Abstract
The proliferation of phototrophy within early-branching prokaryotes represented a significant step forward in metabolic evolution. All available evidence supports the hypothesis that the photosynthetic reaction center (RC)—the pigment-protein complex in which electromagnetic energy (i.e., photons of visible or near-infrared light) is converted to chemical energy usable by an organism—arose once in Earth’s history. This event took place over 3 billion years ago and the basic architecture of the RC has diversified into the distinct versions that now exist. Using our recent 2.2-Å X-ray crystal structure of the homodimeric photosynthetic RC from heliobacteria, we have performed a robust comparison of all known RC types with available structural data. These comparisons have allowed us to generate hypotheses about structural and functional aspects of the common ancestors of extant RCs and to expand upon existing evolutionary schemes. Since the heliobacterial RC is homodimeric and loosely binds (and reduces) quinones, we support the view that it retains more ancestral features than its homologs from other groups. In the evolutionary scenario we propose, the ancestral RC predating the division between Type I and Type II RCs was homodimeric, loosely bound two mobile quinones, and performed an inefficient disproportionation reaction to reduce quinone to quinol. The changes leading to the diversification into Type I and Type II RCs were separate responses to the need to optimize this reaction: the Type I lineage added a [4Fe–4S] cluster to facilitate double reduction of a quinone, while the Type II lineage heterodimerized and specialized the two cofactor branches, fixing the quinone in the QA site. After the Type I/II split, an ancestor to photosystem I fixed its quinone sites and then heterodimerized to bind PsaC as a new subunit, as responses to rising O2 after the appearance of the oxygen-evolving complex in an ancestor of photosystem II. These pivotal events thus gave rise to the diversity that we observe today.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Akiyama M, Miyashita H, Kise H et al (2002) Quest for minor but key chlorophyll molecules in photosynthetic reaction centers—unusual pigment composition in the reaction centers of the chlorophyll d-dominated cyanobacterium Acaryochloris marina. Photosynth Res 74:97–107. https://doi.org/10.1023/A:1020915506409
Albert I, Rutherford AW, Grav H et al (1998) The 18 kDa cytochrome c553 from Heliobacterium gestii: gene sequence and characterization of the mature protein. Biochemistry 37:9001–9008. https://doi.org/10.1021/bi9731347
Allen JF (2005) A redox switch hypothesis for the origin of two light reactions in photosynthesis. FEBS Lett 579:963–968. https://doi.org/10.1016/j.febslet.2005.01.015
Bak DW, Elliott SJ (2014) Alternative FeS cluster ligands: tuning redox potentials and chemistry. Curr Opin Chem Biol 19:50–58. https://doi.org/10.1016/j.cbpa.2013.12.015
Barber J (2012) Photosystem II: the water-splitting enzyme of photosynthesis. Cold Spring Harb Symp Quant Biol 77:295–307. https://doi.org/10.1101/sqb.2012.77.014472
Battistuzzi FU, Hedges SB (2009) A major clade of prokaryotes with ancient adaptations to life on land. Mol Biol Evol 26:335–343. https://doi.org/10.1093/molbev/msn247
Berman HM, Westbrook J, Feng Z et al (2000) The protein data bank. Nucleic Acids Res 28:235–242. https://doi.org/10.1093/nar/28.1.235
