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Title: Light-driven quinone reduction in heliobacterial membranes

Abstract

We report that photosynthetic reaction centers (RCs) evolved > 3 billion years ago and have diverged into Type II RCs reducing quinones and Type I RCs reducing soluble acceptors via iron–sulfur clusters. Photosystem I (PSI), the exemplar Type I RC, uses modi- fied menaquinones as intermediate electron transfer cofactors, but it has been controversial if the Type I RC of heliobacteria (HbRC) uses its two bound menaquinones in the same way. The sequence of the quinone-binding site in PSI is not conserved in the HbRC, and the recently solved crystal structure of the HbRC does not reveal a quinone in the analogous site. We found that illumination of heliobacterial membranes resulted in reduction of menaquinone to menaquinol, suggesting that the HbRC can perform a function thought restricted to Type II RCs. Experiments on membranes and live cells are consistent with the hypothesis that the HbRC preferentially reduces soluble electron acceptors (e.g., ferredoxins) in low light, but switches to reducing lipophilic quinones in high light, when the soluble acceptor pool becomes full. Therefore, the HbRC may represent a functional evolutionary intermediate between PSI and the Type II RCs.

Authors:
 [1];  [1];  [2];  [1]; ORCiD logo [1]
  1. Arizona State Univ., Tempe, AZ (United States)
  2. Arizona State Univ., Tempe, AZ (United States); Univ. of Wisconsin, Madison, WI (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:
1494565
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; Heliobacteria; Reaction centers; Quinone; Type I reaction center; Type II reaction center

Citation Formats

Kashey, Trevor S., Luu, Dustin D., Cowgill, John C., Baker, Patricia L., and Redding, Kevin E. Light-driven quinone reduction in heliobacterial membranes. United States: N. p., 2018. Web. doi:10.1007/s11120-018-0496-x.
Kashey, Trevor S., Luu, Dustin D., Cowgill, John C., Baker, Patricia L., & Redding, Kevin E. Light-driven quinone reduction in heliobacterial membranes. United States. doi:10.1007/s11120-018-0496-x.
Kashey, Trevor S., Luu, Dustin D., Cowgill, John C., Baker, Patricia L., and Redding, Kevin E. Mon . "Light-driven quinone reduction in heliobacterial membranes". United States. doi:10.1007/s11120-018-0496-x. https://www.osti.gov/servlets/purl/1494565.
@article{osti_1494565,
title = {Light-driven quinone reduction in heliobacterial membranes},
author = {Kashey, Trevor S. and Luu, Dustin D. and Cowgill, John C. and Baker, Patricia L. and Redding, Kevin E.},
abstractNote = {We report that photosynthetic reaction centers (RCs) evolved > 3 billion years ago and have diverged into Type II RCs reducing quinones and Type I RCs reducing soluble acceptors via iron–sulfur clusters. Photosystem I (PSI), the exemplar Type I RC, uses modi- fied menaquinones as intermediate electron transfer cofactors, but it has been controversial if the Type I RC of heliobacteria (HbRC) uses its two bound menaquinones in the same way. The sequence of the quinone-binding site in PSI is not conserved in the HbRC, and the recently solved crystal structure of the HbRC does not reveal a quinone in the analogous site. We found that illumination of heliobacterial membranes resulted in reduction of menaquinone to menaquinol, suggesting that the HbRC can perform a function thought restricted to Type II RCs. Experiments on membranes and live cells are consistent with the hypothesis that the HbRC preferentially reduces soluble electron acceptors (e.g., ferredoxins) in low light, but switches to reducing lipophilic quinones in high light, when the soluble acceptor pool becomes full. Therefore, the HbRC may represent a functional evolutionary intermediate between PSI and the Type II RCs.},
doi = {10.1007/s11120-018-0496-x},
journal = {Photosynthesis Research},
number = 1,
volume = 138,
place = {United States},
year = {2018},
month = {3}
}

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Figures / Tables:

Figure 1 Figure 1: Schematic of ET cofactors in the HbRC. P800, a pair of BChl g, is the primary electron donor and the FX iron-sulfur cluster is the terminal electron acceptor. The A0 cofactor (81-HO-Chl $a$) serves as an electron transfer intermediate during the process. Unlike PSI, there is no tightly-boundmore » quinone in the HbRC structure. However, to one side of A0 there is an unassigned electron density that appears to have an isoprenyl tail. A menaquinone molecule was fit to this density to visualize where it might bind.« less

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