. Sci Rep 2: 234.
53. Mukherjee, D., Vaughn, M., Khomami, B., and Bruce, B.D. (2011). Modulation of cyanobacterial photosystem I deposition properties on alkanethiolate Au substrate by various experimental conditions. Colloids Surf. B Biointerfaces 88: 181-190.
54. Nelson, N., and Ben-Shem, A. (2005). The structure of photosystem I and evolution of photosynthesis. Bioessays 27: 914-922.
55. Nelson, N., and Yocum, C.F. (2006). Structure and function of photosystems I and II. Annu. Rev. Plant Biol. 57: 521-565.
56. Nesterenko, M.V., Tilley, M., and Upton, S.J. (1994). A simple modification of Blum's silver stain method allows for 30 minute detection of proteins in polyacrylamide gels. J. Biochem. Biophys. Methods 28: 239-242.
57. Notredame, C., Higgins, D.G., and Heringa, J. (2000). T-Coffee: A novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302: 205-217.
58. Olson, D.G., Tripathi, S.A., Giannone, R.J., Lo, J., Caiazza, N.C., Hogsett, D.A., Hettich, R.L., Guss, A.M., Dubrovsky, G., and Lynd, L.R. (2010). Deletion of the Cel48S cellulase from Clostridium thermocellum. Proc. Natl. Acad. Sci. USA 107: 17727-17732.
59. Onai, K., Morishita, M., Kaneko, T., Tabata, S., and Ishiura, M. (2004). Natural transformation of the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1: A simple and efficient method for gene transfer. Mol. Genet. Genomics 271: 50-59.
60. Oostergetel, G.T., Keegstra, W., and Brisson, A. (1998). Automation of specimen selection and data acquisition for protein electron crystallography. Ultramicroscopy 74: 47-59.
61. Schägger, H. (2006). Tricine-SDS-PAGE. Nat. Protoc. 1: 16-22.
62. Schägger, H., and von Jagow, G. (1991). Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal. Biochem. 199: 223-231.
63. Schlodder, E., Hussels, M., Cetin, M., Karapetyan, N.V., and Brecht, M. (2011). Fluorescence of the various red antenna states in photosystem I complexes from cyanobacteria is affected differently by the redox state of P700. Biochim. Biophys. Acta 1807: 1423-1431.
64. Schluchter, W.M., Shen, G.H., Zhao, J.D., and Bryant, D.A. (1996). Characterization of psaI and psaL mutants of Synechococcus sp. strain PCC 7002: A new model for state transitions in cyanobacteria. Photochem. Photobiol. 64: 53-66.
65. Shih, P.M., et al. (2013). Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc. Natl. Acad. Sci. USA 110: 1053-1058.
66. Tabb, D.L., Fernando, C.G., and Chambers, M.C. (2007). MyriMatch: Highly accurate tandem mass spectral peptide identification by multivariate hypergeometric analysis. J. Proteome Res. 6: 654-661.
67. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731-2739.
68. Tsiotis, G., Haase, W., Engel, A., and Michel, H. (1995). Isolation and structural characterization of trimeric cyanobacterial photosystem I complex with the help of recombinant antibody fragments. Eur. J. Biochem. 231: 823-830.
69. Tucker, D.L., and Sherman, L.A. (2000). Analysis of chlorophyllprotein complexes from the cyanobacterium Cyanothece sp. ATCC 51142 by non-denaturing gel electrophoresis. Biochim. Biophys. Acta 1468: 150-160.
70. Umena, Y., Kawakami, K., Shen, J.-R., and Kamiya, N. (2011). Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473: 55-60.
71. Veith, T., and Büchel, C. (2007). The monomeric photosystem Icomplex of the diatom Phaeodactylum tricornutum binds specific fucoxanthin chlorophyll proteins (FCPs) as light-harvesting complexes. Biochim. Biophys. Acta 1767: 1428-1435.
72. Washburn, M.P., Wolters, D., and Yates, J.R., III., (2001). Largescale analysis of the yeast proteome by multidimensional protein identification technology. Nat. Biotechnol. 19: 242-247.
73. Watanabe, M., Iwai, M., Narikawa, R., and Ikeuchi, M. (2009). Is the photosystem II complex a monomer or a dimer? Plant Cell Physiol. 50: 1674-1680.
74. Watanabe, M., Kubota, H., Wada, H., Narikawa, R., and Ikeuchi, M. (2011). Novel supercomplex organization of photosystem I in Anabaena and Cyanophora paradoxa. Plant Cell Physiol. 52: 162-168.
75. Watanabe, M., Semchonok, D.A., Webber-Birungi, M.T., Ehira, S., Kondo, K., Narikawa, R., Ohmori, M., Boekema, E.J., and Ikeuchi, M. (2014). Attachment of phycobilisomes in an antennaphotosystem I supercomplex of cyanobacteria. Proc. Natl. Acad. Sci. USA 111: 2512-2517.
76. Waterbury, J.B., and Stanier, R.Y. (1978). Patterns of growth and development in pleurocapsalean cyanobacteria. Microbiol. Rev. 42: 2-44.
77. Wittig, I., Braun, H.-P., and Schägger, H. (2006). Blue native PAGE. Nat. Protoc. 1: 418-428.
78. Xu, Q., Hoppe, D., Chitnis, V.P., Odom, W.R., Guikema, J.A., and Chitnis, P.R. (1995). Mutational analysis of photosystem I polypeptides in the cyanobacterium Synechocystis sp. PCC 6803. Targeted inactivation of psaI reveals the function of psaI in the structural organization of psaL. J. Biol. Chem. 270: 16243-16250.
79. Xu, W., Tang, H.D., Wang, Y.C., and Chitnis, P.R. (2001). Proteins of the cyanobacterial photosystem I. Biochim. Biophys. Acta 1507: 32-40.
80. Zang, X., Liu, B., Liu, S., Arunakumara, K.K., and Zhang, X. (2007). Optimum conditions for transformation of Synechocystis sp. PCC 6803. J. Microbiol. 45: 241-245.