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Title: Evolution of photosynthetic reaction centers: insights from the structure of the heliobacterial reaction center

Abstract

We report that 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 that the ancestral RC predating the division between Type I and Type II RCs was homodimeric, loosely bound two quinones, and performed an inefficient, light-driven disproportionation reaction to reducemore » 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 an [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. Lastly, these pivotal events thus gave rise to the diversity that we observe today.« less

Authors:
ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]
  1. Arizona State Univ., Tempe, AZ (United States)
Publication Date:
Research Org.:
Arizona State Univ., Tempe, AZ (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Chemical Sciences, Geosciences & Biosciences Division
OSTI Identifier:
1494566
Grant/Contract Number:  
SC0010575
Resource Type:
Accepted Manuscript
Journal Name:
Photosynthesis Research
Additional Journal Information:
Journal Volume: 138; Journal Issue: 1; Journal ID: ISSN 0166-8595
Publisher:
Springer
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Photosynthesis; Reaction center; Evolution of photosynthesis; Sequence alignments; Structural alignments; Heliobacteria

Citation Formats

Orf, Gregory S., Gisriel, Christopher, and Redding, Kevin E. Evolution of photosynthetic reaction centers: insights from the structure of the heliobacterial reaction center. United States: N. p., 2018. Web. doi:10.1007/s11120-018-0503-2.
Orf, Gregory S., Gisriel, Christopher, & Redding, Kevin E. Evolution of photosynthetic reaction centers: insights from the structure of the heliobacterial reaction center. United States. doi:10.1007/s11120-018-0503-2.
Orf, Gregory S., Gisriel, Christopher, and Redding, Kevin E. Fri . "Evolution of photosynthetic reaction centers: insights from the structure of the heliobacterial reaction center". United States. doi:10.1007/s11120-018-0503-2. https://www.osti.gov/servlets/purl/1494566.
@article{osti_1494566,
title = {Evolution of photosynthetic reaction centers: insights from the structure of the heliobacterial reaction center},
author = {Orf, Gregory S. and Gisriel, Christopher and Redding, Kevin E.},
abstractNote = {We report that 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 that the ancestral RC predating the division between Type I and Type II RCs was homodimeric, loosely bound two quinones, and performed an inefficient, light-driven 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 an [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. Lastly, these pivotal events thus gave rise to the diversity that we observe today.},
doi = {10.1007/s11120-018-0503-2},
journal = {Photosynthesis Research},
number = 1,
volume = 138,
place = {United States},
year = {2018},
month = {3}
}

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Works referenced in this record:

Acetogenesis and the Wood–Ljungdahl pathway of CO2 fixation
journal, December 2008

  • Ragsdale, Stephen W.; Pierce, Elizabeth
  • Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1784, Issue 12, p. 1873-1898
  • DOI: 10.1016/j.bbapap.2008.08.012

Structure of photosystem I
journal, October 2001

  • Fromme, Petra; Jordan, Patrick; Krauß, Norbert
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1507, Issue 1-3
  • DOI: 10.1016/S0005-2728(01)00195-5

Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3Å resolution
journal, December 1985

  • Deisenhofer, J.; Epp, O.; Miki, K.
  • Nature, Vol. 318, Issue 6047
  • DOI: 10.1038/318618a0

A General Empirical Model of Protein Evolution Derived from Multiple Protein Families Using a Maximum-Likelihood Approach
journal, May 2001


Bidirectional Electron Transfer in Photosystem I:  Direct Evidence from High-Frequency Time-Resolved EPR Spectroscopy
journal, August 2005

  • Poluektov, Oleg G.; Paschenko, Sergei V.; Utschig, Lisa M.
  • Journal of the American Chemical Society, Vol. 127, Issue 34
  • DOI: 10.1021/ja053315t

Early Evolution of Photosynthesis
journal, October 2010


Independent initiation of primary electron transfer in the two branches of the photosystem I reaction center
journal, February 2010

  • Muller, M. G.; Slavov, C.; Luthra, R.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 9
  • DOI: 10.1073/pnas.0905407107

Transient electron paramagnetic resonance spectroscopy on green-sulfur bacteria and heliobacteria at two microwave frequencies
journal, December 1998

  • van der Est, A.; Hager-Braun, C.; Leibl, W.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1409, Issue 2
  • DOI: 10.1016/S0005-2728(98)00152-2

