Global gene expression of a ΔpsbO:ΔPsbU mutant and a spontaneous revertant in the cyanobacterium Synechocystis sp. strain PCC 6803

Photosynthesis Research

Volumn 94, Issue 2-3, 2007, Pages 265-274

  Summerfield, Tina C ^a   Eaton Rye, Julian J ^b   Sherman, Louis A ^a  

^a PURDUE UNIVERSITY   (United States)

^b UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Cyanobacteria; DNA microarray; Histidine kinase; Oxygen evolving complex; pH; Photosystem II; PsbO; PsbU; Stress response; Synechocystis

Indexed keywords

BACTERIAL PROTEIN; PROTEIN HISTIDINE KINASE; PROTEIN KINASE; PROTEIN-HISTIDINE KINASE; PSBU PROTEIN, SYNECHOCYSTIS; UNCLASSIFIED DRUG;

ARTICLE; BIOLOGICAL MODEL; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; MUTATION; PH; PHOTOSYSTEM II; SYNECHOCYSTIS;

BACTERIAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; HYDROGEN-ION CONCENTRATION; MODELS, BIOLOGICAL; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOTOSYSTEM II PROTEIN COMPLEX; PROTEIN KINASES; SYNECHOCYSTIS;

CYANOBACTERIA; SYNECHOCYSTIS; SYNECHOCYSTIS SP.;

EID: 36849034637     PISSN: 01668595     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11120-007-9237-2     Document Type: Article

References (61)

