Evolution of photosynthetic reaction centers: insights from the structure of the heliobacterial reaction center View Full Text


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Article Info

DATE

2018-03-30

AUTHORS

Gregory S. Orf, Christopher Gisriel, Kevin E. Redding

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. More... »

PAGES

11-37

References to SciGraph publications

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  • 2018-03-12. Light-driven quinone reduction in heliobacterial membranes in PHOTOSYNTHESIS RESEARCH
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  • 2002-11. 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 in PHOTOSYNTHESIS RESEARCH
  • 1992-04. Protein sequences and redox titrations indicate that the electron acceptors in reaction centers from heliobacteria are similar to Photosystem I in PHOTOSYNTHESIS RESEARCH
  • 2005-02. Phylogenetic Analyses of the Core Antenna Domain: Investigatingthe Origin of Photosystem I in JOURNAL OF MOLECULAR EVOLUTION
  • 2010-02-18. An overview on chlorophylls and quinones in the photosystem I-type reaction centers in PHOTOSYNTHESIS RESEARCH
  • 1986-09. Abiotic photosynthesis from ferrous carbonate (siderite) and water in ORIGINS OF LIFE AND EVOLUTION OF BIOSPHERES
  • 2005. Thinking about the evolution of photosynthesis in DISCOVERIES IN PHOTOSYNTHESIS
  • 2001-02. Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution in NATURE
  • 2013-06-30. Temporal and spectral characterization of the photosynthetic reaction center from Heliobacterium modesticaldum in PHOTOSYNTHESIS RESEARCH
  • 2005-11-07. The nature of the photosystem II reaction centre in the chlorophyll d-containing prokaryote, Acaryochloris marina in PHOTOCHEMICAL & PHOTOBIOLOGICAL SCIENCES
  • 1994-07. Evolution of heliobacteria: Implications for photosynthetic reaction center complexes in PHOTOSYNTHESIS RESEARCH
  • Identifiers

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    http://scigraph.springernature.com/pub.10.1007/s11120-018-0503-2

    DOI

    http://dx.doi.org/10.1007/s11120-018-0503-2

    DIMENSIONS

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    PUBMED

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