Functional type 2 photosynthetic reaction centers found in the rare bacterial phylum Gemmatimonadetes
journal, May 2014

  • Zeng, Y.; Feng, F.; Medova, H.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 21
  • DOI: 10.1073/pnas.1400295111

A redox switch hypothesis for the origin of two light reactions in photosynthesis
journal, January 2005


Light-driven quinone reduction in heliobacterial membranes
journal, March 2018

  • Kashey, Trevor S.; Luu, Dustin D.; Cowgill, John C.
  • Photosynthesis Research, Vol. 138, Issue 1
  • DOI: 10.1007/s11120-018-0496-x

Abiotic photosynthesis from ferrous carbonate (siderite) and water
journal, September 1986

  • Joe, H.; Kuma, K.; Paplawsky, W.
  • Origins of Life and Evolution of the Biosphere, Vol. 16, Issue 3-4
  • DOI: 10.1007/BF02422078

Evolution of photosynthetic reaction centers
journal, January 1981


Isolation of a photoactive photosynthetic reaction center-core antenna complex from Heliobacillus mobilis
journal, December 1989

  • Trost, Jeffrey T.; Blankenship, Robert E.
  • Biochemistry, Vol. 28, Issue 26
  • DOI: 10.1021/bi00452a003

Evolution of Photosynthesis
journal, June 2011


ESR Signal of the Iron−Sulfur Center F X and Its Function in the Homodimeric Reaction Center of Heliobacterium modesticaldum ,
journal, May 2006

  • Miyamoto, Ryo; Iwaki, Masayo; Mino, Hiroyuki
  • Biochemistry, Vol. 45, Issue 20
  • DOI: 10.1021/bi0519710

Primary charge separation in bacterial photosynthesis: oxidized chlorophylls and reduced pheophytin.
journal, December 1975

  • Fajer, J.; Brune, D. C.; Davis, M. S.
  • Proceedings of the National Academy of Sciences, Vol. 72, Issue 12
  • DOI: 10.1073/pnas.72.12.4956

The endosymbiotic origin, diversification and fate of plastids
journal, March 2010

  • Keeling, Patrick J.
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 365, Issue 1541
  • DOI: 10.1098/rstb.2009.0103

Charge separation in Photosystem II: A comparative and evolutionary overview
journal, January 2012

  • Cardona, Tanai; Sedoud, Arezki; Cox, Nicholas
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 1
  • DOI: 10.1016/j.bbabio.2011.07.012

Reaction centres: the structure and evolution of biological solar power
journal, February 2002


Heliobacterium chlorum, an anoxygenic brownish-green photosynthetic bacterium containing a ?new? form of bacteriochlorophyll
journal, October 1983

  • Gest, Howard; Favinger, Jeffrey L.
  • Archives of Microbiology, Vol. 136, Issue 1
  • DOI: 10.1007/BF00415602

Heliobacterial photosynthesis
journal, April 2007


P700: the primary electron donor of photosystem I
journal, October 2001

  • Webber, Andrew N.; Lubitz, Wolfgang
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1507, Issue 1-3
  • DOI: 10.1016/S0005-2728(01)00198-0

Novel insights into the origin and diversification of photosynthesis based on analyses of conserved indels in the core reaction center proteins
journal, September 2016

  • Khadka, Bijendra; Adeolu, Mobolaji; Blankenship, Robert E.
  • Photosynthesis Research, Vol. 131, Issue 2
  • DOI: 10.1007/s11120-016-0307-1

Fluorescence Quenching by Chlorophyll Cations in Photosystem II
journal, September 1997

  • Schweitzer, Robert H.; Brudvig, Gary W.
  • Biochemistry, Vol. 36, Issue 38
  • DOI: 10.1021/bi9709203

Spectroscopic evidence for the presence of an iron-sulfur center similar to Fx of Photosystem I inHeliobacillus mobilis
journal, July 1994

  • Kleinherenbrink, Frank A. M.; Chiou, Hung-Cheng; LoBrutto, Russell
  • Photosynthesis Research, Vol. 41, Issue 1
  • DOI: 10.1007/BF02184151

A physiological perspective on the origin and evolution of photosynthesis
journal, November 2017

  • Martin, William F.; Bryant, Donald A.; Beatty, J. Thomas
  • FEMS Microbiology Reviews, Vol. 42, Issue 2
  • DOI: 10.1093/femsre/fux056