Blankenship RE (1992) Origin and early evolution of photosynthesis. Photosynth Res 33:91–111. https://doi.org/10.1104/pp.110.161687
Blankenship RE (2014) Molecular mechanisms of photosynthesis, 2nd edn. Wiley, Chicester
Blankenship RE, Sadekar S, Raymond J (2007) The evolutionary transition from anoxygenic to oxygenic photosynthesis. In: Falkowski PG, Knoll AH (eds) Evolution of primary producers in the sea. Elsevier, Boston, pp 21–35
Brettel K, Leibl W, Liebl U (1998) Electron transfer in the heliobacterial reaction center: evidence against a quinone-type electron acceptor functioning analogous to A1 in photosystem I. Biochim Biophys Acta 1363:175–181
Brok M, Vasmel H, Horikx JTG, Hoff AJ (1986) Electron transport components of Heliobacterium chlorum investigated by EPR spectroscopy at 9 and 35 GHz. FEBS Lett 194:322–326. https://doi.org/10.1016/0014-5793(86)80110-7
Bryant DA, Frigaard N-U (2006) Prokaryotic photosynthesis and phototrophy illuminated. Trends Microbiol 14:488–496. https://doi.org/10.1016/j.tim.2006.09.001
Bryant DA, Liu Z, Li T et al (2012) Comparative and functional genomics of anoxygenic green bacteria from the taxa Chlorobi, Chloroflexi, and Acidobacteria. In: Burnap R, Vermaas W (eds) Functional genomics and evolution of photosynthetic systems. Springer, Dordrecht, pp 47–102
Cardona T (2015) A fresh look at the evolution and diversification of photochemical reaction centers. Photosynth Res 126:111–134. https://doi.org/10.1007/s11120-014-0065-x
Cardona T (2016a) Reconstructing the origin of oxygenic photosynthesis: do assembly and photoactivation recapitulate evolution? Front Plant Sci 7:1–16. https://doi.org/10.3389/fpls.2016.00257
Cardona T (2016b) Origin of bacteriochlorophyll a and the early diversification of photosynthesis. PLoS ONE 11:e0151250. https://doi.org/10.1371/journal.pone.0151250
Cardona T, Sedoud A, Cox N, Rutherford AW (2012) Charge separation in photosystem II: a comparative and evolutionary overview. Biochim Biophys Acta 1817:26–43. https://doi.org/10.1016/j.bbabio.2011.07.012
Cardona T, Sanchez-Baracaldo P, Rutherford AW, Larkum AWD (2017) Molecular evidence for the early evolution of photosynthetic water oxidation. https://doi.org/10.1101/109447
Chauvet A, Sarrou J, Lin S et al (2013) Temporal and spectral characterization of the photosynthetic reaction center from Heliobacterium modesticaldum. Photosynth Res 116:1–9. https://doi.org/10.1007/s11120-013-9871-9
Chen M, Telfer A, Lin S et al (2005) The nature of the photosystem II reaction centre in the chlorophyll d-containing prokaryote, Acaryochloris marina. Photochem Photobiol Sci 4:1060. https://doi.org/10.1039/b507057k
Deisenhofer J, Epp O, Miki K et al (1985) Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3 Å resolution. Nature 318:618–624. https://doi.org/10.1038/318618a0
Dibrova DV, Cherepanov DA, Galperin MY et al (2013) Evolution of cytochrome bc complexes: from membrane-anchored dehydrogenases of ancient bacteria to triggers of apoptosis in vertebrates. Biochim Biophys Acta 1827:1407–1427. https://doi.org/10.1016/j.bbabio.2013.07.006
Diner BA, Petrouleas V, Wendoloski JJ (1991) The iron-quinone electron-acceptor complex of photosystem II. Physiol Plant 81:423–436. https://doi.org/10.1111/j.1399-3054.1991.tb08753.x
Doolittle RF (1986) Of URFs and ORFs: a primer on how to analyze derived amino acid sequences. University Science Books, Mill Valley
Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr Sect D 66:486–501. https://doi.org/10.1107/S0907444910007493
Etiope G, Sherwood Lollar B (2013) Abiotic methane on earth. Rev Geophys 51:276–299. https://doi.org/10.1002/rog.20011
Fajer J, Brune DC, Davis MS et al (1975) Primary charge separation in bacterial photosynthesis: oxidized chlorophylls and reduced pheophytin. Proc Natl Acad Sci USA 72:4956–4960
Ferlez BH, Cowgill JB, Dong W et al (2016) Thermodynamics of the electron acceptors in Heliobacterium modesticaldum: an exemplar of an early homodimeric Type I photosynthetic reaction center. Biochemistry 55:2358–2370. https://doi.org/10.1021/acs.biochem.5b01320
Fischer WW, Hemp J, Johnson JE (2016) Evolution of oxygenic photosynthesis. Annu Rev Earth Planet Sci 44:647–683. https://doi.org/10.1146/annurev-earth-060313-054810
Fromme P, Jordan P, Krauß N (2001) Structure of photosystem I. Biochim Biophys Acta 1507:5–31. https://doi.org/10.1016/S0005-2728(01)00195-5
Fuller RC, Sprague SG, Gest H, Blankenship RE (1985) A unique photosynthetic reaction center from Heliobacterium chlorum. FEBS Lett 182:345–349. https://doi.org/10.1016/0014-5793(85)80330-6
Furbacher PN, Tae GS, Cramer WA (1996) Evolution and origins of the cytochrome bc1 and b6f complexes. In: Baltscheffsky H (ed) Origin and evolution of biological energy conservation. Wiley, New York, pp 221–253
Garcia Costas AM, Liu Z, Tomsho LP et al (2012) Complete genome of Candidatus Chloracidobacterium thermophilum, a chlorophyll-based photoheterotroph belonging to the phylum Acidobacteria. Environ Microbiol 14:177–190. https://doi.org/10.1111/j.1462-2920.2011.02592.x
Gest H, Favinger JL (1983) Heliobacterium chlorum, an anoxygenic brownish-green photosynthetic bacterium containing a “new” form of bacteriochlorophyll. Arch Microbiol 136:11–16. https://doi.org/10.1007/BF00415602
Gisriel C, Sarrou I, Ferlez B et al (2017) Structure of a symmetric photosynthetic reaction center–photosystem. Science 357:1021–1025. https://doi.org/10.1126/science.aan5611
Graige MS, Paddock ML, Bruce JM et al (1996) Mechanism of proton-coupled electron transfer for quinone (QB) reduction in reaction centers of Rb. sphaeroides. J Am Chem Soc 118:9005–9016. https://doi.org/10.1021/ja960056m
Granick S (1957) Speculations on the origins and evolution of photosynthesis. Ann N Y Acad Sci 69:292–308. https://doi.org/10.1111/j.1749-6632.1957.tb49665.x
Granick S (1965) Evolution of heme and chlorophyll. Academic Press Inc, New York
Guergova-Kuras M, Boudreaux B, Joliot A et al (2001) Evidence for two active branches for electron transfer in photosystem I. Proc Natl Acad Sci USA 98:4437–4442. https://doi.org/10.1073/pnas.081078898
Gunner MR, Nicholls A, Honig B (1996) Electrostatic potentials in Rhodopseudomonas viridis reaction centers: implications for the driving force and directionality of electron transferase. J Phys Chem 100:4277–4291. https://doi.org/10.1021/jp9519070
Hansson A, Amann K, Zygadlo A et al (2007) Knock-out of the chloroplast-encoded PSI-J subunit of photosystem I in Nicotiana tabacum. FEBS J 274:1734–1746. https://doi.org/10.1111/j.1742-4658.2007.05722.x
Heathcote P, Fyfe PK, Jones MR (2002) Reaction centres: the structure and evolution of biological solar power. Trends Biochem Sci 27:79–87. https://doi.org/10.1016/S0968-0004(01)02034-5
Heinnickel M, Golbeck JH (2007) Heliobacterial photosynthesis. Photosynth Res 92:35–53. https://doi.org/10.1007/s11120-007-9162-4
Heinnickel M, Shen G, 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. https://doi.org/10.1021/bi0622165
