Dynamic changes in the proteome of synechocystis 6803 in response to CO2 limitation revealed by quantitative proteomics

Journal of Proteome Research

Volumn 9, Issue 11, 2010, Pages 5896-5912

  Battchikova, Natalia ^a   Vainonen, Julia P ^a,b   Vorontsova, Natalia ^a   Kerãnen, Mika ^a   Carmel, Dalton ^a   Aro, Eva Mari ^a  

^a UNIVERSITY OF TURKU   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

acclimation; CO2 uptake; iTRAQ; photoprotection; photosynthesis; Synechocystis

Indexed keywords

BACTERIAL PROTEIN; BICARBONATE TRANSPORT SYSTEM ATP BINDING PROTEIN CMPC; BICARBONATE TRANSPORT SYSTEM ATP BINDING PROTEIN CMPD; BICARBONATE TRANSPORT SYSTEM SUBSTRATE BINDING PROTEIN CMPA; BICARBONATE TRANSPORT SYSTEM SUBSTRATE BINDING PROTEIN CMPB; CARBON DIOXIDE; CARBON DIOXIDE CONCENTRATIN MECHANISM PROTEIN CCMK1; CARBON DIOXIDE CONCENTRATING MECHANISM PROTEIN CCMK2; CARBON UPTAKE PROTEIN CUPA; CARBON UPTAKE PROTEIN CUPS; CHAPERONE; FLAVOPROTEIN FLV2; FLAVOPROTEIN FLV3; NDHA PROTEIN; NDHD3 PROTEIN; NDHG PROTEIN; NDHH PROTEIN; NDHI PROTEIN; NDHJ PROTEIN; NDHK PROTEIN; NDHM PROTEIN; NDHN PROTEIN; NDHO PROTEIN; PROTEOME; RIBULOSE BISPHOSPHATE CARBOXYLASE LARGE SUBUNIT PROTEIN; RIBULOSE BISPHOSPHATE CARBOXYLASE SMALL SUBUNIT PROTEIN; SODIUM DEPENDENT BICARBONATE TRANSPORT SBTA; SODIUM DEPENDENT BICARBONATE TRANSPORT SBTB; UNCLASSIFIED DRUG; UNINDEXED DRUG; WATER SOLUBLE CAROTENOID PROTEIN;

ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; CARBON DIOXIDE FIXATION; CONTROLLED STUDY; DOWN REGULATION; EXTRACTION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; OPEN READING FRAME; PHOTOSYNTHESIS; PHYCOBILISOME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; QUANTITATIVE ANALYSIS; STRESS; SYNECHOCYSTIS; UPREGULATION; WESTERN BLOTTING;

BACTERIAL PROTEINS; CARBON; CARBON DIOXIDE; CYANOBACTERIA; GENE EXPRESSION REGULATION; KINETICS; PROTEOME; PROTEOMICS; SYNECHOCYSTIS; TANDEM MASS SPECTROMETRY;

CYANOBACTERIA; SYNECHOCYSTIS; SYNECHOCYSTIS SP. PCC 6803;

EID: 78149364258     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr100651w     Document Type: Article

References (76)

