Search Menu
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information
Search Scholarly Publications

Title: Light-Driven Na + Pump from Gillisia limnaea : A High-Affinity Na + Binding Site Is Formed Transiently in the Photocycle

Abstract

A group of microbial retinal proteins most closely related to the proton pump xanthorhodopsin has a novel sequence motif and a novel function. Instead of, or in addition to, proton transport, they perform light-driven sodium ion transport, as reported for one representative of this group (KR2) from Krokinobacter. In this paper, we examine a similar protein, GLR from Gillisia limnaea, expressed in Escherichia coli, which shares some properties with KR2 but transports only Na+. The absorption spectrum of GLR is insensitive to Na+ at concentrations of ≤3 M. However, very low concentrations of Na+ cause profound differences in the decay and rise time of photocycle intermediates, consistent with a switch from a “Na+-independent” to a “Na+-dependent” photocycle (or photocycle branch) at ~60 μM Na+. The rates of photocycle steps in the latter, but not the former, are linearly dependent on Na+ concentration. This suggests that a high-affinity Na+ binding site is created transiently after photoexcitation, and entry of Na+ from the bulk to this site redirects the course of events in the remainder of the cycle. A greater concentration of Na+ is needed for switching the reaction path at lower pH. The data suggest therefore competition between H+ and Na+more » to determine the two alternative pathways. The idea that a Na+ binding site can be created at the Schiff base counterion is supported by the finding that upon perturbation of this region in the D251E mutant, Na+ binds without photoexcitation. Furthermore, binding of Na+ to the mutant shifts the chromophore maximum to the red like that of H+, which occurs in the photocycle of the wild type.« less

Authors:
 [1];  [1];  [1];  [1];  [2];  [1]
+ Show Author Affiliations
  1. Department of Physiology and Biophysics, University of California, Irvine, California 92697, United States
  2. Department of Life Science and Interdisciplinary Program of Integrated Biotechnology, Sogang University, Shinsu-Dong 1, Mapo-Gu, Seoul 121-742, Korea
Publication Date:
Research Org.:
Univ. of California, Irvine, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1165228
Alternate Identifier(s):
OSTI ID: 1345588
Grant/Contract Number:  
DEFG03-86ER13525; FG03-86ER13525
Resource Type:
Published Article
Journal Name:
Biochemistry
Additional Journal Information:
Journal Name: Biochemistry Journal Volume: 53 Journal Issue: 48; Journal ID: ISSN 0006-2960
Publisher:
American Chemical Society
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES

Citation Formats

Balashov, Sergei P., Imasheva, Eleonora S., Dioumaev, Andrei K., Wang, Jennifer M., Jung, Kwang-Hwan, and Lanyi, Janos K. Light-Driven Na + Pump from Gillisia limnaea : A High-Affinity Na + Binding Site Is Formed Transiently in the Photocycle. United States: N. p., 2014. Web. doi:10.1021/bi501064n.
Copy to clipboard
Balashov, Sergei P., Imasheva, Eleonora S., Dioumaev, Andrei K., Wang, Jennifer M., Jung, Kwang-Hwan, & Lanyi, Janos K. Light-Driven Na + Pump from Gillisia limnaea : A High-Affinity Na + Binding Site Is Formed Transiently in the Photocycle. United States. https://doi.org/10.1021/bi501064n
Copy to clipboard
Balashov, Sergei P., Imasheva, Eleonora S., Dioumaev, Andrei K., Wang, Jennifer M., Jung, Kwang-Hwan, and Lanyi, Janos K. Mon . "Light-Driven Na + Pump from Gillisia limnaea : A High-Affinity Na + Binding Site Is Formed Transiently in the Photocycle". United States. https://doi.org/10.1021/bi501064n.
Copy to clipboard
@article{osti_1165228,
title = {Light-Driven Na + Pump from Gillisia limnaea : A High-Affinity Na + Binding Site Is Formed Transiently in the Photocycle},
author = {Balashov, Sergei P. and Imasheva, Eleonora S. and Dioumaev, Andrei K. and Wang, Jennifer M. and Jung, Kwang-Hwan and Lanyi, Janos K.},
abstractNote = {A group of microbial retinal proteins most closely related to the proton pump xanthorhodopsin has a novel sequence motif and a novel function. Instead of, or in addition to, proton transport, they perform light-driven sodium ion transport, as reported for one representative of this group (KR2) from Krokinobacter. In this paper, we examine a similar protein, GLR from Gillisia limnaea, expressed in Escherichia coli, which shares some properties with KR2 but transports only Na+. The absorption spectrum of GLR is insensitive to Na+ at concentrations of ≤3 M. However, very low concentrations of Na+ cause profound differences in the decay and rise time of photocycle intermediates, consistent with a switch from a “Na+-independent” to a “Na+-dependent” photocycle (or photocycle branch) at ~60 μM Na+. The rates of photocycle steps in the latter, but not the former, are linearly dependent on Na+ concentration. This suggests that a high-affinity Na+ binding site is created transiently after photoexcitation, and entry of Na+ from the bulk to this site redirects the course of events in the remainder of the cycle. A greater concentration of Na+ is needed for switching the reaction path at lower pH. The data suggest therefore competition between H+ and Na+ to determine the two alternative pathways. The idea that a Na+ binding site can be created at the Schiff base counterion is supported by the finding that upon perturbation of this region in the D251E mutant, Na+ binds without photoexcitation. Furthermore, binding of Na+ to the mutant shifts the chromophore maximum to the red like that of H+, which occurs in the photocycle of the wild type.},
doi = {10.1021/bi501064n},
journal = {Biochemistry},
number = 48,
volume = 53,
place = {United States},
year = {Mon Nov 24 00:00:00 EST 2014},
month = {Mon Nov 24 00:00:00 EST 2014}
}
Copy to clipboard
Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1021/bi501064n
Copyright Statement
Other availability
Search WorldCat Search WorldCat to find libraries that may hold this journal
Citation Metrics:
Cited by: 65 works
Citation information provided by
Web of Science

