Characterization of the putative iron sulfur protein IdiC (ORF5) in Synechococcus elongatus PCC 7942

Photosynthesis Research

Volumn 94, Issue 1, 2007, Pages 91-108

  Pietsch, Daniel ^a   Staiger, Dorothee ^a   Pistorius, Elfriede K ^a   Michel, Klaus Peter ^a  

^a BIELEFELD UNIVERSITY   (Germany)

Author keywords

Ferredoxin:NADP+ oxidoreductase; IdiC; Iron limitation; NDH 1 complex; Photosynthetic and respiratory electron transport chain; Synechococcus elongatus PCC 7942

Indexed keywords

ANTIBODY; IRON SULFUR PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENOME; BIOLOGY; CHEMISTRY; ELECTRON TRANSPORT; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; MUTATION; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; SYNECHOCOCCUS;

AMINO ACID SEQUENCE; ANTIBODIES; COMPUTATIONAL BIOLOGY; ELECTRON TRANSPORT; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; IRON-SULFUR PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SYNECHOCOCCUS;

ESCHERICHIA COLI; IDIA; IRPA; SYNECHOCOCCUS ELONGATUS; SYNECHOCOCCUS ELONGATUS PCC 7942;

EID: 34548181371     PISSN: 01668595     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11120-007-9222-9     Document Type: Article

References (81)

