Summary
Cytochromes c 6 are widely-distributed monoheme proteins that transfer electrons from the cytochrome b 6 f complex to photosystem I in cyanobacteria and certain eukaryotic algae. Cytochrome c 6 has been replaced by plastocyanin in all known plant chloroplasts and in many cyanobacteria and algae, and was thought to be absent from plants until the discovery of chloroplast cytochrome c 6-like proteins, now named cytochromes c 6A. These have midpoint potentials substantially lower than those of typical cytochrome c 6 or plastocyanin indicating that they could not effectively transfer electrons from the cytochrome b 6 f complex to photosystem I. Additional c 6-like cytochromes have been discovered in cyanobacteria. The first of these was cytochrome c M, discovered in Synechocystis sp. PCC 6803 followed by discovery of a c 6-like cytochrome encoded by the petJ2 gene in Synechococcus sp. PCC 7002. Subsequent phylogenetic analysis revealed that most, but not all, cyanobacteria carry several genes for putative c 6-like cytochromes. Two deeply-branching clusters, designated cytochromes c 6B and c 6C, are distinct from either the classical c 6 cytochromes, chloroplast cytochromes c 6A, cyanobacterial cytochromes c M or c 550, or bacterial cytochromes c 555. Like cytochrome c 6A, representative cytochromes c 6C, c 6B, and c M have been analyzed and found to have low midpoint potentials unfavorable for electron transfer from the cytochrome b 6 f complex. High-resolution structures have been solved for c 6C and c 6B cytochromes and key residues identified that govern their low midpoint potentials. However, despite these advances and the widespread distribution of these cryptic cytochromes among cyanobacteria, their functions have remained largely mysterious. Here we review the discovery of cyanobacterial c 6-like cytochromes and current understanding of their properties and possible functions.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- COX:
-
Cytochrome oxidase
- Cyt:
-
Cytochrome
- Cyt b 6 f :
-
Cytochrome b 6 f complex
- Cyt c 6A :
-
Cytochrome c 6A
- Cyt c 6B :
-
Cytochrome c 6B
- Cyt c 6C :
-
Cytochrome c 6C
- Cyt c M :
-
Cytochrome c M
- PC:
-
Plastocyanin
- PQ:
-
Plastoquinone
- PSI:
-
Photosystem I
- PSII:
-
Photosystem II
References
Agarwal R, Matros A, Melzer M, Mock HP, Sainis JK (2010) Heterogeneity in thylakoid membrane proteome of Synechocystis 6803. J Proteomics 73:976–991
Allahverdiyeva Y, Ermakova M, Eisenhut M, Zhang P, Richaud P, Hagemann M, Laurent C, Aro EM (2011) Interplay between flavodiiron proteins and photorespiration in Synechocystis sp. PCC 6803. J Biol Chem 286:24007–24014
Allahverdiyeva Y, Mustila H, Ermakova M, Bersanini L, Richaud P, Ajlani G, Battchikova N, … Aro EM (2013) Flavodiiron proteins Flv1 and Flv3 enable cyanobacterial growth and photosynthesis under fluctuating light. Proc Natl Acad Sci U S A 110:4111–4116
Allahverdiyeva Y, Isojarvi J, Zhang P, Aro EM (2015) Cyanobacterial oxygenic photosynthesis is protected by flavodiiron proteins. Life 5:716–743
Alric J, Lavergne J, Rappaport F, Vermeglio A, Matsuura K, Shimada K, Nagashima KV (2006) Kinetic performance and energy profile in a roller coaster electron transfer chain: a study of modified tetraheme-reaction center constructs. J Am Chem Soc 128:4136–4145
