Abstract
Cyanobacteria perform oxygenic photosynthesis, which makes them unique among the prokaryotes, and this feature together with their abundance and worldwide distribution renders them a central ecological role. Cyanobacteria and chloroplasts of plants and algae are believed to share a common ancestor and the modern chloroplast would thus be the remnant of an endosymbiosis between a eukaryotic cell and an ancestral oxygenic photosynthetic prokaryote. Chloroplast metabolic processes are coordinated with those of the other cellular compartments and are strictly controlled by means of regulatory systems that commonly involve redox reactions. Disulphide/dithiol exchange catalysed by thioredoxin is a fundamental example of such regulation and represents the molecular mechanism for light-dependent redox control of an ever-increasing number of chloroplast enzymatic activities. In contrast to chloroplast thioredoxins, the functions of the cyanobacterial thioredoxins have long remained elusive, despite their common origin. The sequenced genomes of several cyanobacterial species together with novel experimental approaches involving proteomics have provided new tools for re-examining the roles of the thioredoxin systems in these organisms. Thus, each cyanobacterial genome encodes between one and eight thioredoxins and all components necessary for the reduction of thioredoxins. Screening for thioredoxin target proteins in cyanobacteria indicates that assimilation and storage of nutrients, as well as some central metabolic pathways, are regulated by mechanisms involving disulphide/dithiol exchange, which could be catalysed by thioredoxins or related thiol-containing proteins.
Similar content being viewed by others
Abbreviations
- FTR:
-
ferredoxin–thioredoxin reductase
- Grx:
-
glutaredoxin
- GSH:
-
reduced glutathione
- NTR:
-
NADP–thioredoxin reductase
- Prx:
-
peroxiredoxin
- Trx:
-
thioredoxin
References
Alam J, Curtis S, Gleason FK, Gerami-Nejad M, Fuchs JA (1989) Isolation, sequence, and expression in Escherichia coli of an unusual thioredoxin gene from the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 171:162–171
Balmer Y, Buchanan BB (2002) Yet another plant thioredoxin. Trends Plant Sci 7:191–193
Balmer Y, Koller A, del Val G, Manieri W, Schurmann P, Buchanan BB (2003) Proteomics gives insight into the regulatory function of chloroplast thioredoxins. Proc Natl Acad Sci USA 100:370–375
Balmer Y, Vensel WH, Tanaka CK, Hurkman WJ, Gelhaye E, Rouhier N, Jacquot JP, Manieri W, Schurmann P, Droux M, Buchanan BB (2004) Thioredoxin links redox to the regulation of fundamental processes of plant mitochondria. Proc Natl Acad Sci USA 101:2642–2647
Brandes HK, Larimer FW, Hartman FC (1996) The molecular pathway for the regulation of phosphoribulokinase by thioredoxin f. J Biol Chem 271:3333–3335
Buchanan BB (1980) Role of light in the regulation of chloroplast enzymes. Annu Rev Plant Physiol 31:341–374
Buchanan BB, Balmer Y (2005) Redox regulation: a broadening horizon. Annu Rev Plant Biol 56:187–220
Buchanan BB, Schurmann P, Wolosiuk RA, Jacquot JP (2002) The ferredoxin/thioredoxin system: from discovery to molecular structures and beyond. Photosynth Res 73:215–222
Dufresne A, Garczarek L, Partensky F (2005) Accelerated evolution associated with genome reduction in a free-living prokaryote. Genome Biol 6:R14
Florencio FJ, Yee BC, Johnson TC, Buchanan BB (1988) An NADP/thioredoxin system in leaves: purification and characterization of NADP-thioredoxin reductase and thioredoxin h from spinach. Arch Biochem Biophys 266:496–507