1. 2 acquisition, concentration and fixation in cyanobacteria and algae. In: Photosynthesis: Physiology and Metabolism; Leegood, R. C.; Sharkey, T. D.; von Caemmerer, S.; Eds.; Kluwer Academy Publishers: Dordrecht, 2000; pp 369 - 397.
2. 2 concentrating mechanisms in photosynthetic microorganisms Ann. Rev. Plant Physiol. Plant Mol. Biol. 1999, 50, 539-570 (Pubitemid 129491973)
3. 2 concentrating mechanisms in cyanobacteria Funct. Plant. Biol. 2002, 29, 161-173
4. Ogawa, T.; Kaplan, A. Inorganic carbon acquisition systems in cyanobacteria Photosynth. Res. 2003, 77, 105-115
5. Volokita, M.; Zenvirth, D.; Kaplan, A.; Reinhold, L. Nature of the inorganic carbon species actively taken up by the cyanobacterium Anabaena variabilis Plant Physiol. 1984, 76, 599-602
6. 2 fixation Funct. Plant Biol. 2002, 29, 117-121
7. Kaneko, T.; Sato, S.; Kotani, H.; Tanaka, A.; Asamizu, E.; Nakamura, Y.; Miyajima, N.; Hirosawa, M.; Sugiura, M.; Sasamoto, S.; Kimura, T.; Hosouchi, T.; Matsuno, A.; Muraki, A.; Nakazaki, N.; Naruo, K.; Okumura, S.; Shimpo, S.; Takeuchi, C.; Wada, T.; Watanabe, A.; Yamada, M.; Yasuda, M.; Tabata, S. Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions DNA Res. 1996, 3, 109-136 (Pubitemid 126682789)
8. 2 concentration Plant Physiol. 1986, 80, 525-530
9. Omata, T.; Price, G. D.; Badger, M. R.; Okamura, M.; Gohta, S.; Ogawa, T. Identification of an ATP-binding cassette transporter involved in bicarbonate uptake in the cyanobacterium Synechococcus sp. strain PCC 7942 Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 13571-13576
10. Shibata, M.; Katoh, H.; Sonoda, M.; Ohkawa, H.; Shimoyama, M.; Fukuzawa, H.; Kaplan, A.; Ogawa, T. Genes essential to sodium-dependent bicarbonate transport in cyanobacteria: function and phylogenetic analysis J. Biol. Chem. 2002, 277, 18658-18664
11. Battchikova, N.; Aro, E. M. Cyanobacterial NDH-1 complexes: multiplicity in function and subunit composition Physiol. Plant. 2007, 131, 22-32
12. 2 uptake in Synechococcus sp. PCC7002 gives evidence for multiple NDH-1 complexes with specific roles in cyanobacteria Mol. Microbiol. 1999, 32, 1305-1315
13. Ohkawa, H.; Pakrasi, H. B.; Ogawa, T. Two types of functionally distinct NAD(P)H dehydrogenases in Synechocystis sp. strain PCC6803 J. Biol. Chem. 2000, 275, 31630-31634
14. 2-concentrating mechanism in the cyanobacterium Synechocystis sp. strain PCC6803 Plant Physiol. 2003, 132, 218-229
15. Wang, H. L.; Postier, B. L.; Burnap, R. L. Alterations in global patterns of gene expression in Synechocystis sp. PCC 6803 in response to inorganic carbon limitation and the inactivation of ndhR, a LysR family regulator J. Biol. Chem. 2004, 279, 5739-5751
16. Eisenhut, M.; von Wobeser, E. A.; Jonas, L.; Schubert, H.; Ibelings, B. W.; Bauwe, H.; Matthijs, H. C.; Hagemann, M. Long-term response toward inorganic carbon limitation in wild type and glycolate turnover mutants of the cyanobacterium Synechocystis sp. strain PCC 6803 Plant Physiol. 2007, 144, 1946-1959
17. Herranen, M.; Battchikova, N.; Zhang, P.; Graf, A.; Sirpiö, S.; Paakkarinen, V.; Aro, E. M. Towards functional proteomics of membrane protein complexes in Synechocystis sp. PCC 6803 Plant Physiol. 2004, 134, 470-481
18. Zhang, P.; Battchikova, N.; Jansen, T.; Appel, J.; Ogawa, T.; Aro, E. M. Expression and functional roles of the two distinct NDH-1 complexes and the carbon acquisition complex NdhD3/NdhF3/CupA/Sll1735 in Synechocystis sp PCC 6803 Plant Cell 2004, 16, 3326-3340
19. Zhang, P.; Battchikova, N.; Paakkarinen, V.; Katoh, H.; Iwai, M.; Ikeuchi, M.; Pakrasi, H. B.; Ogawa, T.; Aro, E. M. Isolation, subunit composition and interaction of the NDH-1 complexes from Thermosynechococcus elongatus BP-1 Biochem. J. 2005, 390, 513-520
20. Battchikova, N.; Zhang, P.; Rudd, S.; Ogawa, T.; Aro, E. M. Identification of NdhL and Ssl1690 (NdhO) in NDH-1L and NDH-1M complexes of Synechocystis sp. PCC 6803 J. Biol. Chem. 2005, 280, 2587-2595