Proton and electron transfer in bacterial reaction centers
journal, May 2000

  • Okamura, M. Y.; Paddock, M. L.; Graige, M. S.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1458, Issue 1
  • DOI: 10.1016/S0005-2728(00)00065-7

Charge separation in a reaction center incorporating bacteriochlorophyll for photoactive bacteriopheophytin
journal, February 1991


The complex architecture of oxygenic photosynthesis
journal, December 2004

  • Nelson, Nathan; Ben-Shem, Adam
  • Nature Reviews Molecular Cell Biology, Vol. 5, Issue 12
  • DOI: 10.1038/nrm1525

The Genome of Heliobacterium modesticaldum, a Phototrophic Representative of the Firmicutes Containing the Simplest Photosynthetic Apparatus
journal, April 2008

  • Sattley, W. M.; Madigan, M. T.; Swingley, W. D.
  • Journal of Bacteriology, Vol. 190, Issue 13
  • DOI: 10.1128/JB.00299-08

Evolution of cytochrome bc complexes: From membrane-anchored dehydrogenases of ancient bacteria to triggers of apoptosis in vertebrates
journal, November 2013

  • Dibrova, Daria V.; Cherepanov, Dmitry A.; Galperin, Michael Y.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 11-12
  • DOI: 10.1016/j.bbabio.2013.07.006

Structure and Function of Photosystems i and ii
journal, June 2006


A common ancestor for oxygenic and anoxygenic photosynthetic systems
journal, July 1998

  • Schubert, Wolf-Dieter; Klukas, Olaf; Saenger, Wolfram
  • Journal of Molecular Biology, Vol. 280, Issue 2
  • DOI: 10.1006/jmbi.1998.1824

Electron transport components of Heliobacterium chlorum investigated by EPR spectroscopy at 9 and 35 GHz
journal, January 1986


Speculations on the Origins and Evolution of Photosynthesis
journal, August 1957


Time-Resolved Fluorescence Measurements of Photosystem II:  The Effect of Quenching by Oxidized Chlorophyll Z
journal, October 1998

  • Schweitzer, Robert H.; Melkozernov, Alexander N.; Blankenship, Robert E.
  • The Journal of Physical Chemistry B, Vol. 102, Issue 42
  • DOI: 10.1021/jp982098y

Sequence of the Core Antenna Domain from the Anoxygenic Phototroph Heliophilum fasciatum: Implications for Diversity of Reaction Center Type I
journal, June 2004

  • Mix, Lucas J.; Harmer, Tara L.; Cavanaugh, Colleen M.
  • Current Microbiology, Vol. 48, Issue 6
  • DOI: 10.1007/s00284-003-4221-3

The Protein Data Bank
journal, January 2000


Tracking molecular evolution of photosynthesis by characterization of a major photosynthesis gene cluster from Heliobacillus mobilis
journal, December 1998

  • Xiong, J.; Inoue, K.; Bauer, C. E.
  • Proceedings of the National Academy of Sciences, Vol. 95, Issue 25
  • DOI: 10.1073/pnas.95.25.14851

A fresh look at the evolution and diversification of photochemical reaction centers
journal, December 2014


Evolution of heliobacteria: Implications for photosynthetic reaction center complexes
journal, July 1994


Electron transfer in the heliobacterial reaction center: evidence against a quinone-type electron acceptor functioning analogous to A1 in photosystem I
journal, March 1998

  • Brettel, Klaus; Leibl, Winfried; Liebl, Ursula
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1363, Issue 3
  • DOI: 10.1016/S0005-2728(98)00010-3

The nature of the photosystem II reaction centre in the chlorophyll d-containing prokaryote, Acaryochloris marina
journal, January 2005

  • Chen, Min; Telfer, Alison; Lin, Su
  • Photochemical & Photobiological Sciences, Vol. 4, Issue 12
  • DOI: 10.1039/b507057k

Small membrane proteins found by comparative genomics and ribosome binding site models
journal, December 2008


Structure of a symmetric photosynthetic reaction center–photosystem
journal, July 2017


An Improved General Amino Acid Replacement Matrix
journal, April 2008


Structure and dynamics of thylakoids in land plants
journal, March 2014

  • Pribil, Mathias; Labs, Mathias; Leister, Dario
  • Journal of Experimental Botany, Vol. 65, Issue 8
  • DOI: 10.1093/jxb/eru090