Figures / Tables:

Figure 1 Figure 1: Light-induced pH changes in a suspension of E. coli cells with G. limnaea rhodopsin expressed and reconstituted with all-trans-retinal: trace 1, absence of pH change in sodium free medium [in 100 mM KCl (pH 7.5)]; trace 2, proton uptake (alkalinization) in 100 mM NaCl; trace 3, same asmore » trace 2 but after addition of a protonophore (50 μM CCCP), which increases the rate and extent of passive proton influx.« less
All figures and tables (10 total)
Save / Share:
Export Metadata
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.

Works referenced in this record:

Structure of the Rotor Ring of F-Type Na+-ATPase from Ilyobacter tartaricus
journal, April 2005

Evaluation of intrinsic chemical kinetics and transient product spectra from time-resolved spectroscopic data
journal, September 1997

Bacteriorhodopsin photocycle at cryogenic temperatures reveals distributed barriers of conformational substates
journal, May 2007

  • Dioumaev, A. K.; Lanyi, J. K.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 23
  • DOI: 10.1073/pnas.0703859104

Protonation reactions and their coupling in bacteriorhodopsin
journal, August 2000

Structure of bacteriorhodopsin at 1.55 Å resolution
journal, August 1999

  • Luecke, Hartmut; Schobert, Brigitte; Richter, Hans-Thomas
  • Journal of Molecular Biology, Vol. 291, Issue 4
  • DOI: 10.1006/jmbi.1999.3027

Switch from Conventional to Distributed Kinetics in the Bacteriorhodopsin Photocycle
journal, September 2008

  • Dioumaev, Andrei K.; Lanyi, Janos K.
  • Biochemistry, Vol. 47, Issue 42
  • DOI: 10.1021/bi801247e

Bacterial Rhodopsin: Evidence for a New Type of Phototrophy in the Sea
journal, September 2000

Halorhodopsin, a light-driven electrogenic chloride-transport system
journal, April 1990

Proton Transfers in the Photochemical Reaction Cycle of Proteorhodopsin †
journal, April 2002

  • Dioumaev, Andrei K.; Brown, Leonid S.; Shih, Jennifer
  • Biochemistry, Vol. 41, Issue 17
  • DOI: 10.1021/bi025563x

Aspartic acid-96 is the internal proton donor in the reprotonation of the Schiff base of bacteriorhodopsin.
journal, December 1989

  • Otto, H.; Marti, T.; Holz, M.
  • Proceedings of the National Academy of Sciences, Vol. 86, Issue 23
  • DOI: 10.1073/pnas.86.23.9228

From Femtoseconds to Biology: Mechanism of Bacteriorhodopsin's Light-Driven Proton Pump
journal, June 1991

Proton transfer via a transient linear water-molecule chain in a membrane protein
journal, June 2011

  • Freier, E.; Wolf, S.; Gerwert, K.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 28
  • DOI: 10.1073/pnas.1104735108

Channelrhodopsin unchained: Structure and mechanism of a light-gated cation channel
journal, May 2014

  • Lórenz-Fonfría, Víctor A.; Heberle, Joachim
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 5
  • DOI: 10.1016/j.bbabio.2013.10.014

Application of FTIR Spectroscopy to the Structural Study on the Function of Bacteriorhodopsin
journal, January 1995

Proton binding within a membrane protein by a protonated water cluster
journal, February 2005

  • Garczarek, F.; Brown, L. S.; Lanyi, J. K.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 10
  • DOI: 10.1073/pnas.0500421102