21. Ross, P. L.; Huang, Y. N.; Marchese, J. N.; Williamson, B.; Parker, K.; Hattan, S.; Khainovski, N.; Pillai, S.; Dey, S.; Daniels, S.; Purkayastha, S.; Juhasz, P.; Martin, S.; Bartlet-Jones, M.; He, F.; Jacobson, A.; Pappin, D. J. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents Mol. Cell. Proteomics 2004, 3, 1154-1169
22. Rippka, R. Isolation and purification of cyanobacteria Methods Enzymol. 1988, 167, 3-27
23. Shilov, I. V.; Seymour, S. L.; Patel, A. A.; Loboda, A.; Tang, W. H.; Keating, S. P.; Hunter, C. L.; Nuwaysir, L. M.; Schaeffer, D. A. The Paragon algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra Mol. Cell. Proteomics 2007, 6, 1638-1655
24. Tang, W. H.; Shilov, I. V.; Seymour, S. L. Nonlinear fitting method for determining local false discovery rates from decoy database searches J. Proteome Res. 2008, 7, 3661-3667
25. Laemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 1970, 227, 680-685
26. Zhang, P.; Allahverdiyeva, Y.; Eisenhut, M.; Aro, E. M. Flavodiiron proteins in oxygenic photosynthetic organisms: photoprotection of photosystem II by Flv2 and Flv4 in Synechocystis sp. PCC 6803 PLoS One 2009, 4, 1-12
27. Liu, H.; Bergman, N. H.; Thomason, B.; Shallom, S.; Hazen, A.; Crossno, J.; Rasko, D. A.; Ravel, J.; Read, T. D.; Peterson, S. N.; Yates III, J.; Hanna, P. C. Formation and composition of the Bacillus anthracis endospore J. Bacteriol. 2004, 186, 164-178
28. Scherl, A.; Francois, P.; Bento, M.; Deshusses, J. M.; Charbonnier, Y.; Converset, V.; Huyghe, A.; Walter, N.; Hoogland, C.; Appel, R. D.; Sanchez, J. C.; Zimmermann-Ivol, C. G.; Corthals, G. L.; Hochstrasser, D. F.; Schrenzel, J. Correlation of proteomics and transcriptomics profiles of Staphylococcus aureus during the post-exponential phase of growth J. Microbiol. Methods 2005, 60, 247-257
29. Corbin, R. W.; Paliy, O.; Yang, F.; Shabanowitz, J.; Platt, M.; Lyons, C. E.; Root, K.; McAuliffe, J.; Jordan, M. I.; Kustu, S.; Soupene, E.; Hunt, D. F. Toward a protein profile of Escherichia coli: comparison to its transcription profiling Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 9232-9237
30. Barrios-Llerena, M. E.; Chong, P. K.; Gan, C. S.; Snijders, A. P. L.; Reardon, K. F.; Wright, P. C. Short-gun proteomics of cyanobacteria-applications for experimental and data-mining techniques Briefings Funct. Genomics Proteomics 2007, 5, 121-132
31. Gan, C. S.; Reardon, K. F.; Wright, P. C. Comparison of protein and peptide prefractionation methods for the shotgun proteomic analysis of Synechocystis sp. PCC 6803 Proteomics 2004, 5, 2468-2478
32. Chong, P. K.; Gan, C. S.; Pham, T. K.; Wright, P. C. Isobaric tags for relative and absolute quantitation (iTRAQ) reproducibility: Implication of multiple injections J. Proteome Res. 2006, 5, 1232-1240
33. Ow, S. Y.; Wright, P. C. Current trends in high throughput proteomics in cyanobacteria FEBS Lett. 2009, 583, 1744-1752
34. DeRuyter, Y. S.; Fromme, P. Molecular structure of the photosynthetic apparatus. In The Cyanobacteria. Molecular Biology, Genetics and Evolution; Herrero, A.; Flores, E.; Eds.; Caister Academic Press: Norfolk, 2008; pp 217 - 270.
35. 2 concentration in the cyanobacterium Synechocystis PCC6803 J. Plant Physiol. 2003, 160, 967-970
36. 2 on NAD(P)H dehydrogenase, a mediator of cyclic electron transport around photosystem I in the cyanobacterium Synechocystis PCC6803 Plant Cell Physiol. 2003, 44, 534-540
37. Ogawa, T.; Mi, H. Cyanobacterial NADPH dehydrogenase complexes Photosynth. Res. 2007, 93, 69-77
38. 2 uptake systems in cyanobacteria: genes involved and their phylogenetic relationship with homologous genes in other organisms Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 11789-11794
39. Pasquier, C.; Hamodrakas, S. J. An hierarchical artificial neural network system for the classification of transmembrane proteins Protein Eng. 1999, 12, 631-634