Garcia-Fernandez JM, de Marsac NT, Diez J (2004) Streamlined regulation and gene loss as adaptive mechanisms in Prochlorococcus for optimized nitrogen utilization in oligotrophic environments. Microbiol Mol Biol Rev 68:630–638
Gleason FK (1996) Glucose-6-phosphate dehydrogenase from the cyanobacterium, Anabaena sp. PCC 7120: purification and kinetics of redox modulation. Arch Biochem Biophys 334:277–283
Gleason FK, Holmgren A (1981) Isolation and characterization of thioredoxin from the cyanobacterium, Anabaena sp. J Biol Chem 256:8306–8309
Gleason FK, Holmgren A (1988) Thioredoxin and related proteins in prokaryotes. FEMS Microbiol Rev 4:271–297
Holmgren A, Soderberg BO, Eklund H, Branden CI (1975) Three-dimensional structure of Escherichia coli thioredoxin-S2 to 2.8 A resolution. Proc Natl Acad Sci USA 72:2305–2309
Hosoya-Matsuda N, Motohashi K, Yoshimura H, Nozaki A, Inoue K, Ohmori M, Hisabori T (2005) Anti-oxidative stress system in cyanobacteria. Significance of type II peroxiredoxin and the role of 1-Cys peroxiredoxin in Synechocystis sp. strain PCC 6803. J Biol Chem 280:840–846
Jacquot JP, Lancelin JM, Meyer Y (1997) Thioredoxins: structure and function in plant cells. New Phytol 136:543–570
Jaffe EK (2003) An unusual phylogenetic variation in the metal ion binding sites of porphobilinogen synthase. Chem Biol 10:25–34
Kaneko T, Nakamura Y, Wolk CP, Kuritz T, Sasamoto S, Watanabe A, Iriguchi M, Ishikawa A, Kawashima K, Kimura T, Kishida Y, Kohara M, Matsumoto M, Matsuno A, Muraki A, Nakazaki N, Shimpo S, Sugimoto M, Takazawa M, Yamada M, Yasuda M, Tabata S (2001) Complete genomic sequence of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120. DNA Res 8:205–213, 227–253
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
Kobayashi D, Tamoi M, Iwaki T, Shigeoka S, Wadano A (2003) Molecular characterization and redox regulation of phosphoribulokinase from the cyanobacterium Synechococcus sp. PCC 7942. Plant Cell Physiol 44:269–276
Krenn BE, Aardewijn P, Van Walraven HS, Werner-Grune S, Strotmann H, Kraayenhof R (1995) ATP synthase from a cyanobacterial Synechocystis 6803 mutant containing the regulatory segment of the chloroplast gamma subunit shows thiol modulation. Biochem Soc Trans 23:757–760
Laloi C, Rayapuram N, Chartier Y, Grienenberger JM, Bonnard G, Meyer Y (2001) Identification and characterization of a mitochondrial thioredoxin system in plants. Proc Natl Acad Sci USA 98:14144–14149
Lemaire SD, Collin V, Keryer E, Quesada A, Miginiac-Maslow M (2003) Characterization of thioredoxin y, a new type of thioredoxin identified in the genome of Chlamydomonas reinhardtii. FEBS Lett 543:87–92
Lemaire SD, Guillon B, Le Marechal P, Keryer E, Miginiac-Maslow M, Decottignies P (2004) New thioredoxin targets in the unicellular photosynthetic eukaryote Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 101:7475–7480
Liedgens W, Lutz C, Schneider HA (1983) Molecular properties of 5-aminolevulinic acid dehydratase from Spinacia oleracea. Eur J Biochem 135:75–79
Lim CJ, Gleason FK, Fuchs JA (1986) Cloning, expression, and characterization of the Anabaena thioredoxin gene in Escherichia coli. J Bacteriol 168:1258–1264
Lindahl M, Florencio FJ (2003) Thioredoxin-linked processes in cyanobacteria are as numerous as in chloroplasts, but targets are different. Proc Natl Acad Sci USA 100:16107–16112