Identification of 81-hydroxychlorophyll a as a functional reaction center pigment in heliobacteria
journal, July 1991

  • van de Meent, Erik Jan; Kobayashi, Masami; Erkelens, Cornelis
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1058, Issue 3
  • DOI: 10.1016/S0005-2728(05)80131-8

Proton Transfer in Reaction Centers from Photosynthetic Bacteria
journal, June 1992


Twilight zone of protein sequence alignments
journal, February 1999


Protein sequences and redox titrations indicate that the electron acceptors in reaction centers from heliobacteria are similar to Photosystem I
journal, April 1992

  • Trost, Jeffrey T.; Brune, Daniel C.; Blankenship, Robert E.
  • Photosynthesis Research, Vol. 32, Issue 1
  • DOI: 10.1007/BF00028794

Iron–sulfur clusters in type I reaction centers
journal, October 2001

  • Vassiliev, Ilya R.; Antonkine, Mikhail L.; Golbeck, John H.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1507, Issue 1-3
  • DOI: 10.1016/S0005-2728(01)00197-9

Protein Interactions Limit the Rate of Evolution of Photosynthetic Genes in Cyanobacteria
journal, July 2005

  • Shi, Tuo; Bibby, Thomas S.; Jiang, Lin
  • Molecular Biology and Evolution, Vol. 22, Issue 11
  • DOI: 10.1093/molbev/msi216

Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution
journal, June 2001

  • Jordan, Patrick; Fromme, Petra; Witt, Horst Tobias
  • Nature, Vol. 411, Issue 6840
  • DOI: 10.1038/35082000

Electrostatic control of charge separation in bacterial photosynthesis
journal, June 1990

  • Parson, William W.; Chu, Zhen-Tao; Warshel, Arieh
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1017, Issue 3
  • DOI: 10.1016/0005-2728(90)90192-7

Prokaryotic photosynthesis and phototrophy illuminated
journal, November 2006


Menaquinone as the Secondary Electron Acceptor in the Type I Homodimeric Photosynthetic Reaction Center of Heliobacterium modesticaldum
journal, June 2015

  • Kondo, Toru; Itoh, Shigeru; Matsuoka, Masahiro
  • The Journal of Physical Chemistry B, Vol. 119, Issue 27
  • DOI: 10.1021/acs.jpcb.5b03723

Evolution of chlorophyll and bacteriochlorophyll: the problem of invariant sites in sequence analysis.
journal, March 1996

  • Lockhart, P. J.; Larkum, A. W.; Steel, M.
  • Proceedings of the National Academy of Sciences, Vol. 93, Issue 5
  • DOI: 10.1073/pnas.93.5.1930

The iron-quinone electron-acceptor complex of photosystem II
journal, March 1991


Abiotic Methane on Earth: Abiotic Methane on Earth
journal, April 2013

  • Etiope, Giuseppe; Sherwood Lollar, Barbara
  • Reviews of Geophysics, Vol. 51, Issue 2
  • DOI: 10.1002/rog.20011

Temporal and spectral characterization of the photosynthetic reaction center from Heliobacterium modesticaldum
journal, June 2013


Evolution of Oxygenic Photosynthesis
journal, June 2016


Double Reduction of Plastoquinone to Plastoquinol in Photosystem 1
journal, December 2011

  • McConnell, Michael D.; Cowgill, John B.; Baker, Patricia L.
  • Biochemistry, Vol. 50, Issue 51
  • DOI: 10.1021/bi201131r

Controlling Electron Transfer between the Two Cofactor Chains of Photosystem I by the Redox State of One of Their Components
journal, March 2015

  • Santabarbara, Stefano; Bullock, Bradford; Rappaport, Fabrice
  • Biophysical Journal, Vol. 108, Issue 6
  • DOI: 10.1016/j.bpj.2015.01.009

Secondary Electron Transfer Processes in Membranes of Heliobacillus mobilis
journal, October 1995

  • Lin, Su; Chiou, Hung-Cheng; Blankenship, Robert E.
  • Biochemistry, Vol. 34, Issue 39
  • DOI: 10.1021/bi00039a036

Photosynthetic reaction centres: variations on a common structural theme?
journal, January 1991


A unique photosynthetic reaction center from Heliobacterium chlorum
journal, March 1985


