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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]
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  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). Chemical Sciences, Geosciences, and 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.
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Kashey, Trevor S., Luu, Dustin D., Cowgill, John C., Baker, Patricia L., & Redding, Kevin E. Light-driven quinone reduction in heliobacterial membranes. United States. https://doi.org/10.1007/s11120-018-0496-x
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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. https://doi.org/10.1007/s11120-018-0496-x. https://www.osti.gov/servlets/purl/1494565.
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@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 = {Mon Mar 12 00:00:00 EDT 2018},
month = {Mon Mar 12 00:00:00 EDT 2018}
}
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Journal Article:
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Publisher's Version of Record
https://doi.org/10.1007/s11120-018-0496-x
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Cited by: 18 works
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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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Works referenced in this record:

Pigment-protein interactions in the photosynthetic reaction centre from Rhodopseudomonas viridis
journal, October 1986

Recruitment of a Foreign Quinone into the A 1 Site of Photosystem I
journal, July 2001

  • Johnson, T. Wade; Zybailov, Boris; Jones, A. Daniel
  • Journal of Biological Chemistry, Vol. 276, Issue 43
  • DOI: 10.1074/jbc.M104040200

Identification of F X in the Heliobacterial Reaction Center as a [4Fe-4S] Cluster with an S = 3 / 2 Ground Spin State †
journal, May 2006

  • Heinnickel, Mark; Agalarov, Rufat; Svensen, Nina
  • Biochemistry, Vol. 45, Issue 21
  • DOI: 10.1021/bi060031s

Modulation of the fluorescence yield in heliobacterial cells by induction of charge recombination in the photosynthetic reaction center
journal, December 2013

  • Redding, Kevin E.; Sarrou, Iosifina; Rappaport, Fabrice
  • Photosynthesis Research, Vol. 120, Issue 1-2
  • DOI: 10.1007/s11120-013-9957-4

Alteration of the H-Bond to the A 1A Phylloquinone in Photosystem I: Influence on the Kinetics and Energetics of Electron Transfer
journal, March 2011

  • Srinivasan, Nithya; Santabarbara, Stefano; Rappaport, Fabrice
  • The Journal of Physical Chemistry B, Vol. 115, Issue 8
  • DOI: 10.1021/jp109531b

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

Role of the Hydrogen Bond from Leu722 to the A 1A Phylloquinone in Photosystem I † ‡
journal, April 2009

  • Srinivasan, Nithya; Karyagina, Irina; Bittl, Robert
  • Biochemistry, Vol. 48, Issue 15
  • DOI: 10.1021/bi802340s

On the role of the Q B protein of PS II in photoinhibition
journal, January 1986

Heliobacterium modesticaldum, sp. nov., a thermophilic heliobacterium of hot springs and volcanic soils
journal, April 1995

  • Kimble, Linda K.; Mandelco, Linda; Woese, Carl R.
  • Archives of Microbiology, Vol. 163, Issue 4
  • DOI: 10.1007/BF00393378

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

Recruitment of a Foreign Quinone into the A 1 Site of Photosystem I : I. GENETIC AND PHYSIOLOGICAL CHARACTERIZATION OF PHYLLOQUINONE BIOSYNTHETIC PATHWAY MUTANTS IN
journal, March 2000

  • Johnson, T. Wade; Shen, Gaozhong; Zybailov, Boris
  • Journal of Biological Chemistry, Vol. 275, Issue 12
  • DOI: 10.1074/jbc.275.12.8523

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

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

Modulation of fluorescence in Heliobacterium modesticaldum cells
journal, May 2010

  • Collins, Aaron M.; Redding, Kevin E.; Blankenship, Robert E.
  • Photosynthesis Research, Vol. 104, Issue 2-3
  • DOI: 10.1007/s11120-010-9554-8

Identification and characterization of PshBII, a second FA/FB-containing polypeptide in the photosynthetic reaction center of Heliobacterium modesticaldum
journal, May 2010

  • Romberger, Steven P.; Castro, Christian; Sun, Yili
  • Photosynthesis Research, Vol. 104, Issue 2-3
  • DOI: 10.1007/s11120-010-9558-4

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

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

Expression and characterization of cytochrome c 553 from Heliobacterium modesticaldum
journal, February 2014

