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 »
- Authors:
-
- Department of Physiology and Biophysics, University of California, Irvine, California 92697, United States
- 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.
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
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.
@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}
}
https://doi.org/10.1021/bi501064n
Web of Science
Figures / Tables:
Works referenced in this record:
Structure of the Rotor Ring of F-Type Na+-ATPase from Ilyobacter tartaricus
journal, April 2005
- Meier, T.
- Science, Vol. 308, Issue 5722
Evaluation of intrinsic chemical kinetics and transient product spectra from time-resolved spectroscopic data
journal, September 1997
- Dioumaev, Andrei K.
- Biophysical Chemistry, Vol. 67, Issue 1-3
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
Protonation reactions and their coupling in bacteriorhodopsin
journal, August 2000
- Balashov, Sergei P.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1460, Issue 1
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
Correlation between the Hydrogen-Bond Structures and the C═O Stretching Frequencies of Carboxylic Acids as Studied by Density Functional Theory Calculations: Theoretical Basis for Interpretation of Infrared Bands of Carboxylic Groups in Proteins
journal, May 2008
- Takei, Ken-ichi; Takahashi, Ryouta; Noguchi, Takumi
- The Journal of Physical Chemistry B, Vol. 112, Issue 21
Switch from Conventional to Distributed Kinetics in the Bacteriorhodopsin Photocycle
journal, September 2008
- Dioumaev, Andrei K.; Lanyi, Janos K.
- Biochemistry, Vol. 47, Issue 42
Bacterial Rhodopsin: Evidence for a New Type of Phototrophy in the Sea
journal, September 2000
- Beja, O.; Aravind, L.; Koonin, Eugene V.
- Science, Vol. 289, Issue 5486, p. 1902-1906
Halorhodopsin, a light-driven electrogenic chloride-transport system
journal, April 1990
- Lanyi, J. K.
- Physiological Reviews, Vol. 70, Issue 2
Complete Genome Sequences of Krokinobactersp. Strain 4H-3-7-5 and Lacinutrixsp. Strain 5H-3-7-4, Polysaccharide-Degrading Members of the Family Flavobacteriaceae
journal, July 2011
- Klippel, B.; Lochner, A.; Bruce, D. C.
- Journal of Bacteriology, Vol. 193, Issue 17
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
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
From Femtoseconds to Biology: Mechanism of Bacteriorhodopsin's Light-Driven Proton Pump
journal, June 1991
- Mathies, R. A.; Lin, S. W.; Ames, J. B.
- Annual Review of Biophysics and Biophysical Chemistry, Vol. 20, Issue 1
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
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
Application of FTIR Spectroscopy to the Structural Study on the Function of Bacteriorhodopsin
journal, January 1995
- Maeda, Akio
- Israel Journal of Chemistry, Vol. 35, Issue 3-4
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
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
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
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
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
Light isomerizes the chromophore of bacteriorhodopsin
journal, September 1980
- Tsuda, Motoyuki; Glaccum, Moira; Nelson, Burr
- Nature, Vol. 287, Issue 5780
Proton transfers in the bacteriorhodopsin photocycle
journal, August 2006
- Lanyi, Janos K.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1757, Issue 8
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
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
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
The infrared absorption of amino acid side chains
journal, January 2000
- Barth, Andreas
- Progress in Biophysics and Molecular Biology, Vol. 74, Issue 3-5
Infrared Methods for Monitoring the Protonation State of Carboxylic Amino Acids in the Photocycle of Bacteriorhodopsin
journal, January 2001
- Dioumaev, A. K.
- Biochemistry (Moscow), Vol. 66, Issue 11, p. 1269-1276
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
Crystallographic Structure of the K Intermediate of Bacteriorhodopsin: Conservation of Free Energy after Photoisomerization of the Retinal
journal, August 2002
- Schobert, Brigitte; Cupp-Vickery, Jill; Hornak, Viktor
- Journal of Molecular Biology, Vol. 321, Issue 4
Complete Identification of C:O Stretching Vibrational Bands of Protonated Aspartic Acid Residues in the Difference Infrared Spectra of M and N Intermediates versus Bacteriorhodopsin
journal, March 1994
- Sasaki, Jun; Lanyi, Janos K.; Needleman, Richard
- Biochemistry, Vol. 33, Issue 11
Light-induced changes of the pH gradient and the membrane potential in H. halobium
journal, June 1976
- Michel, H.; Oesterhelt, D.