1. 2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot 54:609-622
2. Barber J, Nield J, Duncan J, Bibby TS (2006) Accessory chlorophyll proteins in cyanobacterial photosystem I. In: Goldbeck JH (ed) Photosystem I: the light-driven plastocyanin:ferredoxin oxidoreductase. Springer, Dordrecht, The Netherlands, pp 99-117
3. Battchikova N, Zhang P, Rudd S, Ogawa T, Aro EM (2005) Identification of NdhL and Ssl1690 (NdhO) in NDH-1L and NDH-1M complexes of Synechocystis sp. PCC 6803. J Biol Chem 280:2587-2595
4. Behrenfeld MJ, Kolber ZS (1999) Widespread iron limitation of phytoplankton in the south pacific ocean. Science 283:840-843
5. Berger S, Ellersiek U, Kinzelt D, Steinmüller K (1993) Immunopurification of a subcomplex of the NAD(P)H-plastoquinone-oxidoreductase from the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 326:249-250
6. Bibby TS, Nield J, Barber J (2001) Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria. Nature 412:743-745
7. Boekema EJ, Hifney A, Yakushevska AE, Piotrowski M, Keegstra W, Berry S, Michel KP, Pistorius EK, Kruip J (2001) A giant chlorophyll-protein complex induced by iron deficiency in cyanobacteria. Nature 412:745-748
8. Burnap RL, Troyan T, Sherman LA (1993) The highly abundant chlorophyll-protein complex of iron-deficient Synechococcus sp. PCC 7942 (CP43′) is encoded by the isiA gene. Plant Physiol 103:893-902
9. 2 on NAD(P)H dehydrogenase, a mediator of cyclic electron transport around photosystem I in the cyanobacterium Synechocystis PCC6803. Plant Cell Physiol 44:534-540
10. Duhring U, Axmann IM, Hess WR, Wilde A (2006) An internal antisense RNA regulates expression of the photosynthesis gene isiA. Proc Natl Acad Sci USA 103:7054-7058
11. Durham KA, Porta D, McKay RM, Bullerjahn GS (2003) Expression of the iron-responsive irpA gene from the cyanobacterium Synechococcus sp. strain PCC 7942. Arch Microbiol 179:131-114
12. Dwivedi K, Sen A, Bullerjahn GS (1997) Expression and mutagenesis of the dpsA gene of Synechococcus sp. PCC 7942, encoding a DNA-binding protein involved in oxidative stress protection. FEMS Microbiol Lett 155:85-91
13. Exss-Sonne P, Tölle J, Bader KP, Pistorius EK, Michel KP (2000) The IdiA protein of Synechococcus sp. PCC 7942 functions in protecting photosystem II under oxidative stress. Photosynth Res 63:145-157
14. Fellay R, Frey J, Krisch H (1987) Interposon mutagenesis of soil and water bacteria: a family of DNA fragments designed for in vitro insertional mutagenesis of Gram-negative bacteria. Gene 52:147-154
15. Friedrich T, Scheide D (2000) The respiratory complex I of bacteria, archaea and eukarya and its module common with membrane-bound multisubunit hydrogenases. FEBS Lett 479:1-5
16. Friedrich T, Weiss H (1997) Modular evolution of the respiratory NADH:ubiquinone oxidoreductase and the origin of its modules. J Theor Biol 187:529-540
17. Fry IV, Huflejt M, Erber WW, Peschek GA, Packer L (1986) The role of respiration during adaptation of the freshwater cyanobacterium Synechococcus 6311 to salinity. Arch Biochem Biophys 244:686-691
18. Fulda S, Hagemann M (1995) Salt treatment induces accumulation of flavodoxin in the cyanobacterium Synechocystis sp. PCC 6803. J Plant Physiol 146:520-526
19. Ghassemian M, Straus NA (1996) Fur regulates the expression of iron-stress genes in the cyanobacterium Synechococcus sp. strain PCC 7942. Microbiology 142:1469-1476
20. Golden SS, Brusslan J, Haselkorn R (1987) Genetic engineering of the cyanobacterial chromosome. Methods Enzymol 153:215-231
21. Golding AJ, Johnson GN (2003) Down-regulation of linear and activation of cyclic electron transport during drought. Planta 218:107-114
22. Hart SE, Schlarb-Ridley BG, Bendall DS, Howe CJ (2005) Terminal oxidases of cyanobacteria. Biochem Soc Trans 33:832-835
