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The Evolution of Type I Reaction Centers: The Response to Oxygenic Photosynthesis

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Functional Genomics and Evolution of Photosynthetic Systems

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 33))

Summary

Recent advances in the understanding of homodimeric Type I reaction centers in contemporary anaerobic phototrophs are used to advance a scenario in the evolution of Photosystem I. The transition from anaerobic to aerobic photosynthesis 2.7 billion years ago was accompanied by profound changes on the acceptor side of the ancestral Type I reaction center. At the advent of oxygen evolution, the mobile bacterial dicluster ferredoxin, which initially served to transfer electrons from the FX cluster to target redox proteins, became highly vulnerable to oxidative denaturation. In response, an exceedingly tight binding interface developed between the bacterial dicluster ferredoxin and the Type I reaction center core, thereby making it possible for the FA and FB iron-sulfur clusters to survive in the presence of oxygen. The need for an alternative, mobile electron carrier led to the evolution of an oxygen-insensitive [2Fe-2S] ferredoxin. The recruitment of a PsaD-like protein to generate a binding site for ferredoxin, by necessity, broke the perfect C2-symmetry of the homodimeric reaction center and provided the selective pressure that led to its differentiation into separate PsaA and PsaB polypeptides. The Photosystem I reaction center nevertheless retained a high degree of C2-symmetry surrounding the FX cluster, resulting in a new problem of how to dock the bacterial dicluster ferredoxin in one of the two possible orientations on the PsaA/PsaB heterodimer. Ultimately, all of the information required for preferential docking was coded in the amino acid sequence of the dicluster ferredoxin that became PsaC. The differentiation and inversion of the redox potentials of FA and FB ensured that the electron was preferentially transferred to the [2Fe-2S] ferredoxin in the supersaturated solution of the oxygen-evolving cell.

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Notes

  1. 1.

     Years before present (1950), as in Ga, giga-annum (109 years) and Ma, mega-annum (106 years).

  2. 2.

    The literature survey presented here is not exhaustive; rather, we put forward an evolutionary scenario that is consistent with the biochemical and biophysical evidence from contemporary phototrophs that contain Type I reaction centers. As a result, we will not be delving into the controversies and opposing views of this active field.

  3. 3.

     Even though the PscA proteins from Chlorobi and Acidobacteria share the same ‘A’ suffix, they belong to two different monophyletic groups.

  4. 4.

     The amino acid numbering scheme used in this article is that of PS I from Thermosynechococcus elongatus.

Abbreviations

A0 :

PSI primary electron acceptor

BChl:

bacteriochlorophyll

Chl:

chlorophyll

EPR:

electron ­paramagnetic resonance

Fx:

interpolypeptide [4Fe4S] cluster

P700 :

PSI primary electron donor

PSI:

photosystem I

PSII:

photosystem II

PsaA/B:

heterodimeric PSI reaction center core protein in cyanobacteria, algae, and plants

PsaC:

FA/FB–containing protein

PscA:

homodimeric reaction center core protein in green sulfur bacteria

PshA:

homodimeric reaction center core protein in heliobacteria

References

  • Allen JF (2005) A redox switch hypothesis for the origin of two light reactions in photosynthesis. FEBS Lett 579: 963–968

    Article  PubMed  CAS  Google Scholar 

  • Allen JF and Martin W (2007) Evolutionary biology: out of thin air. Nature 445: 610–612

    Article  PubMed  CAS  Google Scholar 

  • Allen JP and Williams JC (1998) Photosynthetic reaction centers. FEBS Lett 438: 5–9

    Article  PubMed  CAS  Google Scholar 

  • Amesz J (1995) The heliobacteria, a new group of photosynthetic bacteria. J Photochem Photobiol 30: 89–96

    Article  CAS  Google Scholar 

  • Amunts A, Drory O and Nelson N (2007) The structure of a plant photosystem I supercomplex at 3.4  Å resolution. Nature 447: 58–63

    Article  PubMed  CAS  Google Scholar 

  • Antonkine ML, Liu G, Bentrop D, Bryant DA, Bertini I, Luchinat C, Golbeck JH and Stehlik D (2002) Solution structure of the unbound, oxidized photosystem I subunit PsaC, containing [4Fe-4S] clusters FA and FB: a conformational change occurs upon binding to photosystem I. J Biol Inorg Chem 7: 461–472

    Article  PubMed  CAS  Google Scholar 

  • Antonkine ML, Jordan P, Fromme P, Krauß N, Golbeck JH and Stehlik D (2003) Assembly of protein subunits within the stromal ridge of photosystem I. Structural changes between unbound and sequentially PSI-bound polypeptides and correlated changes of the magnetic properties of the terminal iron sulfur clusters. J Mol Biol 327: 671–697

    Article  PubMed  CAS  Google Scholar 

  • Barth P, Lagoutte B and Sétif P (1998) Ferredoxin reduction by photosystem I from Synechocystis sp. PCC 6803: toward an understanding of the respective roles of subunits PsaD and PsaE in ferredoxin binding. Biochemistry 37: 16233–16241

    Article  PubMed  CAS  Google Scholar 

  • Baumann B, Sticht H, Scharpf M, Sutter M, Haehnel W and Rösch P (1996) Structure of Synechococcus elongatus [Fe2S2] ferredoxin in solution. Biochemistry 35: 12831–12841

    Article  PubMed  CAS  Google Scholar 

  • Baymann F, Brugna M, Mühlenhoff U and Nitschke W (2001) Daddy, where did (PS)I come from? Biochim Biophys Acta 1507: 291–310

    Article  PubMed  CAS  Google Scholar 

  • Ben-Shem A, Frolow F and Nelson N (2003) Crystal structure of plant photosystem I. Nature 426: 630–5

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Blankenship RE (2001) Molecular evidence for the evolution of photosynthesis. Trends Plant Sci 6: 4–6

    Article  PubMed  CAS  Google Scholar 

  • Blankenship R (2002) Molecular Mechanisms of Photosynthesis. Blackwell Science, Ltd, London

    Book  Google Scholar 

  • Boekema EJ, Kouril R, Dekker JP and Jensen PE (2006) Association of photosystem I and light-harvesting complex II during state transitions. In: Golbeck JH (ed.) Photosystem I: The Light-Induced Plastocyanin:Ferredoxin Oxidoreductase, pp 41–46. Springer, Dordrecht

    Google Scholar 

  • Brettel K and Leibl W (2001) Electron transfer in photosystem I. Biochim Biophys Acta 1507: 100–114

    Article  PubMed  CAS  Google Scholar 

  • Brocks JJ, Logan GA, Buick R and Summons RE (1999) Archean molecular fossils and the early rise of eukaryotes. Science 285: 1033–1036

    Article  PubMed  CAS  Google Scholar 

  • Bryant DA, Costas AM, Maresca JA, Chew AG, Klatt CG, Bateson MM, Tallon LJ, Hostetler J, Nelson WC, Heidelberg JF and Ward DM (2007) Candidatus Chloracidobacterium thermophilum: an aerobic phototrophic Acidobacterium. Science 317: 523–526

    Article  PubMed  CAS  Google Scholar 

  • Büttner M, Xie DL, Nelson H, Pinther W, Hauska G and Nelson N (1992) Photosynthetic reaction center genes in green sulfur bacteria and in photosystem I are related. Proc Natl Acad Sci USA 89: 8135–8139

    Article  PubMed  Google Scholar 

  • Catling DC, Zahnle KJ and McKay C (2001) Biogenic methane, hydrogen escape, and the irreversible oxidation of early Earth. Science 293: 839–843

    Article  PubMed  CAS  Google Scholar 

  • Chamorovsky SK and Cammack R (1982) Direct determination of the midpoint potential of the acceptor X in chloroplast photosystem I by electrochemical reduction and ESR spectroscopy. Photochem Photobiol 4: 195–200

    CAS  Google Scholar 

  • Chitnis VP, Jung YS, Albee L, Golbeck JH and Chitnis PR (1996) Mutational analysis of photosystem I polypeptides - role of PsaD and the lysyl 106 residue in the reductase activity of photosystem I. J Biol Chem 271: 11772–11780

    Article  PubMed  CAS  Google Scholar 

  • Cohen Y, Chitnis VP, Nechushtai R and Chitnis PR (1993) Stable assembly of PsaE into cyanobacterial photosynthetic membranes is dependent on the presence of other accessory subunits of photosystem I. Plant Mol Biol 23: 895–900

    Article  PubMed  CAS  Google Scholar 

  • Cohen RO, Shen G, Golbeck JH, Xu W, Chitnis PR, Valieva AI, van der Est A, Pushkar Y and Stehlik D (2004) Evidence for asymmetric electron transfer in cyanobacterial photosystem I: analysis of a methionine-to-leucine mutation of the ligand to the primary electron acceptor A0. Biochemistry 43: 4741–4754

    Article  PubMed  CAS  Google Scholar 

  • Croce R, Morosinotto T and Bassi R (2006) LHC1: The antenna complex of photosystem I in plants and green algae. In: Golbeck JH (ed) Photosystem I: The Light-Induced Plastocyanin:Ferredoxin Oxidoreductase, pp 119–137. Springer, Dordrecht

    Google Scholar 

  • Dashdorj N, Xu W, Cohen RO, Golbeck JH and Savikhin S (2005) Asymmetric electron transfer in cyanobacterial photosystem I: charge separation and secondary electron transfer dynamics of mutations near the primary electron acceptor A0. Biophys J 88: 1238–1249

    Article  PubMed  CAS  Google Scholar 

  • Davis IH, Heathcote P, MacLachlan DJ and Evans MCW (1993) Modulation analysis of the electron spin echo signals of in vivo oxidized primary donor 14N chlorophyll centers in bacterial, P870, P960, and plant photosystem I, P700 reaction centers. Biochim Biophys Acta 1143: 183–189

    Article  CAS  Google Scholar 

  • DePamphilis BV, Averill BA, Herskovitz T, Que LJ and Holm R (1974) Synthetic analogs of the active sites of iron-sulfur proteins. VI. Spectral and redox characteristics of the tetranuclear clusters [Fe4S4(SR)4]2-. J Am Chem Soc 96: 4159–4167

    Article  PubMed  CAS  Google Scholar 

  • DiazQuintana A, Leibl W, Bottin H and Sétif P (1998) Electron transfer in photosystem I reaction centers follows a linear pathway in which iron-sulfur cluster FB is the immediate electron donor to soluble ferredoxin. Biochemistry 37: 3429–3439

    Article  CAS  Google Scholar 

  • Ehrenreich A and Widdel F (1994) Anaerobic oxidation of ferrous iron by purple bacteria, a new type of phototrophic metabolism. Appl Environ Microbiol 60: 4517–4526

    PubMed  CAS  Google Scholar 

  • Eisen JA, Nelson KE, Paulsen IT, Heidelberg JF, Wu M, Dodson RJ, Deboy R, Gwinn ML, Nelson WC, Haft DH, Hickey EK, Peterson JD, Durkin AS, Kolonay JL, Yang F, Holt I, Umayam LA, Mason T, Brenner M, Shea TP, Parksey D, Nierman WC, Feldblyum TV, Hansen CL, Craven MB, Radune D, Vamathevan J, Khouri H, White O, Gruber TM, Ketchum KA, Venter JC, Tettelin H, Bryant DA and Fraser CM (2002) The complete genome sequence of Chlorobium tepidum TLS, a photosynthetic, anaerobic, green-sulfur bacterium. Proc Natl Acad Sci USA 99: 9509–9514

    Article  PubMed  CAS  Google Scholar 

  • Ferreira KN, Iverson TM, Maghlaoui K, Barber J and Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303: 1831–1838

    Article  PubMed  CAS  Google Scholar 

  • Figueras JB, Cox RP, Hojrup P, Permentier HP and Miller M (2002) Phylogeny of the PscB reaction center protein from green sulfur bacteria. Photosynth Res 71: 155–164

    Article  PubMed  CAS  Google Scholar 

  • Frankenberg N, Hager-Braun C, Feiler U, Fuhrmann M, Rogl H, Schneebauer N, Nelson N and Hauska G (1996) P840-reaction centers from Chlorobium tepidum-quinone analysis and functional reconstitution into lipid vesicles. Photochem Photobiol 64: 14–19

    Article  CAS  Google Scholar 

  • Fromme P (1996) Structure and function of photosystem I. Curr Opin Struct Biol 6: 473–484

    Article  PubMed  CAS  Google Scholar 

  • Fromme P, Witt HT, Schubert WD, Klukas O, Saenger W and Krauß N (1996) Structure of photosystem I at 4.5  Å resolution: a short review including evolutionary aspects. Biochim Biophys Acta 1275: 76–83

    Article  Google Scholar 

  • Fromme P, Jordan P and Krauß N (2001) Structure of photosystem I. Biochim Biophys Acta 1507: 5–31

    Article  PubMed  CAS  Google Scholar 

  • Golbeck J (1992) Structure and function of photosystem I. Annu Rev Plant Physiol Plant Mol Biol 43: 293–324

    Article  CAS  Google Scholar 

  • Golbeck JH (1993) Shared thematic elements in photochemical reaction centers. Proc Natl Acad Sci. USA 90: 1642–1646

    Article  PubMed  CAS  Google Scholar 

  • Golbeck JH (1994) Photosystem I in Cyanobacteria. In: Bryant DA (ed) The Molecular Biology of Cyanobacteria, pp 179–220. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Golbeck JH (1999) A comparative analysis of the spin state distribution of in vivo and in vitro mutants of PsaC. A biochemical argument for the sequence of electron transfer in Photosystem I as FX -  >  FA -  >  FB -  >  ferredoxin/flavodoxin. Photosynth Res 61: 107–149

    Article  CAS  Google Scholar 

  • Golbeck JH, Lien S and San Pietro A (1977) Isolation and characterization of a subchloroplast particle enriched in iron-sulfur protein and P700. Arch Biochem Biophys 178: 140–150

    Article  PubMed  CAS  Google Scholar 

  • Gunner MR, Robertson DE and Dutton PL (1986) Kinetic studies on the reaction center protein from Rhodopseudomonas sphaeroides: the temperature and free energy dependence of electron transfer between various quinones in the QA site and the oxidized bacteriochlorophyll dimer. J Phys Chem 90: 3783–3795

    Article  CAS  Google Scholar 

  • Gupta RS (2003) Evolutionary relationships among photosynthetic bacteria. Photosynth Res 76: 173–183

    Article  PubMed  CAS  Google Scholar 

  • Gupta RS, Mukhtar T and Singh B (1999) Evolutionary relationships among photosynthetic prokaryotes (Heliobacterium chlorum, Chloroflexus aurantiacus, cyanobacteria, Chlorobium tepidum and proteobacteria): implications regarding the origin of photosynthesis. Mol Microbiol 32: 893–906

    Article  PubMed  CAS  Google Scholar 

  • Hager-Braun C, Zimmermann R and Hauska G (1999) The homodimeric reaction center of Chlorobium. In: Peschek G, Loeffelhardt W, and Schmetterer G (eds) Phototrophic Prokaryotes, pp 169–181. Kluwer Academic Publishers, New York

    Article  CAS  Google Scholar 

  • Hager-Braun C, Jarosch U, Hauska G, Nitschke W and Riedel A (1997) EPR studies of the terminal electron acceptors of the green sulfur bacterial reaction centre. Revisited. Photosynth Res 51: 127–136

    Article  CAS  Google Scholar 

  • Hallahan BJ, Purton S, Ivison A, Wright D and Evans MCW (1995) Analysis of the proposed Fe-Sx binding region of photosystem I by site-directed mutation of PsaA in Chlamydomonas reinhardtii. Photosynth Res 46: 257–264

    Article  CAS  Google Scholar 

  • Hatano A, Seo D, Kitashima M, Sakurai H and Inoue K (2005) Purification of two ferredoxins and cloning of these genes from the photosynthetic bacterium Heliobacillus mobilis. In: van der Est A and Bruce D (eds) 13th International Congress on Photosynthesis, pp 83–85. Allen Press Inc., Lawrence, Kansas

    Google Scholar 

  • Hauska G (1988) Phylloquinone in photosystem I: are quinones the secondary electron acceptors in all types of photosynthetic reaction centers? Trends Biochem Sci 13: 415–416

    Article  PubMed  CAS  Google Scholar 

  • Hauska G, Schoedl T, Remigy H and Tsiotis G (2001) The reaction center of green sulfur bacteria. Biochim Biophys Acta 1507: 260–277

    Article  PubMed  CAS  Google Scholar 

  • Heathcote P, Fyfe PK and Jones MR (2002) Reaction centres: the structure and evolution of biological solar power. Trends Biochem Sci 27: 79–87

    Article  PubMed  CAS  Google Scholar 

  • Heinnickel M and Golbeck JH (2007) Heliobacterial photosynthesis. Photosynth Res 92: 35–53

    Article  PubMed  CAS  Google Scholar 

  • Heinnickel M, Shen G, Agalarov R and Golbeck JH (2005) Resolution and reconstitution of a bound Fe-S protein from the photosynthetic reaction center of Heliobacterium modesticaldum. Biochemistry 44: 9950–9960

    Article  PubMed  CAS  Google Scholar 

  • Heinnickel M, Agalarov R, Svensen N, Krebs C and Golbeck JH (2006) Identification of FX in the heliobacterial reaction center as a [4Fe-4S] cluster with an S  =  3/2 ground spin state. Biochemistry 45: 6756–6764

    Article  PubMed  CAS  Google Scholar 

  • Heinnickel M, Shen, G and Golbeck JH (2007) Identification and characterization of PshB, the dicluster ferredoxin that harbors the terminal electron acceptors FA and FB in Heliobacterium modesticaldum. Biochemistry 46: 2530–2536

    Article  PubMed  CAS  Google Scholar 

  • Heising S and Schink B (1998) Phototrophic oxidation of ferrous iron by a Rhodomicrobium vannielii strain. Microbiology 144: 2263–2269

    Article  PubMed  CAS  Google Scholar 

  • Heising S, Richter L, Ludwig W and Schink B (1999) Chlorobium ferrooxidans sp. nov., a phototrophic green sulfur bacterium that oxidizes ferrous iron in coculture with a “Geospirillum” sp. strain. Arch Microbiol 172: 116–124

    Article  PubMed  CAS  Google Scholar 

  • Holzwarth AR, Müller MG, Niklas J and Lubitz W (2006) Ultrafast transient absorption studies on photosystem I reaction centers from Chlamydomonas reinhardtii. 2: mutations near the P700 reaction center chlorophylls provide new insight into the nature of the primary electron donor. Biophys J 90: 552–565

    Article  PubMed  CAS  Google Scholar 

  • Ihnatowicz A, Pesaresi P and Leister D (2007) The E subunit of photosystem I is not essential for linear electron flow and photoautotrophic growth in Arabidopsis thaliana. Planta 226: 889–895

    Article  PubMed  CAS  Google Scholar 

  • Inoue H, Tsuchiya T, Satoh S, Miyashita H, Kaneko T, Tabata S, Tanaka A and Mimuro M (2004) Unique constitution of photosystem I with a novel subunit in the cyanobacterium Gloeobacter violaceus PCC 7421. FEBS Lett 578: 275–279

    Article  PubMed  CAS  Google Scholar 

  • Ishikita H and Knapp EW (2003) Redox potential of quinones in both electron transfer branches of photosystem I. J Biol Chem 278: 52002–52011

    Article  PubMed  CAS  Google Scholar 

  • Iwaki M and Itoh S (1994) Reaction of reconstituted acceptor quinone and dynamic equilibration of electron transfer in the photosystem I reaction center. Plant Cell Physiol 35: 983–993

    CAS  Google Scholar 

  • Jagannathan B and Golbeck JH (2008) Unifying principles in homodimeric type I photosynthetic reaction centers: Properties of PscB and the FA, FB and FX iron-sulfur clusters in green sulfur bacteria. Biochim Biophys Acta 1777: 1535–1544

    Article  PubMed  CAS  Google Scholar 

  • Jagannathan B and Golbeck JH (2009a) Photosynthesis: Microbial. In: Schaechter M (ed) Encyclopedia of Microbiology, 3rd Edition, pp 325–341. Elsevier, London

    Chapter  Google Scholar 

  • Jagannathan B and Golbeck JH (2009b) Breaking biological symmetry in membrane proteins: the asymmetrical orientation of PsaC on the pseudo-C2 symmetric photosystem I core. Cell Mol Life Sci 66: 1257–1270

    Article  PubMed  CAS  Google Scholar 

  • Jagannathan B and Golbeck JH (2009c) Understanding of the binding interface between PsaC and the PsaA/PsaB heterodimer in photosystem I. Biochemistry 48: 5405–5416

    Article  PubMed  CAS  Google Scholar 

  • Jagannathan B, Dekat S, Golbeck JH and Lakshmi KV (2010) The assembly of a multi-subunit photosynthetic membrane protein complex: A site-specific spin labeling EPR spectroscopic study of the PsaC subunit in photosystem I. Biochemistry 49: 2398–2408

    Google Scholar 

  • Jeanjean R, Latifi A, Matthijs HCP and Havaux M (2008) The PsaE subunit of photosystem I prevents light-induced formation of reduced oxygen species in the cyanobacterium Synechocystis sp. PCC 6803. Biochim Biophys Acta 1777: 308–316

    Article  PubMed  CAS  Google Scholar 

  • Jordan P, Fromme P, Witt HT, Klukas O, Saenger W and Krauß N (2001) Three dimensional structure of photosystem I at 2.5  Å resolution. Nature 411: 909–917

    Article  PubMed  CAS  Google Scholar 

  • Käss H, Fromme P and Lubitz W (1996) Quadrupole parameters of nitrogen nuclei in the cation radical P700•  + determined by ESEEM of single crystals of photosystem I. Chem Phys Lett 257: 197–206

    Article  Google Scholar 

  • Käss H, Fromme P, Witt HT and Lubitz W (2001) Orientation and electronic structure of the primary donor cation radical P700+ in photosystem I: A single crystals EPR and ENDOR study. J Phys Chem 105: 1225–1239

    Article  CAS  Google Scholar 

  • Kasting JF (2001) Earth history. The rise of atmospheric oxygen. Science 293: 819–820

    Article  CAS  Google Scholar 

  • Kaupp M (2002) The function of photosystem I. Quantum chemical insight into the role of tryptophan quinone interactions. Biochemistry 41: 2895–2900

    Article  PubMed  CAS  Google Scholar 

  • Kerr RA (2005) Earth science. The story of O2. Science 308: 1730–1732

    Article  PubMed  CAS  Google Scholar 

  • Kirschvink JL and Kopp RE (2008) Palaeoproterozoic ice houses and the evolution of oxygen-mediating enzymes: the case for a late origin of photosystem II. Philos Trans R Soc Lond B Biol Sci 363: 2755–2765

    Article  PubMed  CAS  Google Scholar 

  • Kjaer B and Scheller HV (1996) An isolated reaction center complex from the green sulfur bacterium Chlorobium vibioforme can photoreduce ferredoxin at high rates. Photosynth Res 47: 33–39

    Article  CAS  Google Scholar 

  • Kjaer B, Frigaard NU, Yang F, Zybailov B, Miller M, Golbeck JH and Scheller HV (1998) Menaquinone-7 in the reaction center complex of the green sulfur bacterium Chlorobium vibrioforme functions as the electron acceptor A1. Biochemistry 37: 3237–3242

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi M, van de Meent EJ, Erkelens C, Amesz J, Ikegami I and Watanabe T (1991a) Bacteriochlorophyll g epimer as a possible reaction center component of heliobacteria. Biochim Biophys Acta 1057: 89–96

    Article  CAS  Google Scholar 

  • Kobayashi M, Watanabe T, Ikegami I, van de Meent EJ and Amesz J (1991b) Enrichment of bacteriochlorophyll g’ in membranes of Heliobacterium chlorum by ether extraction. Unequivocal evidence for its existence in vivo. FEBS Lett 284: 129–31

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi M, Oh-Oka H, Akutsu S, Akiyama M, Tominaga K, Kise H, Nishida F, Watanabe T, Amesz J, Koizumi M, Ishida N and Kano H (2000) The primary electron acceptor of green sulfur bacteria, bacteriochlorophyll 663, is chlorophyll a esterified with ∆2,6-phytadienol. Photosynth Res 63: 269–280

    Article  PubMed  CAS  Google Scholar 

  • Krieger A, Rutherford AW and Johnson GN (1995) On the determination of redox midpoint potential of the primary quinone electron acceptor, QA, in photosystem II. Biochim Biophys Acta 1229: 193–201

    Article  Google Scholar 

  • Lagoutte B, Hanley J and Bottin H (2001) Multiple functions for the C terminus of the PsaD subunit in the cyanobacterial photosystem I complex. Plant Physiol 126: 307–316

    Article  PubMed  CAS  Google Scholar 

  • Lelong C, Sétif P, Lagoutte B and Bottin H (1994) Identification of the amino acids involved in the functional interaction between photosystem I and ferredoxin from Synechocystis sp. PCC 6803 by chemical cross-linking. J Biol Chem 269: 10034–10039

    PubMed  CAS  Google Scholar 

  • Lelong C, Boekema EJ, Kruip J, Bottin H, Rögner M and Sétif P (1996) Characterization of a redox active cross-linked complex between cyanobacterial photosystem I and soluble ferredoxin. EMBO J 15: 2160–2168

    PubMed  CAS  Google Scholar 

  • Liebl U, Mockensturm-Wilson M, Trost JT, Brune DC, Blankenship RE and Vermaas W (1993) Single core polypeptide in the reaction center of the photosynthetic bacterium Heliobacillus mobilis - structural implications and relations to other photosystems. Proc Natl Acad Sci USA 90: 7124–7128

    Article  PubMed  CAS  Google Scholar 

  • Lindahl, P. A., Day, E. P., Kent, T. A., Orme-Johnson, W. H. and Munck, E. (1985) Mossbauer, EPR, and magnetization studies of the Azotobacter vinelandii Fe protein. Evidence for a [4Fe-4S]1+ cluster with spin S  =  3/2. J Biol Chem 260: 11160–73

    PubMed  CAS  Google Scholar 

  • Lockhart PJ, Steel MA and Larkum AW (1996) Gene duplication and the evolution of photosynthetic reaction center proteins. FEBS Lett 385: 193–196

    Article  PubMed  CAS  Google Scholar 

  • Lubitz W (2006) EPR studies of the primary electron donor P700 in photosystem I. In: Golbeck JH (ed.) Advances in Photosynthesis (Series editor Govindjee). Photosystem I. The Plastocyanin: Ferredoxin Oxidoreductase in Photosynthesis, pp 245–269 Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Mac M, Bowlby NR, Babcock GT and McCracken J (1998) Monomeric spin density distrubution in the primary donor of photosystem I as determined by electron magnetic resonance: functional and thermodynamic implications. J Am Chem Soc 120: 13215–13223

    Article  CAS  Google Scholar 

  • Martin W and Russell MJ (2003) On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. Philos Trans Biol Sci 358: 59–85

    Article  CAS  Google Scholar 

  • Meimberg K, Fischer N, Rochaix JD and Mühlenhoff U (1999) Lys35 of PsaC is required for the efficient photoreduction of flavodoxin by photosystem I from Chlamydomonas reinhardtii. Eur J Biochem. 263: 137–144

    Article  PubMed  CAS  Google Scholar 

  • Mix LJ, Haig D and Cavanaugh CM (2005) Phylogenetic analyses of the core antenna domain: investigating the origin of photosystem I. J Mol Evol 60: 153–163

    Article  PubMed  CAS  Google Scholar 

  • Miyamoto R, Mino H, Kondo T, Itoh S and Oh-Oka H (2008) An electron spin-polarized signal of the P800  +  A1(Q)– state in the homodimeric reaction center core complex of Helio­bacterium modesticaldum. Biochemistry 47: 4386–4393

    Article  PubMed  CAS  Google Scholar 

  • Müh F, Renger T and Zouni A (2008) Crystal structure of cyanobacterial photosystem II at 3.0  Å resolution: A closer look at the antenna system and the small membrane-intrinsic subunits. Plant Physiol Biochem 46: 238–264

    Article  PubMed  CAS  Google Scholar 

  • Muhiuddin IP, Rigby SE, Evans MC, Amesz J and Heathcote P (1999) ENDOR and special TRIPLE resonance spectroscopy of photoaccumulated semiquinone electron acceptors in the reaction centers of green sulfur bacteria and heliobacteria. Biochemistry 38: 7159–7167

    Article  PubMed  CAS  Google Scholar 

  • Mühlenhoff U, Zhao JD and Bryant DA (1996) Interaction between photosystem I and flavodoxin from the cyanobacterium Synechococcus sp. PCC 7002 as revealed by chemical cross-linking. Eur J Biochem. 235: 324–331

    Article  PubMed  Google Scholar 

  • Mulkidjanian AY and Junge W (1997) On the origin of photosynthesis as inferred from sequence analysis - A primordial UV-protector as common ancestor of reaction centers and antenna proteins. Photosynth Res 51: 27–42

    Article  CAS  Google Scholar 

  • Mulkidjanian AY, Koonin EV, Makarova KS, Mekhedov SL, Sorokin A, Wolf YI, Dufresne A, Partensky F, Burd H, Kaznadzey D, Haselkorn R and Galperin MY (2006) The cyanobacterial genome core and the origin of photosynthesis. Proc Natl Acad Sci USA 103: 13126–13131

    Article  PubMed  CAS  Google Scholar 

  • Müller MG, Niklas J, Lubitz W and Holzwarth AR (2003) Ultrafast transient absorption studies on photosystem I reaction centers from Chlamydomonas reinhardtii. 1. A new interpretation of the energy trapping and early electron transfer steps in photosystem I. Biophys J 85: 3899–3922

    Article  PubMed  Google Scholar 

  • Nitschke W and Rutherford AW (1991) Photosynthetic reaction centres: variations on a common structural theme? Trends Biochem Sci 16: 241–245

    Article  PubMed  CAS  Google Scholar 

  • Nitschke W, Feiler U, Lockau W and Hauska G (1987) The photosystem of the green sulfur bacterium Chlorobium limicola contains two early electron acceptors similar to photosystem I. FEBS Lett 218: 283–286

    Article  CAS  Google Scholar 

  • Nitschke W, Setif P, Liebl U, Feiler U and Rutherford AW (1990) Reaction center photochemistry of Heliobacterium chlorum. Biochemistry 29: 11079–11088

    Article  PubMed  CAS  Google Scholar 

  • Nitschke W, Mattioli T and Rutherford AW (1996) The Fe-S type photosystems and the evolution of photosynthetic reaction centers. In: Baltscheffsky H (ed) Origin and Evolution of Biological Energy Conservation, pp 177–203. VCH, New York

    Google Scholar 

  • Noodleman L, Norman Jr JG, Osborne JH, Aizman A and Case DA (1985) Models for ferredoxins: Electronic structures of iron-sulfur clusters with one, two and four iron atoms. J Am Chem Soc 107: 3418–3426

    Article  CAS  Google Scholar 

  • Noodleman L, Peng CY, Case DA and Mouesca JM (1995) Orbital interactions, electron delocalization and spin coupling in iron-sulfur clusters. Coord Chem Rev 144: 199–244

    Article  CAS  Google Scholar 

  • Oh-oka H (2007) Type I reaction center of photosynthetic heliobacteria. Photochem Photobiol 83: 177–186

    Article  PubMed  CAS  Google Scholar 

  • Olson JM (2001) Evolution of Photosynthesis (1970), re-examined thirty years later. Photosynth Res 68: 95–112

    Article  PubMed  CAS  Google Scholar 

  • Olson JM (2006) Photosynthesis in the Archean era. Photosynth Res 88: 109–117

    Article  PubMed  CAS  Google Scholar 

  • Olson JM and Blankenship RE (2004) Thinking about the evolution of photosynthesis. Photosynth Res 80: 373–386

    Article  PubMed  CAS  Google Scholar 

  • Olson JM and Pierson BK (1987) Evolution of reaction centers in photosynthetic prokaryotes. Int Rev Cytol 108: 209–248

    Article  PubMed  CAS  Google Scholar 

  • Parrett KG, Mehari T, Warren PG and Golbeck JH (1989) Purification and properties of the intact P700 and FX–containing photosystem I core protein. Biochim Biophys Acta 973: 324–332

    Article  PubMed  CAS  Google Scholar 

  • Permentier HP, Schmidt KA, Kobayashi M, Akiyama M, Hager-Braun C, Neerken S, Miller M and Amesz J (2000) Composition and optical properties of reaction centre core complexes from the green sulfur bacteria Prosthecochloris aestuarii and Chlorobium tepidum. Photosynth Res 64: 27–39

    Article  PubMed  CAS  Google Scholar 

  • Pierson K (1994) Early life on earth. In: Bengtson S (ed) Nobel Symposium No. 84. Columbia Univ Press, New York

    Google Scholar 

  • Ptushenko VV, Cherepanov DA, Krishtalik LI and Semenov AY (2008) Semi-continuum electrostatic calculations of redox potentials in photosystem I. Photosynth Res 97: 55–74

    Article  PubMed  CAS  Google Scholar 

  • Que L, Jr., Bobrick MA, Ibers JA and Holm R (1974) Synthetic analogs of active sites of iron-sulfur proteins. VII. Ligand substitution reactions of the tetranuclear clusters [Fe4S4(SR)4]2- and the structure of [(CH3)4N]2 [Fe4S4(SC6H6)4]. J Am Chem Soc 96: 4168–4177

    Article  PubMed  CAS  Google Scholar 

  • Raymond J and Blankenship RE (2006) Evolutionary relationships among Type I reaction centers. In: Golbeck J (ed) Photosystem I: The Light-Driven Plastocyanin:Ferredoxin NADP+  Oxidoreductase, pp 413–437. Springer, Dordrecht

    Google Scholar 

  • Raymond J, Zhaxybayeva O, Gogarten JP, Gerdes SY and Blankenship RE (2002) Whole-genome analysis of photosynthetic prokaryotes. Science 298: 1616–1620

    Article  PubMed  CAS  Google Scholar 

  • Redding K and van der Est A (2006) The directionality of electron transport in photosystem I. In: Golbeck J (ed) Photosystem I: The Light-Induced Plastocyanin:Ferredoxin Oxidoreductase, pp 413–437. Springer, Dordrecht

    Google Scholar 

  • Renger G and Holzwarth AR (2005) Primary electron transfer. In: Wydrzynski TJ and Satoh K (eds) Photosystem II: The Light-Driven Water: Plastoquinone Oxidoreductase, pp 139–175. Springer, Dordrecht

    Chapter  Google Scholar 

  • Rigby SE, Thapar R, Evans MC and Heathcote P (1994) The electronic structure of P840+. The primary donor of the Chlorobium limicola f. sp. thiosulphatophilum photosynthetic reaction centre. FEBS Lett 350: 24–28

    Article  PubMed  CAS  Google Scholar 

  • Rippka R, Waterbury J and Cohen-Bazire G (1974) A cyanobacterium which lacks thylakoids. Arch Microbiol 100: 419–436

    Article  CAS  Google Scholar 

  • Romberger S, Castro C, Sun Y and Golbeck J (2010) Identification and characterization of PshBII, a second FA/FB-containing polypeptide in the photosynthetic reaction center of Heliobacterium modesticaldum. Photosynth Res 104: 293–303

    Google Scholar 

  • Sattley WM, Madigan MT, Swingley WD, Cheung PC, Clocksin KM, Conrad AL, Dejesa LC, Honchak BM, Jung DO, Karbach LE, Kurdoglu A, Lahiri S, Mastrian SD, Page LE, Taylor HL, Wang ZT, Raymond J, Chen M, Blankenship RE and Touchman JW (2008) The genome of Heliobacterium modesticaldum, a phototrophic representative of the Firmicutes containing the simplest photosynthetic apparatus. J Bacteriol 190: 4687–4696

    Article  PubMed  CAS  Google Scholar 

  • Savitsky A, Gopta O, Mamedov M, Golbeck J, Tikhonov A, Möbius K and Semenov AY (2009) Alteration of the axial Met ligand to electron acceptor A0 in photosystem I: Effect on the generation of P700+ A1– radical pairs as studied by W-band transient EPR. App Mag Res 37: 85–102

    Article  CAS  Google Scholar 

  • Schmidt KA, Neerken S, Permentier HP, Hager-Braun C and Amesz J (2000) Electron transfer in reaction center core complexes from the green sulfur bacteria Prosthecochloris aestuarii and Chlorobium tepidum. Biochemistry 39: 7212–7220

    Article  PubMed  CAS  Google Scholar 

  • Schubert WD, Klukas O, Saenger W, Witt HT, Fromme P and Krauß N (1998) A common ancestor for oxygenic and anoxygenic photosynthetic systems: A comparison based on the structural model of photosystem I. J Mol Biol 280: 297–314

    Article  PubMed  CAS  Google Scholar 

  • Sétif P (2001) Ferredoxin and flavodoxin reduction by photosystem I. Biochim Biophys Acta 1507: 161–179

    Article  PubMed  Google Scholar 

  • Sétif P, Fischer N, Lagoutte B, Bottin H and Rochaix JD (2002) The ferredoxin docking site of photosystem I. Biochim Biophys Acta 1555: 204–209

    Article  PubMed  Google Scholar 

  • Srinivasan N and Golbeck J (2009) Protein-cofactor interactions in bioenergetic systems. Biochim Biophys Acta 1787: 1057–1088

    Article  PubMed  CAS  Google Scholar 

  • Srinivasan N, Karyagina I, Bittl R, van der Est A and Golbeck JH (2009) Role of the hydrogen bond from Leu722 to the A1A phylloquinone in photosystem I. Biochemistry 48: 3315–3324

    Article  PubMed  CAS  Google Scholar 

  • Sticht H and Rösch P (1998) The structure of iron-sulfur proteins. Prog Biophys Mol Biol 70: 95–136

    Article  PubMed  CAS  Google Scholar 

  • Summons RE, Jahnke LL, Hope JM and Logan GA (1999) 2-Methylhopanoids as biomarkers for cyanobacterial oxygenic photosynthesis. Nature 400: 554–557

    Article  PubMed  CAS  Google Scholar 

  • Tian F, Toon OB, Pavlov AA and De Sterck H (2005) A hydrogen-rich early Earth atmosphere. Science 308: 1014–1017

    Article  PubMed  CAS  Google Scholar 

  • Trost JT and Blankenship RE (1989) Isolation of a photoactive photosynthetic reaction center-core antenna complex from Heliobacillus mobilis. Biochemistry 28: 9898–9904

    Article  PubMed  CAS  Google Scholar 

  • Tsukatani Y, Miyamoto R, Itoh S and Oh-Oka H (2004) Function of a PscD subunit in a homodimeric reaction center complex of the photosynthetic green sulfur bacterium Chlorobium tepidum studied by insertional gene inactivation. Regulation of energy transfer and ferredoxin-mediated NADP+ reduction on the cytoplasmic side. J Biol Chem 279: 51122–51130

    Article  PubMed  CAS  Google Scholar 

  • van de Meent EJ, Kobayashi M, Erkelens C, van Veelen PA, Amesz J and Watanabe T (1991) Identification of 81-hydroxychlorophyll a as a functional reaction center pigment in heliobacteria. Biochim Biophys Acta 1058: 356–362

    Article  Google Scholar 

  • van der Est A (2006) Electron transfer involving phylloquinone in photosystem I. In: Golbeck J (ed) Phototosystem I: The Light-Induced Plastocyanin:Ferredoxin Oxidoreductase, pp 387–411. Springer, Dordrecht

    Google Scholar 

  • van der Est A, Chirico S, Karyagina I, Cohen R, Shen G and Golbeck J (2009) Alteration of the axial Met ligand to electron acceptor A0 in Photosystem I: An investigation of low temperature electron transfer by multifrequency time -resolved and CW EPR. App Mag Res 37: 103–121

    Article  CAS  Google Scholar 

  • Varotto C, Pesaresi P, Meurer J, Oelmuller R, Steiner-Lange S, Salamini F and Leister D (2000) Disruption of the Arabidopsis photosystem I gene psaE1 affects photosynthesis and impairs growth. Plant J 22: 115–124

    Article  PubMed  CAS  Google Scholar 

  • Vassiliev IR, Jung YS, Smart LB, Schulz R, Mcintosh L and Golbeck JH (1995) A mixed-ligand iron-sulfur cluster (C556SPsaB or C565SPsaB) in the FX-binding site leads to a decreased quantum efficiency of electron transfer in photosystem I. Biophys J 69: 1544–1553

    Article  PubMed  CAS  Google Scholar 

  • Vassiliev IR, Jung YS, Mamedov MD, Semenov AY and Golbeck JH (1997) Near-IR absorbance changes and electrogenic reactions in the microsecond-to-second time domain in photosystem I. Biophys J 72: 301–315

    Article  PubMed  CAS  Google Scholar 

  • Vassiliev IR, Jung YS, Yang F and Golbeck JH (1998) PsaC subunit of photosystem I is oriented with iron-sulfur cluster FB as the immediate electron donor to ferredoxin and flavodoxin. Biophys J 74: 2029–2035

    Article  PubMed  CAS  Google Scholar 

  • Vassiliev IR, Ronan MT, Hauska G and Golbeck JH (2000) The bound electron acceptors in green sulfur bacteria: resolution of the g-tensor for the FX iron-sulfur cluster in Chlorobium tepidum. Biophys J 78: 3160–3169

    Article  PubMed  CAS  Google Scholar 

  • Vassiliev IR, Antonkine ML and Golbeck JH (2001) Iron-sulfur clusters in Type I reaction centers. Biochim Biophys Acta 1507: 139–160

    Article  PubMed  CAS  Google Scholar 

  • Vassilieva EV, Antonkine ML, Zybailov BL, Yang F, Jakobs CU, Golbeck JH and Bryant DA (2001) Electron transfer may occur in the chlorosome envelope: the CsmI and CsmJ proteins of chlorosomes are 2Fe-2S ferredoxins. Biochemistry 40: 464–473

    Article  PubMed  CAS  Google Scholar 

  • Vermaas WFJ (1994) Evolution of heliobacteria: implications for photosynthetic reaction center complexes. Photosynth Res 41: 285–294

    Article  PubMed  CAS  Google Scholar 

  • Vermaas WFJ (2002) Evolution of photosynthesis. In: Daly AO (ed) Encyclopedia of Life Sciences, pp 1–18. Nature Publishing Group, London

    Google Scholar 

  • Vos MH and van Gorkom HJ (1990) Thermodynamical and structural information on photosynthetic systems obtained from electroluminescence kinetics. Biophys J 58: 1547–1555

    Article  PubMed  CAS  Google Scholar 

  • Wächterhäuser G (1992) Groundworks for an evolutionary biochemistry: the iron-sulfur world. Prog Biophys Mol Biol 58: 85–201

    Article  Google Scholar 

  • Webber AN and Lubitz W (2001) P700: The primary electron donor of photosystem I. Biochim Biophys Acta 1507: 61–79

    Article  PubMed  CAS  Google Scholar 

  • Xiong J, Fischer WM, Inoue K, Nakahara M and Bauer CE (2000) Molecular evidence for the early evolution of photosynthesis. Science 289: 1724–1730

    Article  PubMed  CAS  Google Scholar 

  • Xu W, Chitnis P, Valieva A, van der Est A, Pushkar YN, Krzystyniak M, Teutloff C, Zech SG, Bittl R, Stehlik D, Zybailov B, Shen G and Golbeck JH (2003a) Electron transfer in cyanobacterial photosystem I: I. Physiological and spectroscopic characterization of site-directed mutants in a putative electron transfer pathway from A0 through A1 to FX. J Biol Chem 278: 27864–27875

    Article  PubMed  CAS  Google Scholar 

  • Xu W, Chitnis PR, Valieva A, van der Est A, Brettel K, Guergova-Kuras M, Pushkar YN, Zech SG, Stehlik D, Shen G, Zybailov B and Golbeck JH (2003b) Electron transfer in cyanobacterial photosystem I: II. Determination of forward electron transfer rates of site-directed mutants in a putative electron transfer pathway from A0 through A1 to FX. J Biol Chem 278: 27876–27887

    Article  PubMed  CAS  Google Scholar 

  • Yu L, Zhao JD, Mühlenhoff U, Bryant DA and Golbeck JH (1993) PsaE is required for in vivo cyclic electron flow around photosystem I in the cyanobacterium Synechococcus sp. PCC 7002. Plant Physiol 103: 171–180

    PubMed  CAS  Google Scholar 

  • Yu J, Smart LB, Jung YS, Golbeck J and McIntosh L (1995) Absence of PsaC subunit allows assembly of Photosystem I core but prevents the binding of PsaD and PsaE in Synechocystis sp. PCC 6803. Plant Mol. Biol. 29: 331–42

    Article  PubMed  CAS  Google Scholar 

  • Zahnle K, Arndt N, Cockell C, Halliday A, Nisbet E, Selsis F and Sleep NH (2007) Emergence of a habitable planet. Space Science Reviews 129: 35–78

    Article  CAS  Google Scholar 

  • Zhao J, Li N, Warren PV, Golbeck JH and Bryant DA (1992) Site-directed conversion of a cysteine to aspartate leads to the assembly of a [3Fe-4S] cluster in PsaC of photosystem I. The photoreduction of FA is independent of FB. Biochemistry 31: 139–160

    Article  Google Scholar 

  • Zhao J, Snyder WB, Muhlenhoff U, Rhiel E, Warren PV, Golbeck JH and Bryant DA (1993) Cloning and characterization of the psaE gene of the cyanobacterium Synechococcus sp. PCC 7002 - Characterization of a psaE mutant and overproduction of the protein in Escherichia coli. Mol Microbiol 9: 183–194

    Article  PubMed  CAS  Google Scholar 

  • Zouni A, Witt HT, Kern J, Fromme P, Krauß N, Saenger W and Orth P (2001) Crystal structure of photosystem II from Synechococcus elongatus at 3.8  Å resolution. Nature 409: 739–743

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by grants from the NSF (MCB-1021725) and the DOE (DE-FG-02-98-ER20314).

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Authors and Affiliations

  1. Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, PA, USA

    Bharat Jagannathan & Gaozhong Shen

  2. Department of Biochemistry and Molecular Biology and Department of Chemistry, The Pennsylvania State University, University Park, PA, USA

    John H. Golbeck

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  1. Bharat Jagannathan
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  2. Gaozhong Shen
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  3. John H. Golbeck
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Correspondence to John H. Golbeck .

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  1. Dept. Microbiology & Molecular Genetics, Oklahoma State University, Stillwater, 74075, Oklahoma, USA

    Robert Burnap

  2. School of Life Sciences &, Center for Bioenergy & Photosynthesis, Arizona State University, Tempe, 85287-4501, Arizona, USA

    Wim Vermaas

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Jagannathan, B., Shen, G., Golbeck, J.H. (2012). The Evolution of Type I Reaction Centers: The Response to Oxygenic Photosynthesis. In: Burnap, R., Vermaas, W. (eds) Functional Genomics and Evolution of Photosynthetic Systems. Advances in Photosynthesis and Respiration, vol 33. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-1533-2_12

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