Anderson SL, McIntosh L (1991) Light-activated heterotrophic growth of the cyanobacterium Synechocystis sp. strain PCC 6803: a blue-light-requiring process. J Bacteriol 173:2761–2767
Arora DP, Hossain S, Xu Y, Boon EM (2015) Nitric oxide regulation of bacterial biofilms. Biochemistry 54:3717–3728
Bailey S, Melis A, Mackey KR, Cardol P, Finazzi G, van Dijken G, Berg G, … Grossman A (2008) Alternative photosynthetic electron flow to oxygen in marine Synechococcus. Biochim Biophys Acta 1777:269–276
Bailleul B, Johnson X, Finazzi G, Barber J, Rappaport F, Telfer A (2008) The thermodynamics and kinetics of electron transfer between cytochrome b 6 f and photosystem I in the chlorophyll d-dominated cyanobacterium, Acaryochloris marina. J Biol Chem 283:25218–25226
Bauer CE, Elsen S, Bird TH (1999) Mechanisms for redox control of gene expression. Annu Rev Microbiol 53:495–523
Baymann F, Rappaport F (1998) Electrostatic interactions at the donor side of the photosynthetic reaction center of Rhodopseudomonas viridis. Biochemistry 37:15320–15326
Baymann F, Rappaport F, Joliot P, Kallas T (2001a) Rapid electron transfer to photosystem I and unusual spectral features of cytochrome c(6) in Synechococcus sp. PCC 7002 in vivo. Biochemistry 40:10570–10577
Baymann F, Tron P, Schoepp-Cothenet B, Aubert C, Bianco P, Stetter KO, Nitschke W, Schutz M (2001b) Cytochromes c555 from the hyperthermophilic bacterium Aquifex aeolicus (VF5). 1. Characterization of two highly homologous, soluble and membranous, cytochromes c555. Biochemistry 40:13681–13689
Bernroitner M, Tangl D, Lucini C, Furtmuller PG, Peschek GA, Obinger C (2009) Cyanobacterial cytochrome c(M): probing its role as electron donor for Cu(A) of cytochrome c oxidase. Biochim Biophys Acta 1787:135–143
Berry S, Schneider D, Vermaas WF, Rogner M (2002) Electron transport routes in whole cells of Synechocystis sp. strain PCC 6803: the role of the cytochrome bd-type oxidase. Biochemistry 41:3422–3429
Bersanini L, Battchikova N, Jokel M, Rehman A, Vass I, Allahverdiyeva Y, Aro EM (2014) Flavodiiron protein Flv2/Flv4-related photoprotective mechanism dissipates excitation pressure of PSII in cooperation with phycobilisomes in Cyanobacteria. Plant Physiol 164:805–818
Bialek W, Nelson M, Tamiola K, Kallas T, Szczepaniak A (2008) Deeply branching c6-like cytochromes of cyanobacteria. Biochemistry 47:5515–5522
Bialek W, Krzywda S, Jaskolski M, Szczepaniak A (2009) Atomic-resolution structure of reduced cyanobacterial cytochrome c6 with an unusual sequence insertion. FEBS J 276:4426–4436
Bialek W, Krzywda S, Zatwarnicki P, Jaskolski M, Kolesinski P, Szczepaniak A (2014) Insights into the relationship between the haem-binding pocket and the redox potential of c6 cytochromes: four atomic resolution structures of c6 and c6-like proteins from Synechococcus sp. PCC 7002. Acta Crystallogr D Biol Crystallogr 70:2823–2832
Busch A, Friedrich B, Cramm R (2002) Characterization of the norB gene, encoding nitric oxide reductase, in the nondenitrifying cyanobacterium Synechocystis sp. strain PCC6803. Appl Environ Microbiol 68:668–672