Mutation of the Putative Hydrogen-Bond Donor to P 700 of Photosystem I
journal, October 2004

  • Li, Yajing; Lucas, Marie-Gabrielle; Konovalova, Tatyana
  • Biochemistry, Vol. 43, Issue 39
  • DOI: 10.1021/bi036329p

Mechanism of Proton-Coupled Electron Transfer for Quinone (Q B ) Reduction in Reaction Centers of Rb . Sphaeroides
journal, January 1996

  • Graige, M. S.; Paddock, M. L.; Bruce, J. M.
  • Journal of the American Chemical Society, Vol. 118, Issue 38
  • DOI: 10.1021/ja960056m

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
journal, January 1993

  • Warren, Patrick V.; Golbeck, John H.; Warden, Joseph T.
  • Biochemistry, Vol. 32, Issue 3
  • DOI: 10.1021/bi00054a016

On the energetics of the primary electron-transfer process in bacterial reaction centers
journal, August 1994

  • Warshel, A.; Chu, Z. T.; Parson, W. W.
  • Journal of Photochemistry and Photobiology A: Chemistry, Vol. 82, Issue 1-3
  • DOI: 10.1016/1010-6030(94)02010-8

Features and development of Coot
journal, March 2010

  • Emsley, P.; Lohkamp, B.; Scott, W. G.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4
  • DOI: 10.1107/S0907444910007493

A Major Clade of Prokaryotes with Ancient Adaptations to Life on Land
journal, November 2008

  • Battistuzzi, F. U.; Hedges, S. B.
  • Molecular Biology and Evolution, Vol. 26, Issue 2
  • DOI: 10.1093/molbev/msn247

Single core polypeptide in the reaction center of the photosynthetic bacterium Heliobacillus mobilis: structural implications and relations to other photosystems.
journal, August 1993

  • Liebl, U.; Mockensturm-Wilson, M.; Trost, J. T.
  • Proceedings of the National Academy of Sciences, Vol. 90, Issue 15
  • DOI: 10.1073/pnas.90.15.7124

PROMALS3D: a tool for multiple protein sequence and structure alignments
journal, February 2008

  • Pei, Jimin; Kim, Bong-Hyun; Grishin, Nick V.
  • Nucleic Acids Research, Vol. 36, Issue 7
  • DOI: 10.1093/nar/gkn072

An overview on chlorophylls and quinones in the photosystem I-type reaction centers
journal, February 2010

  • Ohashi, Shunsuke; Iemura, Tatsuya; Okada, Naoki
  • Photosynthesis Research, Vol. 104, Issue 2-3
  • DOI: 10.1007/s11120-010-9530-3

Heliobacterium chlorum: cell organization and structure
journal, November 1986

  • Miller, Kenneth R.; Jacob, Jules S.; Smith, Ursula
  • Archives of Microbiology, Vol. 146, Issue 2
  • DOI: 10.1007/BF00402335

Picosecond-photodichroism studies of the transient states in Rhodopseudomonas sphaeroides reaction centers at 5 K. Effects of electron transfer on the six bacteriochlorin pigments
journal, October 1985

  • Kirmaier, Christine; Holten, Dewey; Parson, William W.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 810, Issue 1
  • DOI: 10.1016/0005-2728(85)90205-1

Purification of the photosynthetic reaction center from Heliobacterium modesticaldum
journal, March 2012


Thermodynamic properties of the photochemical reaction center of Heliobacterium chlorum
journal, December 1985

  • Prince, Roger C.; Gest, Howard; Blankenship, Robert E.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 810, Issue 3
  • DOI: 10.1016/0005-2728(85)90224-5

Alternative FeS cluster ligands: tuning redox potentials and chemistry
journal, April 2014


The FX iron–sulfur cluster serves as the terminal bound electron acceptor in heliobacterial reaction centers
journal, February 2012


MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets
journal, March 2016

  • Kumar, Sudhir; Stecher, Glen; Tamura, Koichiro
  • Molecular Biology and Evolution, Vol. 33, Issue 7
  • DOI: 10.1093/molbev/msw054

The reaction center complex from the green sulfur bacterium Chlorobium tepidum: a structural analysis by scanning transmission electron microscopy
journal, April 1999