23. Havaux M, Guedeney G, Hagemann M, Yeremenko N, Matthijs HC, Jeanjean R (2005) The chlorophyll-binding protein IsiA is inducible by high light and protects the cyanobacterium Synechocystis PCC6803 from photooxidative stress. FEBS Lett 579:2289-2293
24. Herbert SK, Martin RE, Fork DC (1995) Light adaptation of cyclic electron transport through photosystem I in the cyanobacterium Synechococcus sp. PCC 7942. Photosynth Res 46:277-285
25. Herdman M, Castenholz RW, Iteman I, Waterbury JB, Rippka R (2000) The archae, cyanobacteria and deeply branching bacteria. In: Boone DR, Castenholz RW, Garrity GM (eds) Bergey's manual of systematic bacteriology. Springer-Verlag, New York
26. Herranen M, Battchikova N, Zhang P, Graf A, Sirpio S, Paakkarinen V, Aro EM (2004) Towards functional proteomics of membrane protein complexes in Synechocystis sp. PCC 6803. Plant Physiol 134:470-481
27. Ivanov AG, Park YI, Miskiewicz E, Raven JA, Huner NP, Oquist G (2000) Iron stress restricts photosynthetic intersystem electron transport in Synechococcus sp. PCC 7942. FEBS Lett 485:173-177
28. Ivanov AG, Krol M, Sveshnikov D, Selstam E, Sandstrom S, Koochek M, Park YI, Vasil'ev S, Bruce D, Oquist G, Huner NP (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
29. 6 f reductase pathways in direct or indirect photosystem I driven cyclic electron flow in Synechocystis PCC 6803. In: Peschek G, Löffelhardt W, Schmetterer G (eds) The phototrophic prokaryotes. Kluwer Academic/Plenum Publishers, New York, pp 251-258
30. Jeanjean R, Zuther E, Yeremenko N, Havaux M, Matthijs HC, Hagemann M (2003) A photosystem 1 psaFJ-null mutant of the cyanobacterium Synechocystis PCC 6803 expresses the isiAB operon under iron replete conditions. FEBS Lett 549:52-56
31. Johnson GN (2005) Cyclic electron transport in C3 plants: fact or artefact? J Exp Bot 56:407-416
32. Joliot P, Joliot A (2006) Cyclic electron transfer around photosystem I. In: Golbeck JH (ed) Photosystem I: the light-driven plastocyanin:ferredoxin oxidoreductase, vol 24. Springer, Dordrecht, The Netherlands, pp 639-656
33. Joset F, Jeanjean R, Hagemann M (1996) Dynamics of the response of cyanobacteria to salt stress: deciphering the molecular events. Physiol Plant 96:738-744
34. Kouril R, Arteni AA, Lax J, Yeremenko N, D'Haene S, Rogner M, Matthijs HC, Dekker JP, Boekema EJ (2005) Structure and functional role of supercomplexes of IsiA and photosystem I in cyanobacterial photosynthesis. FEBS Lett 579:3253-3257
35. Kunert A, Vinnemeier J, Erdmann N, Hagemann M (2003) Repression by Fur is not the main mechanism controlling the iron-inducible isiAB operon in the cyanobacterium Synechocystis sp. PCC 6803. FEMS Microbiol Lett 227:255-262
36. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685
37. Laudenbach DE, Straus NA (1988) Characterization of a cyanobacterial iron stress-induced gene similar to psbC. J Bacteriol 170:5018-5026
38. Lax JEM, Arteni AA, Boekema E, Pistorius EK, Michel KP, Roegner M (2007) Structural response of photosystem II to iron deficiency: Characterization of a new photosystem II-IdiA complex from the cyanobacterium Thermosynechococcus elongatus BP-1. Biochim Biophys 1767:528-534
39. 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
40. Marjorette M, Pena O, Bullerjahn GS (1995) The DpsA protein of Synechococcus sp. strain PCC 7942 is a DNA-binding hemoprotein. J Biol Chem 270:22478-22782
41. Martin JH, Fitzwater SE (1988) Iron deficiency limits phytoplankton growth in the north-east Pacific subarctic. Nature 331:341-343
42. Martin JH, Coale KH, Johnson KS, Fitzwater SE, Gordon RM, Tanner SJ, Hunter CN, Elrod VA, Nowicki JL, Coley TL, Barber RT, Lindley S, Watson AJ, Van Scoy K, Law CS, Liddicoat MI, Ling R, Stanton T, Stockel J, Collins C, Anderson A, Bidigare R, Ondrusek M, Latasa M, Millero FJ, Lee K, Yao W, Zhang JZ, Friederich G, Sakamoto C, Chavez F, Buck K, Kolber ZS, Greene R, Falkowksi P, Chrisholm SW, Hoge F, Swift R, Yungel J, Turner S, Nightingale P, Hatton A, Liss P, Tindale NW (1994) Testing the iron hypothesis in the ecosystem of the equatorial Pacific Ocean. Nature 371:123-129