40. Xu, M.; Ogawa, T.; Pakrasi, H. B.; Mi, H. Identification and localization of the CupB protein involved in constitutive CO2 uptake in the cyanobacterium, Synechocystis sp. strain PCC 6803 Plant Cell Physiol. 2008, 49, 994-997
41. 2-concentrating-mechanisms (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants J. Exp. Bot. 2008, 59, 1441-1461
42. Omata, T.; Gohta, S.; Takahashi, Y.; Harano, Y.; Maeda, S. I. Involvement of a CbbR homolog in low CO2-induced activation of the bicarbonate transporter operon in cyanobacteria J. Bacteriol. 2001, 183, 1891-1898
43. Woodger, F. J.; Badger, M. R.; Price, G. D. Inorganic carbon limitation induces transcripts encoding components of the CO2-concentrating mechanism in Synechococcus sp. PCC7942 through a redox-independent pathway Plant Physiol. 2003, 133, 2069-2080
44. Heinhorst, S.; Cannon, G.; Shively, J. M. Carboxysomes and carboxysome-like inclusions. In: Microbiology Monographs. Complex Intracellular Structures in Prokaryotes; Shively, J. M., Ed.; Springer: Berlin, Heidelberg, NY, 2006; pp 141 - 166.
45. Kerfeld, C. A. Water-soluble carotenoid proteins of cyanobacteria Arch. Biochem. Biophys. 2004, 430, 2-9
46. Wilson, A.; Ajlani, G.; Verbavatz, J. M.; Vass, I.; Kerfeld, C. A.; Kirilovsky, D. A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria Plant Cell 2006, 18, 992-1007
47. 2 in cyanobacteria Curr. Biol. 2003, 13, 230-235
48. Gaber, A.; Tamoi, M.; Takeda, T.; Nakano, Y.; Shigeoka, S. NADPH-dependent glutathione peroxidase-like proteins (Gpx-1, Gpx-2) reduce unsaturated fatty acid hydroperoxides in Synechocystis PCC 6803 FEBS Lett. 2001, 499, 32-36
49. Gaber, A.; Yoshimura, K.; Yamamoto, T.; Yabuta, Y.; Takeda, T.; Miyasaka, H.; Nakano, Y.; Shigeoka, S. Glutathione peroxidase-like protein of Synechocystis PCC 6803 confers tolerance to oxidative and environmental stresses in transgenic Arabidopsis Physiologia Plantarum 2006, 128, 251-262
50. Bernroitner, M.; Zamocky, M.; Furtmüller, P. G.; Peschek, G. A.; Obinger, C. Occurrence, phylogeny, structure, and function of catalases and peroxidases in cyanobacteria J. Exp. Botany 2009, 60, 423-440
51. II signal transduction in cyanobacteria: from signals to targets FEMS Microbiology Rev. 2004, 28, 319-333
52. Reyes, J. C.; Muro-Pastor, M. J.; Florencio, F. J. Transcription of glutamine synthetase genes (glnA and glnN) from the cyanobacterium Synechocystis sp. strain PCC 6803 is differently regulated in response to nitrogen availability J. Bacteriol. 1997, 179, 2678-2689
53. Ellis, R. J.; Hartl, F. U. Protein folding in the cell: competing models of chaperonin function FASEB J. 1996, 10, 20-26
54. Fulda, S.; Mikkat, S.; Huang, F.; Huckauf, J.; Marin, K.; Norling, B.; Hagemann, M. Proteome analysis of salt stress response in the cyanobacterium Synechocystis sp. strain PCC 6803 Proteomics 2006, 6, 2733-2745
55. Castielli, O.; de la Cerda, B.; Navarro, J. A.; Hervás, M.; de la Rosa, M. A. Proteomic analyses of the response of cyanobacteria to different stress conditions FEBS Lett. 2009, 583, 1753-1758
56. Slabas, A. R.; Suzuki, I.; Murata, N.; Simon, W. J.; Hall, J. J. Proteomic analysis of the heat shock response in Synechocystis PCC 6803 and a thermally tolerant knockout strain lacking the histidine kinase 34 gene Proteomics 2006, 6, 845-864
57. Suzuki, I.; Simon, W. J.; Slabas, A. R. The heat shock response of Synechocystis sp. PCC 6803 analysed by transcriptomics and proteomics J. Exp. Bot. 2006, 57, 1573-1578
58. Kvint, K.; Nachin, L.; Diez, A.; Nyström, T. The bacterial universal stress protein: function and regulation Curr. Opin. Microbiol. 2003, 6, 140-145
59. Teplova, M.; Tereshko, V.; Sanishvili, R.; Joachimiak, A.; Bushueva, T.; Anderson, W. F.; Egli, M. The structure of the yrdC gene product from Escherichia coli reveals a new fold and suggests a role in RNA binding Protein Sci. 2000, 9, 2557-2566