Hemm MR, Paul BJ, Schneider TD et al (2008) Small membrane proteins found by comparative genomics and ribosome binding site models. Mol Microbiol 70:1487–1501. https://doi.org/10.1111/j.1365-2958.2008.06495.x
Hohmann-Marriott MF, Blankenship RE (2011) Evolution of photosynthesis. Annu Rev Plant Biol 62:515–548. https://doi.org/10.1146/annurev-arplant-042110-103811
Joe H, Kuma K, Paplawsky W et al (1986) Abiotic photosynthesis from ferrous carbonate (siderite) and water. Orig Life Evol Biosph 16:369–370. https://doi.org/10.1007/BF02422078
Jordan P, Fromme P, Witt HT et al (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411:909–917. https://doi.org/10.1038/35082000
Kashey TS, Luu DD, Cowgill JC et al (2018) Light-driven quinone reduction in heliobacterial membranes. Photosynth Res. https://doi.org/10.1007/s11120-018-0496-x
Keeling PJ (2010) The endosymbiotic origin, diversification and fate of plastids. Philos Trans R Soc Lond B 365:729–748. https://doi.org/10.1098/rstb.2009.0103
Khadka B, Adeolu M, Blankenship RE, Gupta RS (2017) Novel insights into the origin and diversification of photosynthesis based on analyses of conserved indels in the core reaction center proteins. Photosynth Res 131:159–171. https://doi.org/10.1007/s11120-016-0307-1
Kirmaier C, Holten D, Parson WW (1985) Picosecond-photodichroism studies of the transient states in Rhodopseudomonas sphaeroides reaction centers at 5 K. Effects of electron transfer on the six bacteriochlorin pigments. Biochim Biophys Acta 810:49–61. https://doi.org/10.1016/0005-2728(85)90205-1
Kirmaier C, Gaul D, DeBey R et al (1991) Charge separation in a reaction center incorporating bacteriochlorophyll for photoactive bacteriopheophytin. Science 251:922–927. https://doi.org/10.1126/science.2000491
Kirmaier C, Laporte L, Schenck CC, Holten D (1995a) The nature and dynamics of the charge-separated intermediate in reaction centers in which bacteriochlorophyll replaces the photoactive bacteriopheophytin. 1. Spectral characterization of the transient state. J Phys Chem 99:8903–8909. https://doi.org/10.1021/j100021a067
Kirmaier C, Laporte L, Schenck CC, Holten D (1995b) The nature and dynamics of the charge-separated intermediate in reaction centers in which bacteriochlorophyll replaces the photoactive bacteriopheophytin. 2. The rates and yields of charge separation and recombination. J Phys Chem 99:8910–8917. https://doi.org/10.1021/j100021a068
Kleinherenbrink FAM, Ikegami I, Hiraishi A et al (1993) Electron transfer in menaquinone-depleted membranes of Heliobacterium chlorum. Biochim Biophys Acta 1142:69–73. https://doi.org/10.1016/0005-2728(93)90085-T
Kleinherenbrink FAM, Chiou H-C, LoBrutto R, Blankenship RE (1994) Spectroscopic evidence for the presence of an iron-sulfur center similar to Fx of photosystem I in Heliobacillus mobilis. Photosynth Res 41:115–123. https://doi.org/10.1007/BF02184151
Kobayashi M, van de Meent EJ, Oh-oka H et al (1992) Pigment composition of heliobacteria and green sulfur bacteria. In: Murata N (ed) Research in photosynthesis, vol 1. Kluwer, Dordrecht, pp 393–396
Kondo T, Itoh S, Matsuoka M et al (2015) Menaquinone as the secondary electron acceptor in the Type I homodimeric photosynthetic reaction center of Heliobacterium modesticaldum. J Phys Chem B 119:8480–8489. https://doi.org/10.1021/acs.jpcb.5b03723
Krissinel E, Henrick K (2005) Multiple alignment of protein structures in three dimensions. Lecture notes in computer science (including subseries lecture notes in artificial intelligence and lecture notes in bioinformatics), pp 67–78