Chida H, Yokoyama T, Kawai F, Nakazawa A, Akazaki H, Takayama Y, Hirano T, … Oku T (2006) Crystal structure of oxidized cytochrome c(6A) from Arabidopsis thaliana. FEBS Lett 580:3763–3768
Cho YS, Pakrasi HB, Whitmarsh J (2000) Cytochrome cM from synechocystis 6803. Detection in cells, expression in Escherichia coli, purification and physical characterization. Eur J Biochem 267:1068–1074
Cross R, Lloyd D, Poole RK, Moir JW (2001) Enzymatic removal of nitric oxide catalyzed by cytochrome c′ in Rhodobacter capsulatus. J Bacteriol 183:3050–3054
David PS, Morrison MR, Wong SL, Hill BC (1999) Expression, purification, and characterization of recombinant forms of membrane-bound cytochrome c-550 nm from Bacillus subtilis. Protein Expr Purif 15:69–76
Diaz-Moreno I, Hulsker R, Skubak P, Foerster JM, Cavazzini D, Finiguerra MG, DÃaz-Quintana A, … Ubbink M (2014) The dynamic complex of cytochrome c6 and cytochrome f studied with paramagnetic NMR spectroscopy. Biochim Biophys Acta 1837:1305–1315
Eisenhut M, Ruth W, Haimovich M, Bauwe H, Kaplan A, Hagemann M (2008) The photorespiratory glycolate metabolism is essential for cyanobacteria and might have been conveyed endosymbiontically to plants. Proc Natl Acad Sci U S A 105:17199–17204
Fernandez-Velasco JG, Jamshidi A, Gong XS, Zhou J, Ueng RY (2001) Photosynthetic electron transfer through the cytochrome b 6 f complex can bypass cytochrome f. J Biol Chem 276:30598–30607
Flores E, Frias JE, Rubio LM, Herrero A (2005) Photosynthetic nitrate assimilation in cyanobacteria. Photosynth Res 83:117–133
Frazao C, Dias JM, Matias PM, Romao MJ, Carrondo MA, Hervas M, Navarro JA, … Sheldrick GM (1995) Cytochrome c6 from the green alga Monoraphidium braunii. Crystallization and preminary diffraction studies. Acta Crystallogr D Biol Crystallogr 51:232–234
Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. In: Walker JM (ed) The proteomics protocols handbook. Humana Press, New York, pp 571–607
Gouet P, Courcelle E, Stuart DI (1999) ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15:305–308
Green J, Rolfe MD, Smith LJ (2014) Transcriptional regulation of bacterial virulence gene expression by molecular oxygen and nitric oxide. Virulence 5:794–809
Gupta R, He Z, Luan S (2002) Functional relationship of cytochrome c(6) and plastocyanin in Arabidopsis. Nature 417:567–571
Helman Y, Tchernov D, Reinhold L, Shibata M, Ogawa T, Schwarz R, Ohad I, Kaplan A (2003) Genes encoding A-type flavoproteins are essential for photoreduction of O2 in cyanobacteria. Curr Biol 13:230–235
Helman Y, Barkan E, Eisenstadt D, Luz B, Kaplan A (2005) Fractionation of the three stable oxygen isotopes by oxygen-producing and oxygen-consuming reactions in photosynthetic organisms. Plant Physiol 138:2292–2298
Hervas M, Diaz-Quintana A, Kerfeld CA, Krogmann DW, De la Rosa MA, Navarro JA (2005) Cyanobacterial Photosystem I lacks specificity in its interaction with cytochrome c(6) electron donors. Photosynth Res 83:329–333
Hiraide Y, Oshima K, Fujisawa T, Uesaka K, Hirose Y, Tsujimoto R, Yamamoto H, … Fujita Y (2015) Loss of cytochrome cM stimulates cyanobacterial heterotrophic growth in the dark. Plant Cell Physiol 56:334–345
Ho KK, Krogmann DW (1980) Cytochrome f from spinach and cyanobacteria. Purification and characterization. J Biol Chem 255:3855–3861