1. Baldi P, Long AD (2001) A Bayesian framework for the analysis of microarray expression data: regularized t-test and statistical inferences of gene changes. Bioinformatics 17:509-519
2. Balint I, Bhattacharya J, Perelman A, Schatz D, Moskovitz Y, Keren N, Schwarz R (2006) Inactivation of the extrinsic subunit of photosystem II, PsbU, in Synechococcus PCC 7942 results in elevated resistance to oxidative stress. FEBS Lett 580:2117-2122
3. Barker M, de Vries R, Nield J, Komenda J, Nixon PJ (2006) The Deg proteases protect Synechocystis sp. PCC 6803 during heat and light stresses but are not essential for removal of damaged D1 protein during the photosystem two repair cycle. J Biol Chem 281:30347-30355
4. Bhaya D, Bianco NR, Bryant D, Grossman A (2000) Type IV pilus biogenesis and motility in the cyanobacterium Synechocystis sp. PCC6803. Mol Microbiol 37:941-951
5. Bockholt R, Masepohl B, Pistorius EK (1991) Insertional inactivation of the psbO gene encoding the manganese stabilizing protein of photosystem II in the cyanobacterium Synechococcus PCC7942. Effect on photosynthetic water oxidation and L-amino acid oxidase activity. FEBS Lett 294:59-63
6. 2 evolution. Biochemistry 30:440-446
7. 2O oxidation complex in Synechocystis sp. PCC6803. Biochemistry 35:874-882
8. Clarke SM, Eaton-Rye JJ (1999) Mutation of Phe-363 in the photosystem II protein CP47 impairs photoautotrophic growth, alters the chloride requirement, and prevents photosynthesis in the absence of either PSII-O or PSII-V in Synechocystis sp. PCC 6803. Biochemistry 38:2707-2715
9. Colon-Lopez MS, Sherman DM, Sherman LA (1997) Transcriptional and translational regulation of nitrogenase in light-dark- and continuous-light- grown cultures of the unicellular cyanobacterium Cyanothece sp. strain ATCC 51142. J Bacteriol 179:4319-4327
10. Duguay AR, Silhavy TJ (2004) Quality control in the bacterial periplasm. Biochim Biophys Acta 1694:121-134
11. Eaton-Rye JJ, Shand JA, Nicoll WS (2003) pH-dependent photoautotrophic growth of specific photosystem II mutants lacking lumenal extrinsic polypeptides in Synechocystis PCC 6803. FEBS Lett 543:148-153
12. Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831-1838
13. Fulda S, Huang F, Nilsson F, Hagemann M, Norling B (2000) Proteomics of Synechocystis sp. strain PCC 6803. Identification of periplasmic proteins in cells grown at low and high salt concentrations. Eur J Biochem 267:5900-5907
14. He Q, Vermaas W (1999) Genetic deletion of proteins resembling Type IV pilins in Synechocystis sp. PCC 6803: their role in binding or transfer of newly synthesized chlorophyll. Plant Mol Biol 39:1175-1188
15. Huang F, Hedman E, Funk C, Kieselbach T, Scroder WP, Norling B (2004) Isolation of outer membrane of Synechocystis sp. PCC 6803 and its proteomic characterization. Mol Cell Prot 3:586-595
16. Huang F, Fulda S, Hagemann M, Norling B (2006) Proteomic screening of salt-stress-induced changes in plasma membranes of Synechocystis sp. strain PCC 6803. Proteomics 6:910-920
17. Inoue-Kashino N, Kashino Y, Satoh K, Terashima I, Pakrasi HB (2005) PsbU provides a stable architecture for the oxygen-evolving system in cyanobacterial photosystem II. Biochemistry 44:12214-12228
18. Ishikawa Y, Schroder WP, Funk C (2005) Functional analysis of the PsbP-like protein (sll1418) in Synechocystis sp. PCC 6803. Photosynth Res 84:257-262
19. Jansen T, Kidron H, Soitamo A, Salminen T, Maenpaa P (2003) Transcriptional regulation and structural modelling of the Synechocystis sp. PCC 6803 carboxyl-terminal endoprotease family. FEMS Microbiol Lett 228:121-128
20. 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 (1996) 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 3:109-136
21. Kaneko T, Nakamura Y, Sasamoto S, Watanabe A, Kohara M, Matsumotot M, Shimpo S, Yamada M, Tabata S (2003) Structural analysis of four large plasmids harboring in a unicellular cyanobacterium, Synechocystis sp. PCC 6803. DNA Res 10:221-228
22. Kanesaki Y, Yamamoto H, Paithoonrangsarid K, Shoumskaya M, Suzuki I, Hayashi H, Murata N. (2007) Histidine kinases play important roles in the perception and signal transduction of hydrogen peroxide in the cyanobacterium, Synechocystis sp. PCC 6803. Plant J 49:313-324
23. Kashino Y Lauber WM, Carroll JA, Wang QJ, Whitmarsh J, Satoh K, Pakrasi HB (2002) Proteomic analysis of a highly active photosystem II preparation from the cyanobacterium Synechocystis sp. PCC 6803 reveals the presence of novel polypeptides. Biochemistry 41:8004-8012
24. Kimura A, Eaton-Rye JJ, Morita EH, Nishiyama Y, Hayashi H (2002) Protection of the oxygen-evolving machinery by the extrinsic proteins of Photosystem II is essential for development of cellular thermotolerance in Synechocystis sp. PCC 6803. Plant Cell Physiol 43:932-938
25. Li H, Singh AK, McIntyre LM, Sherman LA (2004) Differential gene expression in response to hydrogen peroxide and the putative PerR regulon of Synechocystis sp. strain PCC 6803. J Bacteriol 186:3331-3345
26. 550 of photosystem II in Synechocystis sp. PCC6803. Biochemistry 43:14161-14170
27. Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438:1040-1044
28. Long AD, Mangalam HJ, Chan BY, Tolleri L, Hatfield GW, Baldi P (2001) Improved statistical inference from DNA microarray data using analysis of variance and a Bayesian statistical framework. Analysis of global gene expression in Escherichia coli K12. J Biol Chem 276:19937-19944
29. Mayes SR, Cook KM, Self SJ, Zhang Z, Barber J (1991) Deletion of the gene encoding the Photosystem II 33 kDa protein from Synechocystis sp. PCC 6803 does not inactivate water-splitting but increases vulnerability to photoinhibition. Biochim Biophys Acta 1060:1-12
30. Meunier PC, Colon-Lopez MS, Sherman LA (1997) Temporal changes in state transitions and photosystem organization in the unicellular, diazotrophic cyanobacterium Cyanothece sp. ATCC 51142. Plant Physiol 115:991-1000