Reversible steps in the bacteriorhodopsin photocycle.
journal, April 1992

  • Lozier, R. H.; Xie, A.; Hofrichter, J.
  • Proceedings of the National Academy of Sciences, Vol. 89, Issue 8
  • DOI: 10.1073/pnas.89.8.3610

Fourier Transform Infrared Spectra of a Late Intermediate of the Bacteriorhodopsin Photocycle Suggest Transient Protonation of Asp-212
journal, July 1999

  • Dioumaev, Andrei K.; Brown, Leonid S.; Needleman, Richard
  • Biochemistry, Vol. 38, Issue 31
  • DOI: 10.1021/bi990873+

The role of protein-bound water molecules in microbial rhodopsins
journal, May 2014

  • Gerwert, Klaus; Freier, Erik; Wolf, Steffen
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 5
  • DOI: 10.1016/j.bbabio.2013.09.006

Electron-crystallographic Refinement of the Structure of Bacteriorhodopsin
journal, June 1996

  • Grigorieff, N.; Ceska, T. A.; Downing, K. H.
  • Journal of Molecular Biology, Vol. 259, Issue 3
  • DOI: 10.1006/jmbi.1996.0328

Light isomerizes the chromophore of bacteriorhodopsin
journal, September 1980

  • Tsuda, Motoyuki; Glaccum, Moira; Nelson, Burr
  • Nature, Vol. 287, Issue 5780
  • DOI: 10.1038/287351a0

Proton transfers in the bacteriorhodopsin photocycle
journal, August 2006

Genomic Makeup of the Marine Flavobacterium Nonlabens (Donghaeana) dokdonensis and Identification of a Novel Class of Rhodopsins
journal, January 2013

  • Kwon, Soon-Kyeong; Kim, Byung Kwon; Song, Ju Yeon
  • Genome Biology and Evolution, Vol. 5, Issue 1
  • DOI: 10.1093/gbe/evs134

Genome sequence of the Antarctic rhodopsins-containing flavobacterium Gillisia limnaea type strain (R-8282T)
journal, October 2012

  • Riedel, Thomas; Held, Brittany; Nolan, Matt
  • Standards in Genomic Sciences, Vol. 7, Issue 1
  • DOI: 10.4056/sigs.3216895

The mechanism of rotating proton pumping ATPases
journal, August 2010

  • Nakanishi-Matsui, Mayumi; Sekiya, Mizuki; Nakamoto, Robert K.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1797, Issue 8
  • DOI: 10.1016/j.bbabio.2010.02.014

The infrared absorption of amino acid side chains
journal, January 2000

Infrared Methods for Monitoring the Protonation State of Carboxylic Amino Acids in the Photocycle of Bacteriorhodopsin
journal, January 2001

Protonation state of Asp (Glu)-85 regulates the purple-to-blue transition in bacteriorhodopsin mutants Arg-82----Ala and Asp-85----Glu: the blue form is inactive in proton translocation.
journal, February 1990

  • Subramaniam, S.; Marti, T.; Khorana, H. G.
  • Proceedings of the National Academy of Sciences, Vol. 87, Issue 3
  • DOI: 10.1073/pnas.87.3.1013

Crystallographic Structure of the K Intermediate of Bacteriorhodopsin: Conservation of Free Energy after Photoisomerization of the Retinal
journal, August 2002

Light-induced changes of the pH gradient and the membrane potential in H. halobium
journal, June 1976

Structure and Function of Halorhodopsin
journal, January 1995

The structural basis of the functioning of bacteriorhodopsin: An overview
journal, April 1979

Breaking the Carboxyl Rule
journal, July 2013

  • Balashov, Sergei P.; Petrovskaya, Lada E.; Imasheva, Eleonora S.
  • Journal of Biological Chemistry, Vol. 288, Issue 29
  • DOI: 10.1074/jbc.M113.465138

CLOSING IN ON BACTERIORHODOPSIN: Progress in Understanding the Molecule
journal, June 1999

  • Haupts, Ulrich; Tittor, Jörg; Oesterhelt, Dieter
  • Annual Review of Biophysics and Biomolecular Structure, Vol. 28, Issue 1
  • DOI: 10.1146/annurev.biophys.28.1.367

Amino acid sequence of bacteriorhodopsin.
journal, October 1979

  • Khorana, H. G.; Gerber, G. E.; Herlihy, W. C.
  • Proceedings of the National Academy of Sciences, Vol. 76, Issue 10
  • DOI: 10.1073/pnas.76.10.5046

Nature's toolkit for microbial rhodopsin ion pumps
journal, April 2014

  • Beja, O.; Lanyi, J. K.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 18
  • DOI: 10.1073/pnas.1405093111

FTIR Spectroscopy of a Light-Driven Compatible Sodium Ion-Proton Pumping Rhodopsin at 77 K
journal, April 2014