  • Rémigy, Hervé-W; Stahlberg, Henning; Fotiadis, Dimitrios
  • Journal of Molecular Biology, Vol. 290, Issue 4
  • DOI: 10.1006/jmbi.1999.2925

Evidence for two active branches for electron transfer in photosystem I
journal, March 2001

  • Guergova-Kuras, M.; Boudreaux, B.; Joliot, A.
  • Proceedings of the National Academy of Sciences, Vol. 98, Issue 8
  • DOI: 10.1073/pnas.081078898

Identification of the special pair of photosystem II in a chlorophyll d-dominated cyanobacterium
journal, April 2007

  • Tomo, T.; Okubo, T.; Akimoto, S.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 17
  • DOI: 10.1073/pnas.0701847104

Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega
journal, January 2011

  • Sievers, Fabian; Wilm, Andreas; Dineen, David
  • Molecular Systems Biology, Vol. 7, Issue 1
  • DOI: 10.1038/msb.2011.75

Phylogenetic Analyses of the Core Antenna Domain: Investigatingthe Origin of Photosystem I
journal, February 2005

  • Mix, Lucas J.; Haig, David; Cavanaugh, Colleen M.
  • Journal of Molecular Evolution, Vol. 60, Issue 2
  • DOI: 10.1007/s00239-003-0181-2

Electrostatic Potentials in Rhodopseudomonas viridis Reaction Centers:  Implications for the Driving Force and Directionality of Electron Transfer
journal, January 1996

  • Gunner, M. R.; Nicholls, Anthony; Honig, Barry
  • The Journal of Physical Chemistry, Vol. 100, Issue 10
  • DOI: 10.1021/jp9519070

Type 1 Reaction Center of Photosynthetic Heliobacteria†
journal, January 2007


Photosystem II: The Water-Splitting Enzyme of Photosynthesis
journal, January 2012


Back-reactions, short-circuits, leaks and other energy wasteful reactions in biological electron transfer: Redox tuning to survive life in O 2
journal, January 2012


Conservation of Distantly Related Membrane Proteins: Photosynthetic Reaction Centers Share a Common Structural Core
journal, August 2006

  • Sadekar, Sumedha; Raymond, Jason; Blankenship, Robert E.
  • Molecular Biology and Evolution, Vol. 23, Issue 11
  • DOI: 10.1093/molbev/msl079

Energy transfer, charge separation and pigment arrangement in the reaction center of Photosystem II
journal, March 1994

  • Schelvis, J. P. M.; van Noort, P. I.; Aartsma, T. J.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1184, Issue 2-3
  • DOI: 10.1016/0005-2728(94)90229-1

Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution
journal, February 2001

  • Zouni, Athina; Witt, Horst-Tobias; Kern, Jan
  • Nature, Vol. 409, Issue 6821
  • DOI: 10.1038/35055589

Electron transfer in menaquinone-depleted membranes of Heliobacterium chlorum
journal, April 1993

  • Kleinherenbrink, F. A. M.; Ikegami, I.; Hiraishi, A.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1142, Issue 1-2
  • DOI: 10.1016/0005-2728(93)90085-T

Thinking About the Evolution of Photosynthesis
journal, January 2004


    Works referencing / citing this record:

    Expression and purification of affinity-tagged variants of the photochemical reaction center from Heliobacterium modesticaldum
    journal, September 2019


    Why are photosynthetic reaction centres dimeric?
    journal, January 2019

    • Taylor, Natasha; Kassal, Ivan
    • Chemical Science, Vol. 10, Issue 41
    • DOI: 10.1039/c9sc03712h

    Early Archean origin of Photosystem II
    journal, November 2018

    • Cardona, Tanai; Sánchez-Baracaldo, Patricia; Rutherford, A. William
    • Geobiology, Vol. 17, Issue 2
    • DOI: 10.1111/gbi.12322

    Reduced sulphur sources favour Hg II reduction during anoxygenic photosynthesis by Heliobacteria
    journal, September 2019

    • Lavoie, Noémie C.; Grégoire, Daniel S.; Stenzler, Bejamin R.
    • Geobiology, Vol. 18, Issue 1
    • DOI: 10.1111/gbi.12364

    On the origin of oxygenic photosynthesis and Cyanobacteria
    journal, November 2019

    • Sánchez‐Baracaldo, Patricia; Cardona, Tanai
    • New Phytologist, Vol. 225, Issue 4
    • DOI: 10.1111/nph.16249