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Le SQ, Gascuel O (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25:1307–1320. https://doi.org/10.1093/molbev/msn067
Li Y, Lucas MG, Konovalova T et al (2004) Mutation of the putative hydrogen-bond donor to P700 of photosystem I. Biochemistry 43:12634–12647. https://doi.org/10.1021/bi036329p
Liebl U, Mockensturm-Wilson M, Trost JT et al (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
Lin S, Chiou HC, Blankenship RE (1995) Secondary electron transfer processes in membranes of Heliobacillus mobilis. Biochemistry 34:12761–12767
Lince MT, Vermaas W (1998) Association of His117 in the D2 protein of photosystem II with a chlorophyll that affects excitation-energy transfer efficiency to the reaction center. Eur J Biochem 256:595–602
Lockhart PJ, Larkum AWD, Steel MA et al (1996) Evolution of chlorophyll and bacteriochlorophyll: the problem of invariant sites in sequence analysis. Proc Natl Acad Sci USA 93:1930–1934. https://doi.org/10.1073/pnas.93.5.1930
Martin WF, Bryant DA, Beatty JT (2017) A physiological perspective on the origin and evolution of photosynthesis. FEMS Microbiol Rev 205–231. https://doi.org/10.1093/femsre/fux056
McConnell MD, Cowgill JB, Baker PL et al (2011) Double reduction of plastoquinone to plastoquinol in photosystem I. Biochemistry 50:11034–11046. https://doi.org/10.1021/bi201131r
Miller KR, Jacob JS, Smith U et al (1986) Heliobacterium chlorum: cell organization and structure. Arch Microbiol 146:111–114. https://doi.org/10.1007/BF00402335
Mix LJ, Harmer TL, Cavanaugh CM (2004) Sequence of the core antenna domain from the anoxygenic phototroph Heliophilum fasciatum: implications for diversity of reaction center Type I. Curr Microbiol 48:438–440. https://doi.org/10.1007/s00284-003-4221-3
Mix LJ, Haig D, Cavanaugh CM (2005) Phylogenetic analyses of the core antenna domain: investigating the origin of photosystem I. J Mol Evol 60:153–163. https://doi.org/10.1007/s00239-003-0181-2
Miyamoto R, Iwaki M, Mino H et al (2006) ESR signal of the iron–sulfur center FX and its function in the homodimeric reaction center of Heliobacterium modesticaldum. Biochemistry 45:6306–6316. https://doi.org/10.1021/bi0519710
Miyamoto R, Mino H, Kondo T et al (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. https://doi.org/10.1021/bi701612v
Muhiuddin IP, Heathcote P, Carter S et al (2001) Evidence from time resolved studies of the P700+ /A1—radical pair for photosynthetic electron transfer on both the PsaA and PsaB branches of the photosystem I reaction centre. FEBS Lett 503:56–60. https://doi.org/10.1016/S0014-5793(01)02696-5
Müller MG, Niklas J, Lubitz W, 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. https://doi.org/10.1016/S0006-3495(03)74804-8
Müller MG, Slavov C, Luthra R et al (2010) Independent initiation of primary electron transfer in the two branches of the photosystem I reaction center. Proc Natl Acad Sci USA 107:4123–4128. https://doi.org/10.1073/pnas.0905407107
Nelson N, Ben-Shem A (2004) The complex architecture of oxygenic photosynthesis. Nat Rev Mol Cell Biol 5:971–982. https://doi.org/10.1038/nrm1525
Nelson N, Yocum CF (2006) Structure and function of photosystems I and II. Annu Rev Plant Biol 57:521–565. https://doi.org/10.1146/annurev.arplant.57.032905.105350