31. Morgan TR, Shand JA, Clarke SM, Eaton-Rye JJ (1998) Specific requirements for cytochrome c-550 and the manganese-stabilizing protein in photoautotrophic strains of Synechocystis sp. PCC 6803 with mutations in the domain Gly-351 to Thr-436 of the chlorophyll-binding protein CP47. Biochemistry 37:14437-14449
32. Murata N, Suzuki I (2006) Exploitation of genomic sequences in a systematic analysis to access how cyanobacteria sense environmental stress. J Exp Bot 57:235-247
33. Nakai M, Sugita D, Omata T, Endo T (1993) Sec-Y protein is localized in both the cytoplasmic and thylakoid membranes in the cyanobacterium Synechococcus PCC7942. Biochem Biophys Res Commun 193:228-234
34. Nakai M, Nohara T, Sugita D, Endo T (1994) Identification and characterization of the sec-A protein homologue in the cyanobacterium Synechococcus PCC7942. Biochem Biophys Res Commun 200:844-851
35. Nishiyama Y, Los DA, Murata N (1999) PsbU, a protein associated with Photosystem II, is required for the acquisition of cellular thermotolerance in Synechococcus species PCC 7002. Plant Physiol 120:301-308
36. Nishiyama Y, Yamamoto H, Allakhverdiev SI, Inaba M, Yokota A, Murata N (2001) Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO J 20:5587-5594
37. Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta 1757:742-749
38. Paithoonrangsarid K Shoumskaya MA, Kanesaki Y, Satoh S, Tabata S, Los DA, Zinchenko VV, Hayashi H, Tanticharoen M, Suzuki I, Murata N (2004) Five histidine kinases perceive osmotic stress and regulate distinct sets of genes in Synechocystis. J Biol Chem 279:53078-53086
39. Philbrick JB, Diner BA, Zilinskas BA (1991) Construction and characterization of cyanobacterial mutants lacking the manganese-stabilizing polypeptide of photosystem II. J Biol Chem 266:13370-13376
40. Postier BL Wang HL, Singh A, Impson L, Andrews HL, Klahn J, Li H, Risinger G, Pesta D, Deyholos M, Galbraith DW, Sherman LA, Burnap RL (2003) The construction and use of bacterial DNA microarrays based on an optimized two-stage PCR strategy. BMC Genomics 4:23
41. Raivio TL, Silhavy TJ (2001) Periplasmic stress and ECF sigma factors. Annu Rev Microbiol 55:591-624
42. Reddy KJ, Webb R, Sherman LA (1990) Bacterial RNA isolation with one hour centrifugation in a table-top ultracentrifuge. Biotechniques 8:250-251
43. Roose JL, Kashino Y, Pakrasi HB (2007) The PsbQ protein defines cyanobacterial Photosystem II complexes with highest activity and stability. Proc Natl Acad Sci USA 104:2548-2553
44. Shen JR, Inoue Y (1993) Binding and functional properties of two new extrinsic components, cytochrome c-550 and a 12-kDa protein, in cyanobacterial photosystem II. Biochemistry 32:1825-1832
45. Shen JR, Burnap RL, Inoue Y (1995) An independent role of cytochrome c-550 in cyanobacterial photosystem II as revealed by double-deletion mutagenesis of the psbO and psbV genes in Synechocystis sp. PCC 6803. Biochemistry 34:12661-12668
46. Shen JR, Ikeuchi M, Inoue Y (1997) Analysis of the psbU gene encoding the 12-kDa extrinsic protein of photosystem II and studies on its role by deletion mutagenesis in Synechocystis sp. PCC 6803. J Biol Chem 272:17821-17826
47. 550 in cyanobacterial oxygen evolution. Biochemistry 37:1551-1558
48. Shoumskaya MA, Paithoonrangsarid K, Kanesaki Y, Los DA, Zinchenko VV, Tanticharoen M, Suzuki I, Murata N (2005) Identical Hik-Rre systems are involved in perception and transduction of salt signals and hyperosmotic signals but regulate the expression of individual genes to different extents in Synechocystis. J Biol Chem 280:21531-21538
49. Singh AK, Sherman LA (2002) Characterization of a stress-responsive operon in the cyanobacterium Synechocystis sp. strain PCC 6803. Gene 297:11-19
50. Singh AK, Sherman LA (2007) Reflections on the function of IsiA, a cyanobacterial stress-inducible, Chl-binding protein. Photosynth Res. doi: 10.10007/s11120-007-9151-7
51. Singh AK, McIntyre LM, Sherman LA (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
52. Singh AK, Summerfield TC, Li H, Sherman LA (2006) The heat shock response in the cyanobacterium Synechocystis sp. Strain PCC 6803 and regulation of gene expression by HrcA and SigB. Arch Microbiol 186:273-286
53. Srivastava R, Pisareva T, Norling B (2005) Proteomic studies of the thylakoid membrane of Synechocystis sp. PCC 6803. Proteomics 5:4905-4916
54. Summerfield TC, Shand JA, Bentley FK, Eaton-Rye JJ (2005a) PsbQ (Sll1638) in Synechocystis sp. PCC 6803 is required for photosystem II activity in specific mutants and in nutrient-limiting conditions. Biochemistry 44:805-815
55. Summerfield TC, Winter RT, Eaton-Rye JJ (2005b) Investigation of a requirement for the PsbP-like protein in Synechocystis sp. PCC 6803. Photosynth Res 84:263-268
56. Suzuki I, Kanesaki Y, Hayashi H, Hall JJ, Simon WJ, Slabas AR, Murata N (2005) The histidine kinase Hik34 is involved in thermotolerance by regulating the expression of heat shock genes in Synechocystis. Plant Physiol 138:1409-1421
57. Thornton LE, Ohkawa H, Roose JL, Kashino Y, Keren N, Pakrasi HB (2004) Homologs of plant PsbP and PsbQ proteins are necessary for regulation of Photosystem II activity in the cyanobacterium Synechocystis 6803. Plant Cell 16:2164-2175
58. Veerman J, Bentley FK, Eaton-Rye JJ, Mullineaux CW, Vasil'ev S, Bruce D (2005) The PsbU subunit of photosystem II stabilizes energy transfer and primary photochemistry in the phycobilisome-photosystem II assembly of Synechocystis sp. PCC 6803. Biochemistry 44:16939-16948
59. Williams JGK (1988) Construction of specific mutations in photosystem II photosynthetic reaction center by genetic engineering methods in Synechocystis 6803. In: Parker L, Glazer AN (eds). Methods in enzymology. Academic Press, San Diego, pp 766-778
60. Wilson A, Ajlani G, Verbavatz JM, Vass I, Kerfeld CA, Kirilovsky D (2006) A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria. Plant Cell 18:992-1007
61. Zak E, Norling B, Maitra R, Huang F, Andersson B, Pakrasi HB (2001) The initial steps of biogenesis of cyanobacterial photosystems occur in plasma membranes. Proc Natl Acad Sci USA 98:13443-13448