Lindahl M, Florencio FJ (2004) Systematic screening of reactive cysteine proteomes. Proteomics 4:448–450
Marchand C, Le Marechal P, Meyer Y, Miginiac-Maslow M, Issakidis-Bourguet E, Decottignies P (2004) New targets of Arabidopsis thioredoxins revealed by proteomic analysis. Proteomics 4:2696–2706
Mestres-Ortega D, Meyer Y (1999) The Arabidopsis thaliana genome encodes at least four thioredoxins m and a new prokaryotic-like thioredoxin. Gene 240:307–316
Meyer Y, Reichheld JP, Vignols F (2005) Thioredoxins in Arabidopsis and other plants. Photosynth Res 86:419–433
Miller AG, Hunter KJ, O’Leary SJ, Hart LJ (2000) The photoreduction of H(2)O(2) by Synechococcus sp. PCC 7942 and UTEX 625. Plant Physiol 123:625–636
Motohashi K, Kondoh A, Stumpp MT, Hisabori T (2001) Comprehensive survey of proteins targeted by chloroplast thioredoxin. Proc Natl Acad Sci USA 98:11224–11229
Muller EG (1994) Deoxyribonucleotides are maintained at normal levels in a yeast thioredoxin mutant defective in DNA synthesis. J Biol Chem 269:24466–24471
Muller EG, Buchanan BB (1989) Thioredoxin is essential for photosynthetic growth. The thioredoxin m gene of Anacystis nidulans. J Biol Chem 264:4008–4014
Navarro F, Florencio FJ (1996) The cyanobacterial thioredoxin gene is required for both photoautotrophic and heterotrophic growth. Plant Physiol 111:1067–1075
Navarro F, Martin-Figueroa E, Florencio FJ (2000) Electron transport controls transcription of the thioredoxin gene (trxA) in the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol Biol 43:23–32
Pennisi E (2006) Microbial ecology. How a marine bacterium adapts to multiple environments. Science 311:1697
Pérez-Pérez ME, Florencio FJ, Lindahl M (2006) Selecting thioredoxins for disulphide proteomics: target proteomes of three thioredoxins from the cyanobacterium Synechocystis sp. PCC 6803. Proteomics 6 (Suppl 1):S186–195
Potamitou A, Holmgren A, Vlamis-Gardikas A (2002) Protein levels of Escherichia coli thioredoxins and glutaredoxins and their relation to null mutants, growth phase, and function. J Biol Chem 277:18561–18567
Rippka R, Deruelles J, Waterbury JB, Herman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61
Rippka R, Waterbury J, Cohen-Bazire G (1974) A cyanobacterium which lacks thylakoids. Arch Microbiol 100:419–436
Rocap G, Larimer FW, Lamerdin J, Malfatti S, Chain P, Ahlgren NA, Arellano A, Coleman M, Hauser L, Hess WR, Johnson ZI, Land M, Lindell D, Post AF, Regala W, Shah M, Shaw SL, Steglich C, Sullivan MB, Ting CS, Tolonen A, Webb EA, Zinser ER, Chisholm SW (2003) Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424:1042–1047
Rouhier N, Villarejo A, Srivastava M, Gelhaye E, Keech O, Droux M, Finkemeier I, Samuelsson G, Dietz KJ, Jacquot JP, Wingsle G (2005) Identification of plant glutaredoxin targets. Antioxid Redox Signal 7:919–929
Saitoh M, Nishitoh H, Fujii M, Takeda K, Tobiume K, Sawada Y, Kawabata M, Miyazono K, Ichijo H (1998) Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. Embo J 17:2596–2606
Schneider GJ, Tumer NE, Richaud C, Borbely G, Haselkorn R (1987) Purification and characterization of RNA polymerase from the cyanobacterium Anabaena 7120. J Biol Chem 262:14633–14639
Serrato AJ, Pérez-Ruiz JM, Spinola MC, Cejudo FJ (2004) A novel NADPH thioredoxin reductase, localized in the chloroplast, which deficiency causes hypersensitivity to abiotic stress in Arabidopsis thaliana. J Biol Chem 279:43821–43827
Simon RD (1976) The biosynthesis of multi-L-arginyl-poly(L-aspartic acid) in the filamentous cyanobacterium Anabaena cylindrica. Biochim Biophys Acta 422:407–418
Sippola K, Aro EM (1999) Thiol redox state regulates expression of psbA genes in Synechococcus sp. PCC 7942. Plant Mol Biol 41:425–433
Sparla F, Pupillo P, Trost P (2002) The C-terminal extension of glyceraldehyde-3-phosphate dehydrogenase subunit B acts as an autoinhibitory domain regulated by thioredoxins and nicotinamide adenine dinucleotide. J Biol Chem 277:44946–44952
Spencer P, Jordan PM (1993) Purification and characterization of 5-aminolaevulinic acid dehydratase from Escherichia coli and a study of the reactive thiols at the metal-binding domain. Biochem J 290(Pt 1):279–287
Tichy M, Vermaas W (1999) In vivo role of catalase-peroxidase in Synechocystis sp. strain PCC 6803. J Bacteriol 181:1875–1882
Verdoucq L, Vignols F, Jacquot JP, Chartier Y, Meyer Y (1999) In vivo characterization of a thioredoxin h target protein defines a new peroxiredoxin family. J Biol Chem 274:19714–19722
Vignols F, Brehelin C, Surdin-Kerjan Y, Thomas D, Meyer Y. (2005) A yeast two-hybrid knockout strain to explore thioredoxin-interacting proteins in vivo. Proc Natl Acad Sci USA 102:16729–16734
Wenderoth I, Scheibe R, von Schaewen A (1997) Identification of the cysteine residues involved in redox modification of plant plastidic glucose-6-phosphate dehydrogenase. J Biol Chem 272:26985–26990
Werner-Grune S, Gunkel D, Schumann J, Strotmann H (1994) Insertion of a “chloroplast-like” regulatory segment responsible for thiol modulation into gamma-subunit of F0F1-ATPase of the cyanobacterium Synechocystis 6803 by mutagenesis of atpC. Mol Gen Genet 244:144–150
Wong JH, Balmer Y, Cai N, Tanaka CK, Vensel WH, Hurkman WJ, Buchanan BB (2003) Unraveling thioredoxin-linked metabolic processes of cereal starchy endosperm using proteomics. FEBS Lett 547:151–156
Wynn R, Cocco MJ, Richards FM (1995) Mixed disulfide intermediates during the reduction of disulfides by Escherichia coli thioredoxin. Biochemistry 34:11807–11813
Yamamoto H, Miyake C, Dietz KJ, Tomizawa K, Murata N, Yokota A (1999) Thioredoxin peroxidase in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 447:269–273
Yamazaki D, Motohashi K, Kasama T, Hara Y, Hisabori T (2004) Target proteins of the cytosolic thioredoxins in Arabidopsis thaliana. Plant Cell Physiol 45:18–27
Yano H, Kuroda S, Buchanan BB (2002) Disulfide proteome in the analysis of protein function and structure. Proteomics 2:1090–1096
Yano H, Wong JH, Lee YM, Cho MJ, Buchanan BB (2001) A strategy for the identification of proteins targeted by thioredoxin. Proc Natl Acad Sci USA 98:4794–4799
Yee BC, de la Torre A, Crawford NA, Lara C, Carlson DE, Buchanan BB (1981) The ferredoxin/thioredoxin enzyme regulation in a cyanobacterium. Arch Microbiol 130:14–18
Zhang N, Kallis RP, Ewy RG, Portis AR Jr (2002) Light modulation of Rubisco in Arabidopsis requires a capacity for redox regulation of the larger Rubisco activase isoform. Proc Natl Acad Sci USA 99:3330–3334
Zhang N, Portis AR Jr (1999) Mechanism of light regulation of Rubisco: a specific role for the larger Rubisco activase isoform involving reductive activation by thioredoxin-f. Proc Natl Acad Sci USA 96:9438–9443
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Florencio, F.J., Pérez-Pérez, M.E., López-Maury, L. et al. The diversity and complexity of the cyanobacterial thioredoxin systems. Photosynth Res 89, 157–171 (2006). https://doi.org/10.1007/s11120-006-9093-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-006-9093-5