- FEBS Letters, Vol. 65, Issue 2
Structure and Function of Halorhodopsin
journal, January 1995
- Oesterhelt, Dieter
- Israel Journal of Chemistry, Vol. 35, Issue 3-4
The role of back-reactions and proton uptake during the N .fwdarw. O transition in bacteriorhodopsin's photocycle: a kinetic resonance Raman study
journal, August 1990
- Ames, James B.; Mathies, Richard A.
- Biochemistry, Vol. 29, Issue 31
The structural basis of the functioning of bacteriorhodopsin: An overview
journal, April 1979
- Ovchinnikov, Yu. A.; Abdulaev, N. G.; Feigina, M. Yu.
- FEBS Letters, Vol. 100, Issue 2
Breaking the Carboxyl Rule
journal, July 2013
- Balashov, Sergei P.; Petrovskaya, Lada E.; Imasheva, Eleonora S.
- Journal of Biological Chemistry, Vol. 288, Issue 29
Structural Changes in Bacteriorhodopsin During Ion Transport at 2 Angstrom Resolution
journal, October 1999
- Luecke, H.
- Science, Vol. 286, Issue 5438
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
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
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
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
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
Proton/sodium pumping pyrophosphatases: the last of the primary ion pumps
journal, August 2014
- Tsai, Jia-Yin; Kellosalo, Juho; Sun, Yuh-Ju
- Current Opinion in Structural Biology, Vol. 27
Environmental Genome Shotgun Sequencing of the Sargasso Sea
journal, April 2004
- Venter, J. C.
- Science, Vol. 304, Issue 5667
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
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
Pathways of proton release in the bacteriorhodopsin photocycle
journal, September 1992
- Zimanyi, Laszlo; Varo, Gyorgy; Chang, Man
- Biochemistry, Vol. 31, Issue 36
PURPLE MEMBRANE: SURFACE CHARGE DENSITY and THE MULTIPLE EFFECT OF pH and CATIONS
journal, December 1990
- Jonas, Roy; Ebrey, Thomas G.
- Photochemistry and Photobiology, Vol. 52, Issue 6
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
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
Functions of a New Photoreceptor Membrane
journal, October 1973
- Oesterhelt, D.; Stoeckenius, W.
- Proceedings of the National Academy of Sciences, Vol. 70, Issue 10
Role of Na + and K + in Enzyme Function
journal, October 2006
- Page, Michael J.; Di Cera, Enrico
- Physiological Reviews, Vol. 86, Issue 4
Halorhodopsin is a light-driven chloride pump.
journal, September 1982
- Schobert, B.; Lanyi, J. K.
- Journal of Biological Chemistry, Vol. 257, Issue 17
Eubacterial rhodopsins — Unique photosensors and diverse ion pumps
journal, May 2014
- Brown, Leonid S.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 5
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
A model-independent approach to assigning bacteriorhodopsin's intramolecular reactions to photocycle intermediates
journal, November 1993
- Hessling, B.; Souvignier, G.; Gerwert, K.
- Biophysical Journal, Vol. 65, Issue 5
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
Predicted bacteriorhodopsin from Exiguobacterium sibiricum is a functional proton pump
journal, September 2010
- Petrovskaya, L. E.; Lukashev, E. P.; Chupin, V. V.
- FEBS Letters, Vol. 584, Issue 19
Xanthorhodopsin: A Proton Pump with a Light-Harvesting Carotenoid Antenna
journal, September 2005
- Balashov, S. P.
- Science, Vol. 309, Issue 5743
Crystal Structure of Na + , K + -ATPase in the Na + -Bound State
journal, September 2013
- Nyblom, Maria; Poulsen, Hanne; Gourdon, Pontus
- Science, Vol. 342, Issue 6154
A Vibrational Spectral Maker for Probing the Hydrogen-Bonding Status of Protonated Asp and Glu Residues
journal, April 2005
- Nie, Beining; Stutzman, Jerrod; Xie, Aihua
- Biophysical Journal, Vol. 88, Issue 4