Nitschke W, Rutherford AW (1991) Photosynthetic reaction centers—variations on a common structural theme. Trends Biochem Sci 16:241–245
Nitschke W, Mattioli T, 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. VCH, New York, pp 177–203
Ohashi S, Iemura T, Okada N et al (2010) An overview on chlorophylls and quinones in the photosystem I-type reaction centers. Photosynth Res 104:305–319. https://doi.org/10.1007/s11120-010-9530-3
Oh-oka H (2007) Type 1 reaction center of photosynthetic heliobacteria. Photochem Photobiol 83:177–186. https://doi.org/10.1562/2006-03-29-IR-860
Okamura MY, Feher G (1992) Proton transfer in reaction centers from photosynthetic bacteria. Annu Rev Biochem 61:861–896. https://doi.org/10.1146/annurev.bi.61.070192.004241
Okamura MY, Paddock ML, Graige MS, Feher G (2000) Proton and electron transfer in bacterial reaction centers. Biochim Biophys Acta 1458:148–163. https://doi.org/10.1016/S0005-2728(00)00065-7
Olson JM (1981) Evolution of photosynthetic reaction centers. Biosystems 14:89–94
Olson JM, Blankenship RE (2004) Thinking about the evolution of photosynthesis. In: Govindjee, Beatty JT, Gest H, Allen JF (eds) Discoveries in photosynthesis. Advances in photosynthesis and respiration, vol 20. Springer, Dordrecht, pp 1073–1086
Pan J, Saer RG, Lin S et al (2016) Electron transfer in bacterial reaction centers with the photoactive bacteriopheophytin replaced by a bacteriochlorophyll through coordinating ligand substitution. Biochemistry 55:4909–4918. https://doi.org/10.1021/acs.biochem.6b00317
Parson WW, Chu ZT, Warshel A (1990) Electrostatic control of charge separation in bacterial photosynthesis. Biochim Biophys Acta 1017:251–272. https://doi.org/10.1016/0005-2728(90)90192-7
Pei J, Kim B-H, Grishin NV (2008) PROMALS3D: a tool for multiple protein sequence and structure alignments. Nucleic Acids Res 36:2295–2300. https://doi.org/10.1093/nar/gkn072
Poluektov OG, Paschenko SV, Utschig LM et al (2005) Bidirectional electron transfer in photosystem I: direct evidence from high-frequency time-resolved EPR spectroscopy. J Am Chem Soc 127:11910–11911. https://doi.org/10.1021/ja053315t
Pribil M, Labs M, Leister D (2014) Structure and dynamics of thylakoids in land plants. J Exp Bot 65:1955–1972
Prince RC, Gest H, Blankenship RE (1985) Thermodynamic properties of the photochemical reaction center of Heliobacterium chlorum. Biochim Biophys Acta 810:377–384. https://doi.org/10.1016/0005-2728(85)90224-5
PyMOL (2014) The PyMOL molecular graphics system, version 1.8. Schrödinger, LLC. https://pymol.org
Ragsdale SW, Pierce E (2008) Acetogenesis and the Wood-Ljungdahl pathway of CO2 fixation. Biochim Biophys Acta 1784:1873–1898. https://doi.org/10.1016/j.bbapap.2008.08.012
Rémigy H-W, Stahlberg H, Fotiadis D et al (1999) The reaction center complex from the green sulfur bacterium Chlorobium tepidum: a structural analysis by scanning transmission electron microscopy. J Mol Biol 290:851–858. https://doi.org/10.1006/jmbi.1999.2925
Romberger SP, Golbeck JH (2012) The FX iron-sulfur cluster serves as the terminal bound electron acceptor in heliobacterial reaction centers. Photosynth Res 111:285–290. https://doi.org/10.1007/s11120-012-9723-z
Rost B (1999) Twilight zone of protein sequence alignments. Protein Eng Des Sel 12:85–94. https://doi.org/10.1093/protein/12.2.85
Rutherford AW, Mattiolo TA, Nitschke W (1996) The FeS-type photosystems and the evolution of photosynthetic reaction centers. In: Baltscheffsky H (ed) Origin and evolution of biological energy conversion. VCH, New York, pp 177–204
Rutherford AW, Osyczka A, Rappaport F (2012) Back-reactions, short-circuits, leaks and other energy wasteful reactions in biological electron transfer: redox tuning to survive life in O2. FEBS Lett 586:603–616
Sadekar S, Raymond J, Blankenship RE (2006) Conservation of distantly related membrane proteins: photosynthetic reaction centers share a common structural core. Mol Biol Evol 23:2001–2007. https://doi.org/10.1093/molbev/msl079
Santabarbara S, Heathcote P, Evans MCW (2005) Modelling of the electron transfer reactions in photosystem I by electron tunnelling theory: the phylloquinones bound to the PsaA and the PsaB reaction centre subunits of PS I are almost isoenergetic to the iron-sulfur cluster FX. Biochim Biophys Acta 1708:283–310
Santabarbara S, Bullock B, Rappaport F, Redding KE (2015) Controlling electron transfer between the two cofactor chains of photosystem I by the redox state of one of their components. Biophys J 108:1537–1547. https://doi.org/10.1016/j.bpj.2015.01.009
Sarrou I, Khan Z, Cowgill JB et al (2012) Purification of the photosynthetic reaction center from Heliobacterium modesticaldum. Photosynth Res 111:291–302. https://doi.org/10.1007/s11120-012-9726-9
Sattley WM, Swingley WD (2013) Properties and evolutionary implications of the heliobacterial genome. In: Beatty JT (ed) Advances in botanical research vol 66: genome evolution of photosynthetic bacteria. Academic Press Inc., Oxford, pp 67–97
Sattley WM, Madigan MT, Swingley WD et al (2008) The genome of Heliobacterium modesticaldum, a phototrophic representative of the Firmicutes containing the simplest photosynthetic apparatus. J Bacteriol 190:4687–4696. https://doi.org/10.1128/JB.00299-08
Schelvis JPM, van Noort PI, Aartsma TJ, van Gorkom HJ (1994) Energy transfer, charge separation and pigment arrangement in the reaction center of photosystem II. Biochim Biophys Acta 1184:242–250. https://doi.org/10.1016/0005-2728(94)90229-1
Schubert W-D, Klukas O, Saenger W et al (1998) A common ancestor for oxygenic and anoxygenic photosynthetic systems. J Mol Biol 280:297–314. https://doi.org/10.1006/jmbi.1998.1824
Schweitzer RH, Brudvig GW (1997) Fluorescence quenching by chlorophyll cations in photosystem II. Biochemistry 36:11351–11359. https://doi.org/10.1021/bi9709203
Schweitzer RH, Melkozernov AN, Blankenship RE, Brudvig GW (1998) Time-resolved fluorescence measurements of photosystem II: the effect of quenching by oxidized chlorophyll Z. J Phys Chem B 102:8320–8326. https://doi.org/10.1021/jp982098y
Shi T, Bibby TS, Jiang L et al (2005) Protein interactions limit the rate of evolution of photosynthetic genes in cyanobacteria. Mol Biol Evol 22:2179–2189. https://doi.org/10.1093/molbev/msi216
Sievers F, Wilm A, Dineen D et al (2011) Fast, scalable generation of high quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol. https://doi.org/10.1038/msb.2011.75
Sneath PHA, Sokal RR (1973) Numerical taxonomy. Freeman, San Francisco
The UniProt Consortium (2017) UniProt: the universal protein knowledgebase. Nucleic Acids Res 45:D158–D169. https://doi.org/10.1093/nar/gkw1099
Tomo T, Okubo T, Akimoto S et al (2007) Identification of the special pair of photosystem II in a chlorophyll d-dominated cyanobacterium. Proc Natl Acad Sci USA 104:7283–7288. https://doi.org/10.1073/pnas.0701847104
Trost JT, Blankenship RE (1989) Isolation of a photoactive photosynthetic reaction center-core antenna complex from Heliobacillus mobilis. Biochemistry 28:9898–9904