43. + reductase in cyanobacteria provides regulation for transient photosystem I-driven cyclic electron transport. Funct Plant Biol 29:201-210
44. Melkozernov AN, Bibby TS, Lin S, Barber J, Blankenship RE (2003) Time-resolved absorption and emission show that the CP43′ antenna ring of iron-stressed Synechocystis sp. PCC6803 is efficiently coupled to the photosystem I reaction center core. Biochemistry 42:3893-3903
45. 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
46. Mi H, Endo T, Schreiber U, Ogawa T (1994) NAD(P)H dehydrogenase-dependent cyclic electron flow around photosystem I in the cyanobacterium Synechocystis sp. PCC 6803: a study of dark-starved cells and spheroplasts. Plant Cell Physiol 35:163-173
47. Mi H, Endo T, Schreiber U, Ogawa T, Asada K (1992) Electron donation from cyclic and respiratory flows to the photosynthetic intersystem chain is mediated by the pyridine nucleotide dehydrogenase in the cyanobacterium Synechocystis PCC 6803. Plant Cell Physiol 33:1233-1237
48. Michel KP, Pistorius EK (1992) Isolation of a photosystem II associated 36 kDa polypeptide and an iron stress 34 kDa polypeptide from thylakoid membranes of the cyanobacterium Synechococcus PCC 6301 grown under mild iron deficiency. Z Naturforsch [C] 47:867-874
49. Michel KP, Pistorius EK (2004) Adaptation of the photosynthetic electron transport chain in cyanobacteria to iron deficiency: the function of IdiA and IsiA. Physiol Plant 119:1-15
50. Michel KP, Thole HH, Pistorius EK (1996) IdiA, a 34 kDa protein in the cyanobacteria Synechococcus sp. strains PCC 6301 and PCC 7942, is required for growth under iron and manganese limitations. Microbiology 142:2635-2645
51. Michel KP, Exss-Sonne P, Scholten-Beck G, Kahmann U, Ruppel HG, Pistorius EK (1998) Immunocytochemical localization of IdiA, a protein expressed under iron or manganese limitation in the mesophilic cyanobacterium Synechococcus PCC 6301 and the thermophilic cyanobacterium Synechococcus elongatus. Planta 205:73-81
52. Michel KP, Krüger F, Pühler A, Pistorius EK (1999) Molecular characterization of idiA and adjacent genes in the cyanobacteria Synechococcus sp. strains PCC 6301 and PCC 7942. Microbiology 145:1473-1484
53. Michel KP, Pistorius EK, Golden SS (2001) Unusual regulatory elements for iron deficiency induction of the idiA gene of Synechococcus elongatus PCC 7942. J Bacteriol 183:5015-5024
54. Michel KP, Berry S, Hifney A, Pistorius EK (2003) Adaptation to iron deficiency: a comparison between the cyanobacterium Synechococcus elongatus PCC 7942 wild-type and a DpsA-free mutant. Photosynth Res 75:71-84
55. Mullineaux CW, Allen F (1990) State 1-state 2 transitions in the cyanobacterium Synechococcus 6301 are controlled by the redox state of electron carriers between photosystem I and II. Photosynth Res 23:297-311
56. Munekage Y, Hojo M, Meurer J, Endo T, Tasaka M, Shikanai T (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110:361-371
57. Munekage Y, Hashimoto M, Miyake C, Tomizawa K, Endo T, Tasaka M, Shikanai T (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429:579-582
58. Nield J, Morris EP, Bibby TS, Barber J (2003) Structural analysis of the photosystem I supercomplex of cyanobacteria induced by iron deficiency. Biochemistry 42:3180-3188
59. Ogawa T, Kaplan A (2003) Inorganic carbon acquisition systems in cyanobacteria. Photosynth Res 77:105-115
60. Ohkawa H, Pakrasi HB, Ogawa T (2000) Two types of functionally distinct NAD(P)H dehydrogenases in Synechocystis sp. strain PCC 6803. J Biol Chem 275:31630-31634
61. Park YI, Sandström S, Gustafsson P, Öquist G (1999) Expression of the isiA gene is essential for the survival of the cyanobacterium Synechococcus sp. PCC 7942 by protecting photosystem II from excess light under iron limitation. Mol Microbiol 32:123-129