  • Ono, Hikaru; Inoue, Keiichi; Abe-Yoshizumi, Rei
  • The Journal of Physical Chemistry B, Vol. 118, Issue 18
  • DOI: 10.1021/jp500756f

A light-driven sodium ion pump in marine bacteria
journal, April 2013

  • Inoue, Keiichi; Ono, Hikaru; Abe-Yoshizumi, Rei
  • Nature Communications, Vol. 4, Issue 1
  • DOI: 10.1038/ncomms2689

Proton/sodium pumping pyrophosphatases: the last of the primary ion pumps
journal, August 2014

Environmental Genome Shotgun Sequencing of the Sargasso Sea
journal, April 2004

Infrared Difference Spectra of the Intermediates L, M, N, and O of the Bacteriorhodopsin Photoreaction Obtained by Time-Resolved Attenuated Total Reflection Spectroscopy
journal, December 1997

  • Zscherp, Christian; Heberle, Joachim
  • The Journal of Physical Chemistry B, Vol. 101, Issue 49
  • DOI: 10.1021/jp971047i

Aspartate–Histidine Interaction in the Retinal Schiff Base Counterion of the Light-Driven Proton Pump of Exiguobacterium sibiricum
journal, July 2012

  • Balashov, S. P.; Petrovskaya, L. E.; Lukashev, E. P.
  • Biochemistry, Vol. 51, Issue 29
  • DOI: 10.1021/bi300409m

Pathways of proton release in the bacteriorhodopsin photocycle
journal, September 1992

  • Zimanyi, Laszlo; Varo, Gyorgy; Chang, Man
  • Biochemistry, Vol. 31, Issue 36
  • DOI: 10.1021/bi00151a022

PURPLE MEMBRANE: SURFACE CHARGE DENSITY and THE MULTIPLE EFFECT OF pH and CATIONS
journal, December 1990

Two light-transducing membrane proteins: bacteriorhodopsin and the mammalian rhodopsin.
journal, February 1993

  • Khorana, H. G.
  • Proceedings of the National Academy of Sciences, Vol. 90, Issue 4
  • DOI: 10.1073/pnas.90.4.1166

Bacteriorhodopsin-like proteins of eubacteria and fungi: the extent of conservation of the haloarchaeal proton-pumping mechanism
journal, January 2006

  • Brown, Leonid S.; Jung, Kwang-Hwan
  • Photochemical & Photobiological Sciences, Vol. 5, Issue 6
  • DOI: 10.1039/b514537f

Functions of a New Photoreceptor Membrane
journal, October 1973

  • Oesterhelt, D.; Stoeckenius, W.
  • Proceedings of the National Academy of Sciences, Vol. 70, Issue 10
  • DOI: 10.1073/pnas.70.10.2853

Role of Na + and K + in Enzyme Function
journal, October 2006

Halorhodopsin is a light-driven chloride pump.
journal, September 1982

Eubacterial rhodopsins — Unique photosensors and diverse ion pumps
journal, May 2014

Bacteriorhodopsin D85N: Three spectroscopic species in equilibrium
journal, February 1993

  • Turner, George J.; Miercke, Larry J. W.; Thorgeirsson, Thorgeir E.
  • Biochemistry, Vol. 32, Issue 5
  • DOI: 10.1021/bi00056a019

A model-independent approach to assigning bacteriorhodopsin's intramolecular reactions to photocycle intermediates
journal, November 1993

Ion channels versus ion pumps: the principal difference, in principle
journal, April 2009

  • Gadsby, David C.
  • Nature Reviews Molecular Cell Biology, Vol. 10, Issue 5
  • DOI: 10.1038/nrm2668

Predicted bacteriorhodopsin from Exiguobacterium sibiricum is a functional proton pump
journal, September 2010

Xanthorhodopsin: A Proton Pump with a Light-Harvesting Carotenoid Antenna
journal, September 2005

Crystal Structure of Na + , K + -ATPase in the Na + -Bound State
journal, September 2013

A Vibrational Spectral Maker for Probing the Hydrogen-Bonding Status of Protonated Asp and Glu Residues
journal, April 2005

    Sort by:
    [ × clear filter / sort ]

    Figures / Tables found in this record:

    Figure 1 (p. 3)figure
    Figure 2 (p. 3)figure
    Figure 3 (p. 4)figure
    Figure 4 (p. 5)figure
    Figure 5 (p. 6)figure
    Figure 6 (p. 6)figure
    Figure 7 (p. 7)figure
    Figure 8 (p. 7)figure
    Figure 9 (p. 8)figure
    Figure 10 (p. 10)figure
      [ × clear filter / sort ]
      Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.

      Similar Records in DOE PAGES and OSTI.GOV collections: