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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 Q A 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 O 2 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

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