62. Reddy KJ, Bullerjahn GS, Sherman DM, Sherman LA (1988) Cloning, nucleotide sequence, and mutagenesis of a gene (irpA) involved in iron-deficient growth of the cyanobacterium Synechococcus sp. strain PCC 7942. J Bacteriol 170:4466-4476
63. Riethman HC, Sherman LA (1988) Purification and characterization of an iron stress-induced chlorophyll-protein from the cyanobacterium Anacystis nidulans R2. Biochim Biophys Acta 935:141-151
64. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2 edn. Cold Spring Harbor Laboratory, New York
65. Sandström S, Park YI, Öquist G, Gustafsson P (2001) CP43′, the isiA gene product, functions as an excitation energy dissipater in the cyanobacterium Synechococcus sp. PCC 7942. Photochem Photobiol 74:431-437
66. Schaegger H, von Jagow G (1987) Tricine-sodium dodecylsulphate- polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166:368-379
67. Scherer S (1990) Do photosynthetic and respiratory electron transport chains share redox proteins? Trends Biochem Sci 15:458-462
68. Schmetterer G (1994) Cyanobacterial respiration. In: Bryant DA (ed) The molecular biology of cyanobacteria, vol 4. Kluwer Academic Publishers, The Netherlands, pp 409-435
69. Singh AK, Sherman LA (2006) Iron-independent dynamics of IsiA production during the transition to stationary phase in the cyanobacterium Synechocystis sp. PCC 6803. FEMS Microbiol Lett 256:159-164
70. Singh AK, Li H, Sherman LA (2004) Microarray analysis and redox control of gene expression in the cyanobacterium Synechocystis sp. PCC 6803. Physiol Plant 120:27-35
71. Stephan DP, Ruppel HG, Pistorius EK (2000) Interrelation between cyanophycin synthesis, l-arginine catabolism and photosynthesis in the cyanobacterium Synechocystis sp. strain PCC 6803. Z Naturforsch [C] 55:927-942
72. Straus NA (1994) Iron deprivation: physiology and gene regulation. In: Bryant DA (ed) The molecular biology of cyanobacteria. Kluwer Academic Publishers, Dordrecht, pp 731-750
73. Thomas JC, Ughy B, Lagoutte B, Ajlani G (2006) A second isoform of the ferredoxin:NADP oxidoreductase generated by an in-frame initiation of translation. Proc Natl Acad Sci USA 103:18368-18373
74. Tölle J, Michel KP, Kruip J, Kahmann U, Preisfeld A, Pistorius EK (2002) Localization and function of the IdiA homologue Slr1295 in the cyanobacterium Synechocystis sp. strain PCC 6803. Microbiology 148:3293-3305
75. van Thor JJ, Jeanjean R, Havaux M, Sjollema KA, Joset F, Hellingwerf KJ, Matthijs HC (2000) Salt shock-inducible photosystem I cyclic electron transfer in Synechocystis PCC6803 relies on binding of ferredoxin:NADP(+) reductase to the thylakoid membranes via its CpcD phycobilisome-linker homologous N-terminal domain. Biochim Biophys Acta 1457:129-144
76. Vermaas WFJ (2001) Photosynthesis and respiration in cyanobacteria. In: Encyclopedia of life sciences. Nature Publishing Group, London, pp 1-7
77. Vinnemeier J, Kunert A, Hagemann M (1998) Transcriptional analysis of the isiAB operon in salt-stressed cells of the cyanobacterium Synechocystis sp. PCC 6803. FEMS Microbiol Lett 169:323-330
78. Webb R, Troyan T, Sherman D, Sherman LA (1994) MapA, an iron-regulated, cytoplasmic membrane protein in the cyanobacterium Synechococcus sp. strain PCC 7942. J Bacteriol 176:4906-4913
79. Yeremenko N, Jeanjean R, Prommeenate P, Krasikov V, Nixon PJ, Vermaas WF, Havaux M, Matthijs HC (2005) Open reading frame ssr2016 is required for antimycin A-sensitive photosystem I-driven cyclic electron flow in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 46:1433-1436
80. Yousef N, Pistorius EK, Michel KP (2003) Comparative analysis of idiA and isiA transcription under iron starvation and oxidative stress in Synechococcus elongatus PCC 7942 wild type and selected mutants. Arch Microbiol 180:471-483
81. 6 f complex. J Biol Chem 276:38159-38165