  • Kashey, Trevor S.; Cowgill, John B.; McConnell, Michael D.
  • Photosynthesis Research, Vol. 120, Issue 3
  • DOI: 10.1007/s11120-014-9982-y

Quinone exchange at the A1 site in Photosystem I in spinach and cyanobacteria
journal, June 1997

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

Occurrence of menaquinone as the sole isoprenoid quinone in the photosynthetic bacterium Heliobacterium chlorum
journal, March 1989

Insights into heliobacterial photosynthesis and physiology from the genome of Heliobacterium modesticaldum
journal, February 2010

Electron donation from membrane-bound cytochrome c to the photosynthetic reaction center in whole cells and isolated membranes of Heliobacterium gestii
journal, February 2002

  • Oh-oka, Hirozo; Iwaki, Masayo; Itoh, Shigeru
  • Photosynthesis Research, Vol. 71, Issue 1/2, p. 137-147
  • DOI: 10.1023/A:1014911832504

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

Loss of Phylloquinone in Chlamydomonas Affects Plastoquinone Pool Size and Photosystem II Synthesis
journal, March 2007

  • Lefebvre-Legendre, Linnka; Rappaport, Fabrice; Finazzi, Giovanni
  • Journal of Biological Chemistry, Vol. 282, Issue 18
  • DOI: 10.1074/jbc.M610249200

On the Role of Quinones in Bacterial Electron Transport. The Respiratory System of Bacillus megaterium
journal, December 1969

Protein–cofactor interactions in bioenergetic complexes: The role of the A1A and A1B phylloquinones in Photosystem I
journal, September 2009

  • Srinivasan, Nithya; Golbeck, John H.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1787, Issue 9
  • DOI: 10.1016/j.bbabio.2009.04.010

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

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

Nanosecond electron transfer kinetics in photosystem I following substitution of quinones for vitamin K 1 as studied by time resolved EPR
journal, June 1991

ENDOR and Special TRIPLE Resonance Spectroscopy of Photoaccumulated Semiquinone Electron Acceptors in the Reaction Centers of Green Sulfur Bacteria and Heliobacteria †
journal, June 1999

  • Muhiuddin, Irine P.; Rigby, Stephen E. J.; Evans, Michael C. W.
  • Biochemistry, Vol. 38, Issue 22
  • DOI: 10.1021/bi982042u

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

The bound iron–sulfur clusters of Type-I homodimeric reaction centers
journal, April 2010

Contribution of vitamin K1 to the electron spin polarization in spinach photosystem I
journal, September 1990

  • Rustandi, Richard R.; Snyder, Seth W.; Feezel, Laura L.
  • Biochemistry, Vol. 29, Issue 35
  • DOI: 10.1021/bi00487a006

Heliobacterium modesticaldum, sp. nov., a thermophilic heliobacterium of hot springs and volcanic soils
journal, April 1995

  • Kimble, Linda K.; Mandelco, Linda; Woese, Carl R.
  • Archives of Microbiology, Vol. 163, Issue 4
  • DOI: 10.1007/s002030050202
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    Works referencing / citing this record:

    Evolution of photosynthetic reaction centers: insights from the structure of the heliobacterial reaction center
    journal, March 2018

    • Orf, Gregory S.; Gisriel, Christopher; Redding, Kevin E.
    • Photosynthesis Research, Vol. 138, Issue 1
    • DOI: 10.1007/s11120-018-0503-2

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

    Reconstitution of the heliobacterial photochemical reaction center and cytochrome c553 into a proteoliposome system
    journal, December 2019

    A Molecular Biology Tool Kit for the Phototrophic Firmicute Heliobacterium modesticaldum
    journal, August 2019

    • Baker, Patricia L.; Orf, Gregory S.; Khan, Zahid
    • Applied and Environmental Microbiology, Vol. 85, Issue 19
    • DOI: 10.1128/aem.01287-19

    Using the Endogenous CRISPR-Cas System of Heliobacterium modesticaldum To Delete the Photochemical Reaction Center Core Subunit Gene
    journal, September 2019

    • Baker, Patricia L.; Orf, Gregory S.; Kevershan, Kimberly
    • Applied and Environmental Microbiology, Vol. 85, Issue 23
    • DOI: 10.1128/aem.01644-19
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