Ho KK, Kerfeld CA, Krogmann DW (2011) The water-soluble cytochromes of cyanobacteria. In: Peschek GA, Obinger C, Renger G (eds) Bioenergetic Processes of Cyanobacteria: From Evolutionary Singularity to Ecological Diversity. Springer, Dordrecht, pp 515–540
Holton RW, Myers J (1967) Water-soluble cytochromes from a blue-green alga. I. Extraction, purification, and spectral properties of cytochromes C (549, 552, and 554, Anacystis nidulans). Biochim Biophys Acta 131:362–374
Howe CJ, Schlarb-Ridley BG, Wastl J, Purton S, Bendall DS (2006) The novel cytochrome c6 of chloroplasts: a case of evolutionary bricolage? J Exp Bot 57:13–22
Howitt CA, Vermaas WF (1998) Quinol and cytochrome oxidases in the cyanobacterium Synechocystis sp. PCC 6803. Biochemistry 37:17944–17951
Huang F, Parmryd I, Nilsson F, Persson AL, Pakrasi HB, Andersson B, Norling B (2002) Proteomics of Synechocystis sp. strain PCC 6803: identification of plasma membrane proteins. Mol Cell Proteomics 1:956–966
Kallas T (2012) Cytochrome b 6 f complex at the heart of energy transduction and redox signaling. In: Eaton-Rye JJ, Tripathy BC, Sharkey TD (eds) Photosynthesis: Plastid Biology, Energy Conversion and Carbon Assimilation. Springer, Dordrecht, pp 501–560
Kerfeld CA, Krogmann DW (1998) Photosynthetic cytochromes c in cyanobacteria, algae, and plants. Annu Rev Plant Physiol Plant Mol Biol 49:397–425
Kerfeld CA, Anwar HP, Interrante R, Merchant S, Yeates TO (1995) The structure of chloroplast cytochrome c6 at 1.9 A resolution: evidence for functional oligomerization. J Mol Biol 250:627–647
Kirilovsky D, Kerfeld CA (2012) The orange carotenoid protein in photoprotection of photosystem II in cyanobacteria. Biochim Biophys Acta 1817:158–166
Kruglik SG, Lambry JC, Cianetti S, Martin JL, Eady RR, Andrew CR, Negrerie M (2007) Molecular basis for nitric oxide dynamics and affinity with Alcaligenes xylosoxidans cytochrome c. J Biol Chem 282:5053–5062
Kufryk GI, Vermaas WF (2006) Sll 1717 affects the redox state of the plastoquinone pool by modulating quinol oxidase activity in thylakoids. J Bacteriol 188:1286–1294
Lea-Smith DJ, Ross N, Zori M, Bendall DS, Dennis JS, Scott SA, Smith AG, Howe CJ (2013) Thylakoid terminal oxidases are essential for the cyanobacterium Synechocystis sp. PCC 6803 to survive rapidly changing light intensities. Plant Physiol 162:484–495
Lebrun E, Brugna M, Baymann F, Muller D, Lievremont D, Lett MC, Nitschke W (2003) Arsenite oxidase, an ancient bioenergetic enzyme. Mol Biol Evol 20:686–693
Li Z, Andrews H, Eaton-Rye JJ, Burnap RL (2004) In situ effects of mutations of the extrinsic cytochrome c550 of photosystem II in Synechocystis sp. PCC6803. Biochemistry 43:14161–14170
Ludwig M, Bryant DA (2011) Transcription profiling of the model Cyanobacterium Synechococcus sp. strain PCC 7002 by next-gen (SOLiD) SEQUENCING of cDNA. Front Microbiol 2:41
Ludwig M, Bryant DA (2012a) Acclimation of the global transcriptome of the cyanobacterium Synechococcus sp. strain PCC 7002 to nutrient limitations and different nitrogen sources. Front Microbiol 3:145
Ludwig M, Bryant DA (2012b) Synechococcus sp. strain PCC 7002 transcriptome: acclimation to temperature, salinity, oxidative stress, and mixotrophic growth conditions. Front Microbiol 3:354
Malakhov MP, Wada H, Los DA, Semenenko VE, Murata N (1994) A new type of cytochrome c from synechocystis PCC6803. J Plant Physiol 144:259–264
Malakhov MP, Malakhova OA, Murata N (1999) Balanced regulation of expression of the gene for cytochrome cM and that of genes for plastocyanin and cytochrome c6 in Synechocystis. FEBS Lett 444:281–284
Manna P, Vermaas W (1997) Lumenal proteins involved in respiratory electron transport in the cyanobacterium Synechocystis sp. PCC6803. Plant Mol Biol 35:407–416
Marcaida MJ, Schlarb-Ridley BG, Worrall JA, Wastl J, Evans TJ, Bendall DS, Luisi BF, Howe CJ (2006) Structure of cytochrome c 6A, a novel dithio-cytochrome of Arabidopsis thaliana, and its reactivity with plastocyanin: implications for function. J Mol Biol 360:968–977
Mason JM, Bendall DS, Howe CJ, Worrall JA (2012) The role of a disulfide bridge in the stability and folding kinetics of Arabidopsis thaliana cytochrome c(6A). Biochim Biophys Acta 1824:311–318
Mehler AH (1951) Studies on reactions of illuminated chloroplasts. I. Mechanism of the reduction of oxygen and other Hill reagents. Arch Biochem Biophys 33:65–77
Molina-Heredia FP, Hervas M, Navarro JA, De la Rosa MA (1998) Cloning and correct expression in Escherichia coli of the petE and petJ genes respectively encoding plastocyanin and cytochrome c6 from the cyanobacterium Anabaena sp. PCC 7119. Biochem Biophys Res Commun 243:302–306
Molina-Heredia FP, Diaz-Quintana A, Hervas M, Navarro JA, De La Rosa MA (1999) Site-directed mutagenesis of cytochrome c(6) from Anabaena species PCC 7119. Identification of surface residues of the hemeprotein involved in photosystem I reduction. J Biol Chem 274:33565–33570
Molina-Heredia FP, Balme A, Hervas M, Navarro JA, De la Rosa MA (2002) A comparative structural and functional analysis of cytochrome cM cytochrome c6 and plastocyanin from the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 517:50–54
Molina-Heredia FP, Wastl J, Navarro JA, Bendall DS, Hervas M, Howe CJ, De La Rosa MA (2003) Photosynthesis: a new function for an old cytochrome? Nature 424:33–34
Mullineaux CW (2014) Co-existence of photosynthetic and respiratory activities in cyanobacterial thylakoid membranes. Biochim Biophys Acta 1837:503–511
Nagy CI, Vass I, Rakhely G, Vass IZ, Toth A, Duzs A, Peca L, … Kos PB (2014) Coregulated genes link sulfide:quinone oxidoreductase and arsenic metabolism in Synechocystis sp. strain PCC6803. J Bacteriol 196:3430–3440
Nakamura A, Suzawa T, Kato Y, Watanabe T (2005) Significant species-dependence of P700 redox potential as verified by spectroelectrochemistry: comparison of spinach and Theromosynechococcus elongatus. FEBS Lett 579:2273–2276
Nioche P, Berka V, Vipond J, Minton N, Tsai AL, Raman CS (2004) Femtomolar sensitivity of a NO sensor from Clostridium botulinum. Science 306:1550–1553
Nomura C (2001) Electron transport proteins of Synechococcus sp. PCC 7002. PhD thesis, Pennsylvania State University, University Park
Nomura C, Bryant DA (1999) Cytochrome c6 from Synechococcus sp. PCC 7002. In: Peschek G, Löffelhardt W, Schmetterer G (eds) The Phototrophic Prokaryotes. Kluwer Academic/Plenum Publishers, New York, pp 269–274
Nomura CT, Persson S, Shen G, Inoue-Sakamoto K, Bryant DA (2006a) Characterization of two cytochrome oxidase operons in the marine cyanobacterium Synechococcus sp. PCC 7002: inactivation of ctaDI affects the PS I:PS II ratio. Photosynth Res 87:215–228
Nomura CT, Sakamoto T, Bryant DA (2006b) Roles for heme-copper oxidases in extreme high-light and oxidative stress response in the cyanobacterium Synechococcus sp. PCC 7002. Arch Microbiol 185:471–479
Paumann M, Bernroitner M, Lubura B, Peer M, Jakopitsch C, Furtmuller PG, Peschek GA, Obinger C (2004a) Kinetics of electron transfer between plastocyanin and the soluble CuA domain of cyanobacterial cytochrome c oxidase. FEMS Microbiol Lett 239:301–307
Paumann M, Feichtinger M, Bernroitner M, Goldfuhs J, Jakopitsch C, Furtmuller PG, Regelsberger G, … Obinger C (2004b) Kinetics of interprotein electron transfer between cytochrome c6 and the soluble CuA domain of cyanobacterial cytochrome c oxidase. FEBS Lett 576:101–106
Ponamarev MV, Schlarb BG, Howe CJ, Carrell CJ, Smith JL, Bendall DS, Cramer WA (2000) Tryptophan-heme pi-electrostatic interactions in cytochrome f of oxygenic photosynthesis. Biochemistry 39:5971–5976
Rajagopal BS, Wilson MT, Bendall DS, Howe CJ, Worrall JA (2011) Structural and kinetic studies of imidazole binding to two members of the cytochrome c (6) family reveal an important role for a conserved heme pocket residue. J Biol Chem 16:577–588
Reyes-Sosa FM, Gil-Martinez J, Molina-Heredia FP (2011) Cytochrome c6-like protein as a putative donor of electrons to photosystem I in the cyanobacterium Nostoc sp. PCC 7119. Photosynth Res 110:61–72
Roncel M, Kirilovsky D, Guerrero F, Serrano A, Ortega JM (2012) Photosynthetic cytochrome c550. Biochim Biophys Acta 1817:1152–1163
Sawaya MR, Krogmann DW, Serag A, Ho KK, Yeates TO, Kerfeld CA (2001) Structures of cytochrome c-549 and cytochrome c6 from the cyanobacterium Arthrospira maxima. Biochemistry 40:9215–9225
Schmetterer G (1994) Cyanobacterial respiration. In: Bryant DA (ed) The Molecular Biology of Cyanobacteria. Kluwer Academic, Dordrecht, pp 409–435
Schneider D, Skrzypczak S, Anemuller S, Schmidt CL, Seidler A, Rogner M (2002) Heterogeneous rieske proteins in the cytochrome b 6 f complex of synechocystis PCC6803? J Biol Chem 277:10949–10954
Schultze M, Forberich B, Rexroth S, Dyczmons NG, Roegner M, Appel J (2009) Localization of cytochrome b 6 f complexes implies an incomplete respiratory chain in cytoplasmic membranes of the cyanobacterium Synechocystis sp. PCC 6803. Biochim Biophys Acta 1787:1479–1485
Schuurmans RM, Schuurmans JM, Bekker M, Kromkamp JC, Matthijs HC, Hellingwerf KJ (2014) The redox potential of the plastoquinone pool of the cyanobacterium Synechocystis species strain PCC 6803 is under strict homeostatic control. Plant Physiol 165:463–475
Seidler A (1996) The extrinsic polypeptides of photosystem II. Biochim Biophys Acta 1277:35–60
Shen JR, Vermaas W, Inoue Y (1995) The role of cytochrome c-550 as studied through reverse genetics and mutant characterization in Synechocystis sp. PCC 6803. J Biol Chem 270:6901–6907
Shin I, Ryu HB, Yim HS, Kang SO (2005) Cytochrome c550 is related to initiation of sporulation in Bacillus subtilis. J Microbiol 43:244–250
Shuvalov VA, Allakhverdiev SI, Sakamoto A, Malakhov M, Murata N (2001) Optical study of cytochrome cM formation in Synechocystis. IUBMB Life 51:93–97
Ting CS, Rocap G, King J, Chisholm SW (2002) Cyanobacterial photosynthesis in the oceans: the origins and significance of divergent light-harvesting strategies. Trends Microbiol 10:134–142
van Lis R, Nitschke W, Duval S, Schoepp-Cothenet B (2013) Arsenics as bioenergetic substrates. Biochim Biophys Acta 1827:176–188
Veit S, Takeda K, Tsunoyama Y, Rexroth D, Rogner M, Miki K (2012) Structure of a thermophilic cyanobacterial b 6 f-type Rieske protein. Acta Crystallogr D Biol Crystallogr 68:1400–1408
Wastl J, Bendall DS, Howe CJ (2002) Higher plants contain a modified cytochrome c(6). Trends Plant Sci 7:244–245
Wastl J, Purton S, Bendall DS, Howe CJ (2004) Two forms of cytochrome c6 in a single eukaryote. Trends Plant Sci 9:474–476
Weigel M, Varotto C, Pesaresi P, Finazzi G, Rappaport F, Salamini F, Leister D (2003) Plastocyanin is indispensable for photosynthetic electron flow in Arabidopsis thaliana. J Biol Chem 278:31286–31289
Worrall JA, Schlarb-Ridley BG, Reda T, Marcaida MJ, Moorlen RJ, Wastl J, Hirst J, … Howe CJ (2007) Modulation of heme redox potential in the cytochrome c6 family. J Am Chem Soc 129:9468–9475
Yamada S, Park SY, Shimizu H, Koshizuka Y, Kadokura K, Satoh T, Suruga K, … Oku T (2000) Structure of cytochrome c6 from the red alga Porphyra yezoensis at 1. 57 A resolution. Acta Crystallogr D Biol Crystallogr 56:1577–1582
Yin L, Bauer CE (2013) Controlling the delicate balance of tetrapyrrole biosynthesis. Philos Trans R Soc London B Biol Sci 368:20120262
Zatwarnicki P, Barciszewski J, Krzywda S, Jaskolski M, Kolesinski P, Szczepaniak A (2014) Cytochrome c(6B) of Synechococcus sp. WH 8102–crystal structure and basic properties of novel c(6)-like family representative. Biochem Biophys Res Commun 443:1131–1135
Zhang Z, Pendse ND, Phillips KN, Cotner JB, Khodursky A (2008) Gene expression patterns of sulfur starvation in Synechocystis sp. PCC 6803. BMC Genomics 9:344
Zhang P, Allahverdiyeva Y, Eisenhut M, Aro EM (2009) Flavodiiron proteins in oxygenic photosynthetic organisms: photoprotection of photosystem II by Flv2 and Flv4 in Synechocystis sp. PCC 6803. PLoS ONE 4:e5331
Zhang P, Eisenhut M, Brandt AM, Carmel D, Silen HM, Vass I, Allahverdiyeva Y, … Aro EM (2012) Operon flv4-flv2 provides cyanobacterial photosystem II with flexibility of electron transfer. Plant Cell 24:1952–1971
Acknowledgements
TK gratefully acknowledges grants MCB 0450875 and MRI 0321545 from the U.S. National Science Foundation, which supported some of this work.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer Science+Business Media Dordrecht
About this chapter
Cite this chapter
Bialek, W., Szczepaniak, A., Kolesinski, P., Kallas, T. (2016). Cryptic c 6-Like and c M Cytochromes of Cyanobacteria. In: Cramer, W., Kallas, T. (eds) Cytochrome Complexes: Evolution, Structures, Energy Transduction, and Signaling. Advances in Photosynthesis and Respiration, vol 41. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-7481-9_34
Download citation
DOI: https://doi.org/10.1007/978-94-017-7481-9_34
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-017-7479-6
Online ISBN: 978-94-017-7481-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)