Trost JT, Brune DC, Blankenship RE (1992) Protein sequences and redox titrations indicate that the electron acceptors in reaction centers from heliobacteria are similar to photosystem I. Photosynth Res 32:11–22. https://doi.org/10.1007/BF00028794
van de Meent EJ, Kobayashi M, Erkelens C et al (1991) Identification of 81-hydroxychlorophyll a as a functional reaction center pigment in heliobacteria. Biochim Biophys Acta 1058:356–362. https://doi.org/10.1016/S0005-2728(05)80131-8
van der Est A, Hager-Braun C, Leibl W et al (1998) Transient electron paramagnetic resonance spectroscopy on green-sulfur bacteria and heliobacteria at two microwave frequencies. Biochim Biophys Acta 1409:87–98. https://doi.org/10.1016/S0005-2728(98)00152-2
Vassiliev IR, Antonkine ML, Golbeck JH (2001) Iron-sulfur clusters in Type I reaction centers. Biochim Biophys Acta 1507:139–160. https://doi.org/10.1016/S0005-2728(01)00197-9
Vermaas WFJ (1994) Evolution of heliobacteria: implications for photosynthetic reaction center complexes. Photosynth Res 41:285–294. https://doi.org/10.1007/BF02184169
Warren PV, Golbeck JH, Warden JT (1993) Charge recombination between P700 + and A1– occurs directly to the ground state of P700 in a photosystem I core devoid of FX, FB, and FA. Biochemistry 32:849–857. https://doi.org/10.1021/bi00054a016
Warshel A, Chu ZT, Parson WW (1994) On the energetics of the primary electron-transfer process in bacterial reaction centers. J Photochem Photobiol A 82:123–128. https://doi.org/10.1016/1010-6030(94)02010-8
Webber AN, Lubitz W (2001) P700: the primary electron donor of photosystem I. Biochim Biophys Acta 1507:61–79. https://doi.org/10.1016/S0005-2728(01)00198-0
Whelan S, Goldman N (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18:691–699. https://doi.org/10.1093/oxfordjournals.molbev.a003851
Xiong J, Inoue K, Bauer CE (1998) Tracking molecular evolution of photosynthesis by characterization of a major photosynthesis gene cluster from Heliobacillus mobilis. Proc Natl Acad Sci USA 95:14851–14856. https://doi.org/10.1073/pnas.95.25.14851
Zeng Y, Feng F, Medová H et al (2014) Functional type 2 photosynthetic reaction centers found in the rare bacterial phylum Gemmatimonadetes. Proc Natl Acad Sci USA 111:7795–7800. https://doi.org/10.1073/pnas.1400295111
Zouni A, Witt H-T, Kern J et al (2001) Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409:739–743. https://doi.org/10.1038/35055589
Acknowledgements
The authors thank Dr. Gillian Gile (Arizona State University) for consultation on phylogenetic tree construction, Mr. Bill Johnson (Arizona State University) for artistic input on figures, and Dr. Robert Blankenship (Washington University in St. Louis) for sharing the draft genome of Heliorestis convoluta. All authors were supported by the Division of Chemical Sciences, Geosciences, and Biosciences, Office of Basic Energy Sciences, of the U.S. Department of Energy through Grant DE-SC0010575.
Author information
Authors and Affiliations
Corresponding author
Additional information
Gregory S. Orf and Christopher Gisriel have contributed equally to this work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Orf, G.S., Gisriel, C. & Redding, K.E. Evolution of photosynthetic reaction centers: insights from the structure of the heliobacterial reaction center. Photosynth Res 138, 11–37 (2018). https://doi.org/10.1007/s11120-018-0503-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-018-0503-2