60. Kaczanowska, M.; Ryden-Aulin, M. The YrdC protein-a putative ribosome maturation factor Biochim. Biophys. Acta 2005, 1727, 87-96
61. El Yacoubi, B.; Lyons, B.; Cruz, Y.; Reddy, R.; Nordin, B.; Agnelli, F.; Williamson, J. R.; Schimmel, P.; Swairjo, M. A.; de Crécy-Lagard, V. The universal YrdC/Sua5 family is required for the formation of threonylcarbamoyladenosine in tRNA Nucleic Acid Res 2009, 37, 2894-2909
62. D'Andrea, L. D.; Regan, L. TPR proteins: the versatile helix Trends Biochem. Sci. 2003, 28, 655-662
63. Huang, F.; Parmryd, I.; Nilsson, F.; Persson, A. L.; Pakrasi, H. B.; Andersson, B.; Norling, B. Proteomics of Synechocystis sp. strain PCC 6803: identification of plasma membrane proteins Mol. Cell. Proteomics 2002, 1, 956-966
64. Huang, F.; Fulda, S.; Hagemann, M.; Norling, B. Proteomic screening of salt-stress-induced changes in plasma membranes of Synechocystis sp. strain PCC 6803 Proteomics 2006, 6, 910-920
65. Pisareva, T.; Shumskaya, M.; Maddalo, G.; Ilag, L.; Norling, B. Proteomics of Synechocystis sp. PCC 6803. Identification of novel integral plasma membrane proteins FEBS J. 2007, 274, 791-804
66. Zhang, L. F.; Yang, H. M.; Cui, S. X.; Hu, J.; Wang, J.; Kuang, T. Y.; Norling, B.; Huang, F. Proteomic analysis of plasma membranes of cyanobacterium Synechocystis sp. Strain PCC 6803 in response to high pH stress J. Proteome Res. 2009, 8, 2892-2902
67. Wegener, K. M.; Welsh, E. A.; Thornton, L. E.; Keren, N.; Jacobs, J. M.; Hixson, K. K.; Monroe, M. E.; Camp, D. G.; Smith, R. D.; Pakrasi, H. B. High sensitivity proteomics assisted discovery of a novel operon involved in the assembly of photosystem II, a membrane protein complex J. Biol. Chem. 2008, 283, 27829-27837
68. Kubota, H.; Sakurai, I.; Katayama, K.; Mizusawa, N.; Ohashi, S.; Kobayashi, M.; Zhang, P.; Aro, E. M.; Wada, H. Purification and characterization of photosystem I complex from Synechocystis sp. PCC 6803 by expressing histidine-tagged subunits Biochim. Biophys. Acta 2010, 1797, 98-105
69. Sato, S.; Shimoda, Y.; Muraki, A.; Kohara, M.; Nakamura, M.; Tabata, S. A large-scale protein-protein interaction analysis in Synechocystis sp. PCC6803 DNA Res. 2007, 14, 207-216
70. Nie, L.; Wu, G.; Culley, D. E.; Scholten, J. C. M.; Zhang, W. Integrative analysis of transcriptomic and proteomic data: challenges, solutions and applications Crit. Rev. Biotechnol. 2007, 27, 63-75
71. Hegde, P. S.; White, I. R.; Debouck, C. Interplay of transcriptomics and proteomics Curr. Opin. Biotech. 2003, 14, 647-651
72. Resch, A.; Leicht, S.; Saric, M.; Pasztor, L.; Jakob, A.; Götz, F.; Nordheim, A. Comparative proteome analysis of Staphylococcus aureus biofilm and planktonic cells and correlation with transcriptome profiling Proteomics 2006, 6, 1867-1877
73. Baliga, N. S.; Pan, M.; Goo, Y. A.; Yi, E. C.; Goodlett, D. R.; Dimitrov, K.; Shannon, P.; Aebersold, R.; Ng, W. V.; Hood, L. Coordinate regulation of energy transduction modules in Halobacterium sp. analyzed by a global systems approach Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 14913-14918
74. Griffin, T. J.; Gygi, S. P.; Ideker, T.; Rist, B.; Eng, J.; Hood, L.; Aebersold, R. Complementary profiling of gene expression at the transcriptome and proteome levels in Saccharomyces cerevisiae Mol. Cell. Proteomics 2002, 1.4, 323-333
75. de Groot, M. J.; Daran-Lapujade, P.; van Breukelen, B.; Knijnenburg, T. A.; de Hulster, E. A.; Reinders, M. J.; Pronk, J. T.; Heck, A. J.; Slijper, M. Quantitative proteomics and transcriptomics of anaerobic and aerobic yeast cultures reveals post-transcriptional regulation of key cellular processes Microbiology 2007, 153, 3864-3878
76. Rice, P.; Longden, I.; Bleasby, A. EMBOSS: The European Molecular Biology Open Software Suite. Trends in Genetics 2000, 16, 276-277