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The Convergent Evolution of Cytochrome c 6 and Plastocyanin Has Been Driven by Geochemical Changes

Abstract

Cytochrome c 6 and plastocyanin are two small, soluble heme- and copper-containing proteins, respectively, that are located in the thylakoidal lumen and transfer electrons from cytochrome b 6-f to photosystem I in most oxygen-evolving photosynthetic organisms. In cyanobacteria, the two metalloproteins do indeed play an extra respiratory role as donors of electrons to cytochrome c oxidase. They are both phylogenetically and structurally unrelated—one is a c-type cytochrome, with four a-helices and a heme iron; the other is a Type 1 blue copper protein, with a β-barrel folding—but share a number of physicochemical parameters and structural similarities that allow them to replace each other depending on copper availability. A plausible hypothesis is that there has been an evolutionary transition from cytochrome c 6 to plastocyanin, with the heme protein being first “invented” by Nature, when iron was much more available than copper because of the reducing character of the Earth’s atmosphere, but being later replaced by the copper protein because of the reverse changes in iron and copper availabilities as the photosynthetic dioxygen concentration began to rise. Thus, this is an excellent case study of convergent evolution at the molecular level, which is herein interpreted as a consequence of microbial adaptation to environmental conditions.

Keywords

  • Copper Protein
  • Thylakoidal Lumen
  • Redox Partner
  • Blue Copper Protein
  • Synechocystis Cell

These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  • Albarrán C, Navarro JA, Molina-Heredia FP, Murdoch PS, De la Rosa MA and Hervás M (2005) Laser flash-induced kinetic analysis of cytochrome f oxidation by wild-type and mutant plastocyanin from the cyanobacterium Nostoc sp. PCC 7119. Biochemistry 44: 11601–11607

    PubMed  CrossRef  Google Scholar 

  • Albarrán C, Navarro JA, De la Rosa MA and Hervás M (2007) The specificity in the interaction between cytochrome f and plastocyanin from the cyanobacterium Nostoc sp. PCC 7119 is mainly determined by the copper protein. Biochemistry 46: 997–1003

    PubMed  CrossRef  Google Scholar 

  • Anderson SL and McIntosh L (1991) Light-activated heterotrophic growth of the cyanobacterium Synechocystis sp. PCC 6803: A blue-light-requiring process. J Bacteriol 173: 2761–2767

    PubMed  CAS  Google Scholar 

  • Banci L, Bertini I, Ciofi-Baffoni S, Kandias N, Robinson NJ, Spryoulias G, Su X-G, Tottey S and Vanarotti M (2006) The delivery of copper for thylakoid import observed by NMR. Proc Natl Acad Sci USA 103: 8320–8325

    PubMed  CrossRef  CAS  Google Scholar 

  • Berkner LV and Marshall LC (1965) History of major atmospheric components. Proc Natl Acad Sci USA 53: 1215–1225

    CrossRef  CAS  Google Scholar 

  • Bertini I and Cavallaro G (2008) Metals in the “omics” world: Copper homeostasis and cytochrome c oxidase assembly in a new light. J Biol Inorg Chem 13: 3–14

    PubMed  CrossRef  CAS  Google Scholar 

  • Blankenship RE (1992) Origin and early evolution of photosynthesis. Photosynth Res 33: 91–111

    PubMed  CrossRef  CAS  Google Scholar 

  • Bovy A, de Vrieze G, Borrias M and Weisbeek P (1992) Transcriptional regulation of the plastocyanin and cytochrome c553 genes from the cyanobacterium Anabaena species PCC 7937. Mol Microl 6: 1507–1513

    CrossRef  CAS  Google Scholar 

  • Briggs LM, Pecoraro VL and McIntosh L (1990) Copper-induced expression, cloning, and regulatory studies of the plastocyanin gene from the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol Biol 15: 633–642

    PubMed  CrossRef  CAS  Google Scholar 

  • Bryant DA (ed) (1994) The Molecular Biology of Cyanobacteria. Advances in Photosynthesis and Respiration Series, Vol 1. Kluwer Academic Publishing, Dordrecht

    CrossRef  Google Scholar 

  • Cavet JS, Borrelly GPM and Robinson NJ (2003) Zn, Cu and Co in cyanobacteria: Selective control of metal availability. FEMS Microbiol Rev 27: 165–181

    PubMed  CrossRef  CAS  Google Scholar 

  • Crichton RR (2008) Biological inorganic chemistry: An introduction. Elsevier, Amsterdam

    Google Scholar 

  • Crichton RR and Pierre JL (2001) Old iron, young copper: From Mars to Venus. Biometals 14: 99–112

    PubMed  CrossRef  CAS  Google Scholar 

  • Crichton RR and Ward RJ (eds) (2006) Metal-based neurodegeneration: From molecular mechanisms to therapeutic strategies. John Wiley & Sons, Chichester

    Google Scholar 

  • Crowley B, Díaz-Quintana A, Molina-Heredia FP, Nieto P, Sutter M, Haehnel W, De la Rosa MA and Ubbink M (2002) The interactions of cyanobacterial cytochrome c 6 and cytochrome f characterized by NMR. J Biol Chem 277: 48685–48689

    PubMed  CrossRef  CAS  Google Scholar 

  • De la Cerda B, Díaz-Quintana A, Navarro JA, Hervás M and De la Rosa MA (1999) Site-directed mutagenesis of cytochrome c 6 from Synechocystis sp. PCC 6803. The heme-protein possesses a negatively charged area that may be isofunctional with the acidic patch of plastocyanin. J Biol Chem 274: 13292–13297

    PubMed  CrossRef  Google Scholar 

  • De la Rosa MA, Navarro JA, Díaz-Quintana A, De la Cerda B, Molina-Heredia FP, Balme A, Murdoch PS, Díaz-Moreno I, Durán RV and Hervás M (2002) An evolutionary analysis of the reaction mechanisms of photosystem I reduction by cytochrome c 6 and plastocyanin. Bioelectrochemistry 55: 41–45

    PubMed  CrossRef  Google Scholar 

  • De la Rosa MA, Molina-Heredia FP, Hervás M and Navarro JA (2006) Convergent evolution of cytochrome c 6 and plastocyanin. In: Golbeck J (ed) Photosystem I. The Light-Driven Plastocyanin/Cytochrome c 6:Ferredoxin/Flavodoxin Reductase, pp 683–696. Springer, Dordrecht

    CrossRef  Google Scholar 

  • De la Cerda B, Castielli O, Durán RV, Navarro JA, Hervás M and De la Rosa MA (2008) A proteomic approach to iron and copper homeostasis in cyanobacteria. Brief Funct Genomic Proteomic 6: 322–329

    CrossRef  Google Scholar 

  • Des Marais DJ (1998) Earth’s early biosphere. Gravit Space Biol Bull 11: 23–30

    PubMed  Google Scholar 

  • Deuerling E, Schulze-Specking A, Tomoyasu T, Mogk A and Bukau B (1999) Trigger factor and DnaK cooperate in folding of newly synthesized proteins. Nature 400: 693–696

    PubMed  CrossRef  CAS  Google Scholar 

  • Díaz-Quintana A, Navarro, JA, Hervás M, Molina-Heredia FP, De la Cerda B and De la Rosa MA (2003) A comparative structural and functional analysis of cyanobacterial plastocyanin and cytochrome c 6 as alternative electron donors to photosystem I. Photosynth Res 75: 97–110

    PubMed  CrossRef  Google Scholar 

  • Díaz-Moreno I, Díaz-Quintana A, De la Rosa MA and Ubbink M (2005a) Structure of the complex between plastocyanin and cytochrome f from the cyanobacterium Nostoc sp. PCC 7119 as determined by paramagnetic NMR. The balance between electrostatic and hydrophobic interactions within the transient complex determines the relative orientation of the two proteins. J Biol Chem 280: 18908–18915

    CrossRef  Google Scholar 

  • Díaz-Moreno I, Díaz-Quintana A, Molina-Heredia FP, Nieto PM, Hansson Ö, De la Rosa MA and Karlsson BG (2005b) NMR analysis of the transient complex between membrane photosystem I and soluble cytochrome c 6. J Biol Chem 280: 7925–7931

    CrossRef  Google Scholar 

  • Díaz-Quintana A, Hervás M, Navarro JA and De la Rosa MA (2008) Plastocyanin and cytochrome c 6: The soluble electron carriers between the cytochrome b 6 f complex and photosystem I. In: Fromme P (ed) Structure of Photosynthetic Proteins, pp 181–200. Wiley-VCH, Weinheim

    CrossRef  Google Scholar 

  • Durán RV, Hervás M, De la Rosa MA and Navarro JA (2004) The efficient functioning of photosynthesis and respiration in Synechocystis sp. PCC 6803 strictly requires the presence of either cytochrome c 6 or plastocyanin. J Biol Chem 279: 7229–7233

    PubMed  CrossRef  Google Scholar 

  • Durán RV, Hervás M, De la Rosa MA and Navarro JA (2006) A laser flash-induced kinetic analysis of in vivo photosystem I reduction by site-directed mutants of plastocyanin and cytochrome c 6 in Synechocystis sp. PCC 6803. Biochemistry 45: 1054–1060

    PubMed  CrossRef  Google Scholar 

  • Finazzi G, Sommer F and Hippler M (2005) Release of oxidized plastocyanin from photosystem I limits electron transfer between photosystem I and cytochrome b 6 f complex in vivo. Proc Natl Acad Sci USA 102: 7031–7036

    PubMed  CrossRef  CAS  Google Scholar 

  • Fischer AG (1965) Fossils, early life, and atmospheric history. Proc Natl Acad Sci USA 53: 1205–1213

    CrossRef  Google Scholar 

  • Frazão C, Soares CM, Carrondo MA, Pohl E, Dauter Z, Wilson KS, Hervás M, Navarro JA, De la Rosa MA and Sheldrick GM (1995) Ab initio determination of the crystal structure of cytochrome c 6 and comparison with plastocyanin. Structure 3: 1159–1169

    PubMed  CrossRef  Google Scholar 

  • Goldblatt C, Lenton TM and Watson AJ (2006) Bistability of atmospheric oxygen and the great oxidation. Nature 443: 683–686

    PubMed  CrossRef  CAS  Google Scholar 

  • Guss JM and Freeman HC (1983) Structure of oxidized poplar plastocyanin at 1.6 Å resolution. J Mol Biol 169: 521–563

    CAS  Google Scholar 

  • Guss JM, Harrowell PR, Murata M, Norris VA and Freeman HC (1986) Crystal structure analyses of reduced (CuI) poplar plastocyanin at six pH values. J Mol Biol 192: 361–387

    PubMed  CrossRef  CAS  Google Scholar 

  • Halliwell B and Gutteridge JM (1984) Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem J 219: 1–14

    PubMed  CAS  Google Scholar 

  • Hervás M, Navarro JA, Díaz A, Bottin H and De la Rosa MA (1995) Laser-flash kinetic analysis of the fast electron transfer from plastocyanin and cytochrome c 6 to photosystem I. Experimental evidence on the evolution of the reaction mechanism. Biochemistry 34: 11321–11326

    PubMed  CrossRef  Google Scholar 

  • Hervás M, Navarro JA and De la Rosa MA (2003) Electron transfer between soluble proteins and membrane complexes in photosynthesis. Accounts Chem Res 36: 798–805

    CrossRef  Google Scholar 

  • Hippler M, Drepper F, Farah J and Rochaix JD (1997) Fast electron transfer from cytochrome c 6 and plastocyanin to photosystem I of Chlamydomonas reinhardtii requires PsaF. Biochemistry 36: 6343–6349

    PubMed  CrossRef  CAS  Google Scholar 

  • Ho KK and Krogmann DW (1984) Electron donors to P700 in cyanobacteria and algae. An instance of unusual genetic variability. Biochim Biophys Acta 766: 310–316

    CrossRef  CAS  Google Scholar 

  • Hope AB (2000) Electron transfer amongst cytochrome f, plastocyanin and photosystem I: Kinetics and mechanisms. Biochim Biophys Acta 1456: 5–26

    PubMed  CrossRef  CAS  Google Scholar 

  • Inoue T, Sugawara H, Hamanaka S, Tsukui H, Suzuki E, Kohzuma T and Kai Y (1999) Crystal structure determinations of oxidized and reduced plastocyanin from the cyanobacterium Synechococcus sp. PCC 7942. Biochemistry 38: 6063–6069

    PubMed  CrossRef  CAS  Google Scholar 

  • Kannt A, Young S and Bendall DS (1996) The role of acidic residues of plastocyanin in its interaction with cytochrome f. Biochim Biophys Acta 1277: 115–126

    CrossRef  CAS  Google Scholar 

  • Kasting JF and Donahue TM (1981) Evolution of oxygen and ozone in Earth’s atmosphere. In: Proceedings of the Conference Life in the Universe, Moffett Field, CA, 1979, pp 149–162. MIT Press, Cambridge, MA

    Google Scholar 

  • Kasting JF and Siefert JL (2003) Life and the evolution of Earth’s atmosphere. Science 296: 1066–1068

    CrossRef  Google Scholar 

  • Katoh H, Hagino N, Grossman AR and Ogawa T (2001) Genes essential to iron transport in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 183: 2779–2784

    PubMed  CrossRef  CAS  Google Scholar 

  • Keren N, Aurora R and Pakrasi HB (2004) Critical roles of bacterioferritins in iron storage and proliferation of cyanobacteria. Plant Physiol 135: 1–8

    CrossRef  Google Scholar 

  • Kobayashi M, Ishizuka T, Katayama M, Kanehisa M, Bhattacharyya-Pakrasi M, Pakrasi HB and Ikeuchi M (2004) Response to oxidative stress involves a novel peroxiredoxin gene in the unicellular cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 45: 290–299

    PubMed  CrossRef  CAS  Google Scholar 

  • Macalady J and Banfield JF (2003) Molecular geomicrobiology: Genes and geochemical cycling. Earth Planet Sci Lett 209: 1–17

    CrossRef  CAS  Google Scholar 

  • Malakhov MP, Malakhova OA and Murata N (1999) Balanced regulation of expression of the gen for cytochrome c M and that of genes for plastocyanin and cytochrome c 6 in Synechocystis. FEBS Lett 444: 281–284

    PubMed  CrossRef  CAS  Google Scholar 

  • Martin JH et al. (1994) Testing the iron hypothesis in ecosystems of the equatorial Pacific Ocean. Nature 371: 123–129

    CrossRef  CAS  Google Scholar 

  • Merchant S, Allen MD, Kropat J, Moseley JL, Long JC, Tottey S and Terauchi AM (2006) Between a rock and a hard place: Trace element nutrition in Chlamydomonas. Biochim Biophys Acta 1763: 578–594

    PubMed  CrossRef  CAS  Google Scholar 

  • Messerschmidt A, Huber R, Poulos T and Wieghardt K (eds) (2001) Handbook of Metalloproteins. John Wiley & Sons, Chichester

    Google Scholar 

  • Metzger SU, Pakrasi HB and Whitmarsh J (1995) Characterization of a double deletion mutant that lacks cytochrome c 6 and cytochrome c M in Synechocystis 6803. In: Mathis P (ed) Photosynthesis: From Light to Biosphere, pp 823–826. Kluwer Academic Publishing, Dordrecht

    Google Scholar 

  • Molina-Heredia FP, Hervás M, Navarro JA and De la Rosa MA (2001) A single arginyl residue in plastocyanin and cytochrome c 6 from the cyanobacterium Anabaena sp. PCC 7119 is required for efficient reduction of photosystem I. J Biol Chem 276: 601–605

    PubMed  CrossRef  CAS  Google Scholar 

  • Molina-Heredia FP, Wastl J, Navarro JA, Bendall DS, Hervás M, Howe C and De la Rosa MA (2003) Photosynthesis: A new function for an old cytochrome? Nature 424, 33–34.

    PubMed  CrossRef  CAS  Google Scholar 

  • Morel FMM and Price NM (2003) The biogeochemical cycles of trace metals in the oceans. Science 300: 944–947

    PubMed  CrossRef  CAS  Google Scholar 

  • Navarro JA, Durán RV, De la Rosa MA and Hervás M (2005) Respiratory cytochrome c oxidase can be efficiently reduced by the photosynthetic redox proteins cytochrome c 6 and plastocyanin in cyanobacteria. FEBS Lett 579: 3565–3568

    PubMed  CrossRef  CAS  Google Scholar 

  • Newman DK and Banfield JF (2002) Geomicrobiology: How molecular-scale interactions underpin biogeochemical systems. Science 296: 1071–1077

    PubMed  CrossRef  CAS  Google Scholar 

  • Ochiai EI (1983) Copper and the biological evolution. Biosystems 16: 81–86

    PubMed  CrossRef  CAS  Google Scholar 

  • Paumann M, Bernroitner M, Lubura B, Peer M, Jakopitsch C, Furtmüller PG, Peschek GA and 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

    CrossRef  CAS  Google Scholar 

  • Paumann M, Feichtinger M, Bernroitner M, Goldfuhs J, Jakopitsch C, Furtmüller PG, Regelsberger G, Peschek GA and Obinger C (2004b) Kinetics of interprotein electron transfer between cytochrome c 6 and the soluble CuA domain of cyanobacterial cytochrome c oxidase. FEBS Lett 576: 101–106

    CrossRef  CAS  Google Scholar 

  • Paumann M, Lubura B, Regelsberger G, Feichtinger M, Köllensberger G, Jakopitsch C, Furtmüller PG, Peschek GA and Obinger C (2004c) Soluble CuA domain of cyanobacterial cytochrome c oxidase. J Biol Chem 279: 10293–10303

    CrossRef  CAS  Google Scholar 

  • Paumann M, Regelsberger G, Obinger C and Peschek GA (2005) The bioenergetic role of dioxygen and the terminal oxidase(s) in cyanobacteria. Biochim Biophys Acta 1707: 231–253

    PubMed  CrossRef  CAS  Google Scholar 

  • Peschek G (1999) Photosynthesis and respiration of cyanobacteria. In: Peschek G, Loffelhardt W and Schmetterer G (eds) The Phototrophic Prokaryotes, pp 201–209. Kluwer Academic Publishing, New York

    CrossRef  Google Scholar 

  • Pils D, Gregor W and Schmetterer G (1997) Evidence for in vivo activity of three distinct respiratory terminal oxidases in the cyanobacterium Synechocystis sp. PCC 6803. FEMS Microbiol Lett 152: 83–88

    CrossRef  CAS  Google Scholar 

  • Rogers LJ (1987) Ferredoxins, flavodoxins and related proteins: Structure, function and evolution. In: Fay P and Van Baalen C (eds) The Cyanobacteria, pp 35–67. Elsevier, Amsterdam

    Google Scholar 

  • Sandmann G, Reck H, Kessler E and Böger P (1983) Distribution of plastocyanin and soluble plastidic cytochrome c in various classes of algae. Arch Microbiol 134: 23–37

    CrossRef  CAS  Google Scholar 

  • Sawaya MR, Krogmann DW, Serag A, Ho KK, Yeates TO and Kerfeld CA (2001) Structures of cytochrome c-549 and cytochrome c 6 from the cyanobacterium Arthrospira maxima. Biochemistry 40: 9215–9225

    PubMed  CrossRef  CAS  Google Scholar 

  • Schlarb-Ridley BG, Bendall DS and Howe CJ (2002) Role of electrostatics in the interaction between cytochrome f and plastocyanin of the cyanobacterium Phormidium laminosum. Biochemistry 41: 3279–3285

    PubMed  CrossRef  CAS  Google Scholar 

  • Schmetterer G (1994) Cyanobacterial respiration. In: Bryant DG (ed) The Molecular Biology of Cyanobacteria, pp 409–435. Kluwer Academic Publishing, Dordrecht

    CrossRef  Google Scholar 

  • Shcolnick S and Keren N (2006) Metal homeostasis in cyanobacteria and chloroplasts. Balancing benefits and risks to the photosynthetic apparatus. Plant Physiol 141: 805–810

    PubMed  CrossRef  CAS  Google Scholar 

  • Sigfridsson K (1998) Plastocyanin, an electron-transfer protein. Photosynth Res 57: 1–28

    CrossRef  CAS  Google Scholar 

  • Sigfridsson K, Hansson Ö, Karlsson BG, Baltzer L, Nordling M and Lundberg LG (1995) Spectroscopic and kinetic characterization of the spinach plastocyanin mutant Tyr83-His: A histidine residue with a high pKa value. Biochim Biophys Acta 1228: 28–36

    CrossRef  Google Scholar 

  • Stearn WT (1962) The origin of the male and female symbols of biology. Taxon 11: 109–113

    CrossRef  Google Scholar 

  • Tottey S, Rondet SAM, Borrelly GPM, Robinson PJ, Rich PR and Robinson NJ (2002) A copper metallochaperone for photosynthesis and respiration reveals metal-specific targets, interaction with an importer, and alternative sites for copper acquisition. J Biol Chem 277: 5490–5497

    PubMed  CrossRef  Google Scholar 

  • Tottey S, Harvie DR and Robinson NJ (2005) Understanding how cells allocate metals using metal-sensors and metallochaperones. Accounts Chem Res 38: 775–783

    CrossRef  CAS  Google Scholar 

  • Ubbink M, Ejdebäck M, Karlsson BG and Bendall DS (1998) The structure of the complex of plastocyanin and cytochrome f determined by paramagnetic NMR and restrained rigid-body molecular dynamics. Structure 6: 323–335

    PubMed  CrossRef  CAS  Google Scholar 

  • Van der Plas J, Bovy A, Kruyt F, de Vrieze G, Dassen E, Klein B and Weisbeek P (1989) The gene for the precursor for plastocyanin from the cyanobacterium Anabaena sp. PCC 7937: Isolation, sequence and regulation. Mol Microbiol 3: 275–284

    PubMed  CrossRef  CAS  Google Scholar 

  • Vermaas WFJ (2001) Photosynthesis and respiration in cyanobacteria. In: Encyclopedia of Life Sciences, pp 245–251. http://www.els.net, Nature Publishing Group, London

    Google Scholar 

  • Williams RJP (2007) Life, the environment and our ecosystem. J Inorg Biochem 101: 1550–1561

    PubMed  CrossRef  CAS  Google Scholar 

  • Williams RJP and Fraústo da Silva JJR (1996) The Natural Selection of the Chemical Elements. Oxford University Press, Oxford

    Google Scholar 

  • Wood PM (1978) Interchangeable copper and iron proteins in algal photosynthesis. Studies on plastocyanin and cytochrome c-552 in Chlamydomonas. Eur J Biochem 87: 9–19

    PubMed  CrossRef  CAS  Google Scholar 

  • Zhang L, McSpadden B, Pakrasi HB and Whitmarsh J (1992) Copper-mediated regulation of cytochrome c553 and plastocyanin in the cyanobacterium Synechocystis 6803. J Biol Chem 267: 19054–19059

    PubMed  CAS  Google Scholar 

  • Zhang L, Pakrasi HB and Whitmarsh J (1994) Photoautotrophic growth of the cyanobacterium Synechocystis sp. PCC 6803 in the absence of cytochrome c553 and plastocyanin. J Biol Chem 269: 5036–5042

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

Research work at the authors’ laboratory has been funded by the Spanish Ministry of Science and Innovation, the Andalusian Government and the European Commission. The authors thank their co-workers and collaborators, most of them listed in the references herein cited, for their contributions to this research.

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De la Rosa, M.A., Navarro, J.A., Hervás, M. (2011). The Convergent Evolution of Cytochrome c 6 and Plastocyanin Has Been Driven by Geochemical Changes. In: Peschek, G., Obinger, C., Renger, G. (eds) Bioenergetic Processes of Cyanobacteria. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-0388-9_21

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