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

Balashov, Sergei P.; Imasheva, Eleonora S.; Dioumaev, Andrei K.; Wang, Jennifer M.; Jung, Kwang-Hwan; Lanyi, Janos K.

doi:10.1021/bi501064n

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

Journal Article · Mon Nov 24 00:00:00 EST 2014 · Biochemistry

DOI:https://doi.org/10.1021/bi501064n· OSTI ID:1165228

Balashov, Sergei P. ^[1]; Imasheva, Eleonora S. ^[1]; Dioumaev, Andrei K. ^[1]; Wang, Jennifer M. ^[1]; Jung, Kwang-Hwan ^[2]; Lanyi, Janos K. ^[1]

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

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.

View Journal Article

Cite

Export

Save

Research Organization:: Univ. of California, Irvine, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: DEFG03-86ER13525; FG03-86ER13525

OSTI ID:: 1165228

Alternate ID(s):: OSTI ID: 1345588

Journal Information:: Biochemistry, Journal Name: Biochemistry Vol. 53 Journal Issue: 48; ISSN 0006-2960

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 65 works

Citation information provided by
Web of Science

References (61)

Structure of the Rotor Ring of F-Type Na+-ATPase from Ilyobacter tartaricus Meier, T. Science, Vol. 308, Issue 5722 https://doi.org/10.1126/science.1111199	journal	April 2005
Evaluation of intrinsic chemical kinetics and transient product spectra from time-resolved spectroscopic data Dioumaev, Andrei K. Biophysical Chemistry, Vol. 67, Issue 1-3 https://doi.org/10.1016/S0301-4622(96)02268-5	journal	September 1997
Bacteriorhodopsin photocycle at cryogenic temperatures reveals distributed barriers of conformational substates Dioumaev, A. K.; Lanyi, J. K. Proceedings of the National Academy of Sciences, Vol. 104, Issue 23 https://doi.org/10.1073/pnas.0703859104	journal	May 2007
Protonation reactions and their coupling in bacteriorhodopsin Balashov, Sergei P. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1460, Issue 1 https://doi.org/10.1016/S0005-2728(00)00131-6	journal	August 2000
Structure of bacteriorhodopsin at 1.55 Å resolution Luecke, Hartmut; Schobert, Brigitte; Richter, Hans-Thomas Journal of Molecular Biology, Vol. 291, Issue 4 https://doi.org/10.1006/jmbi.1999.3027	journal	August 1999
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 Takei, Ken-ichi; Takahashi, Ryouta; Noguchi, Takumi The Journal of Physical Chemistry B, Vol. 112, Issue 21 https://doi.org/10.1021/jp801151k	journal	May 2008
Switch from Conventional to Distributed Kinetics in the Bacteriorhodopsin Photocycle Dioumaev, Andrei K.; Lanyi, Janos K. Biochemistry, Vol. 47, Issue 42 https://doi.org/10.1021/bi801247e	journal	September 2008
Bacterial Rhodopsin: Evidence for a New Type of Phototrophy in the Sea Beja, O.; Aravind, L.; Koonin, Eugene V. Science, Vol. 289, Issue 5486, p. 1902-1906 https://doi.org/10.1126/science.289.5486.1902	journal	September 2000
Halorhodopsin, a light-driven electrogenic chloride-transport system Lanyi, J. K. Physiological Reviews, Vol. 70, Issue 2 https://doi.org/10.1152/physrev.1990.70.2.319	journal	April 1990
Complete Genome Sequences of Krokinobactersp. Strain 4H-3-7-5 and Lacinutrixsp. Strain 5H-3-7-4, Polysaccharide-Degrading Members of the Family Flavobacteriaceae Klippel, B.; Lochner, A.; Bruce, D. C. Journal of Bacteriology, Vol. 193, Issue 17 https://doi.org/10.1128/JB.05518-11	journal	July 2011
Proton Transfers in the Photochemical Reaction Cycle of Proteorhodopsin ^† Dioumaev, Andrei K.; Brown, Leonid S.; Shih, Jennifer Biochemistry, Vol. 41, Issue 17 https://doi.org/10.1021/bi025563x	journal	April 2002
Aspartic acid-96 is the internal proton donor in the reprotonation of the Schiff base of bacteriorhodopsin. Otto, H.; Marti, T.; Holz, M. Proceedings of the National Academy of Sciences, Vol. 86, Issue 23 https://doi.org/10.1073/pnas.86.23.9228	journal	December 1989
From Femtoseconds to Biology: Mechanism of Bacteriorhodopsin's Light-Driven Proton Pump Mathies, R. A.; Lin, S. W.; Ames, J. B. Annual Review of Biophysics and Biophysical Chemistry, Vol. 20, Issue 1 https://doi.org/10.1146/annurev.bb.20.060191.002423	journal	June 1991
Proton transfer via a transient linear water-molecule chain in a membrane protein Freier, E.; Wolf, S.; Gerwert, K. Proceedings of the National Academy of Sciences, Vol. 108, Issue 28 https://doi.org/10.1073/pnas.1104735108	journal	June 2011
Channelrhodopsin unchained: Structure and mechanism of a light-gated cation channel Lórenz-Fonfría, Víctor A.; Heberle, Joachim Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 5 https://doi.org/10.1016/j.bbabio.2013.10.014	journal	May 2014
Application of FTIR Spectroscopy to the Structural Study on the Function of Bacteriorhodopsin Maeda, Akio Israel Journal of Chemistry, Vol. 35, Issue 3-4 https://doi.org/10.1002/ijch.199500038	journal	January 1995
Proton binding within a membrane protein by a protonated water cluster Garczarek, F.; Brown, L. S.; Lanyi, J. K. Proceedings of the National Academy of Sciences, Vol. 102, Issue 10 https://doi.org/10.1073/pnas.0500421102	journal	February 2005
Reversible steps in the bacteriorhodopsin photocycle. Lozier, R. H.; Xie, A.; Hofrichter, J. Proceedings of the National Academy of Sciences, Vol. 89, Issue 8 https://doi.org/10.1073/pnas.89.8.3610	journal	April 1992
Fourier Transform Infrared Spectra of a Late Intermediate of the Bacteriorhodopsin Photocycle Suggest Transient Protonation of Asp-212 Dioumaev, Andrei K.; Brown, Leonid S.; Needleman, Richard Biochemistry, Vol. 38, Issue 31 https://doi.org/10.1021/bi990873+	journal	July 1999
The role of protein-bound water molecules in microbial rhodopsins Gerwert, Klaus; Freier, Erik; Wolf, Steffen Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 5 https://doi.org/10.1016/j.bbabio.2013.09.006	journal	May 2014
Electron-crystallographic Refinement of the Structure of Bacteriorhodopsin Grigorieff, N.; Ceska, T. A.; Downing, K. H. Journal of Molecular Biology, Vol. 259, Issue 3 https://doi.org/10.1006/jmbi.1996.0328	journal	June 1996
Light isomerizes the chromophore of bacteriorhodopsin Tsuda, Motoyuki; Glaccum, Moira; Nelson, Burr Nature, Vol. 287, Issue 5780 https://doi.org/10.1038/287351a0	journal	September 1980
Proton transfers in the bacteriorhodopsin photocycle Lanyi, Janos K. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1757, Issue 8 https://doi.org/10.1016/j.bbabio.2005.11.003	journal	August 2006
Genomic Makeup of the Marine Flavobacterium Nonlabens (Donghaeana) dokdonensis and Identification of a Novel Class of Rhodopsins Kwon, Soon-Kyeong; Kim, Byung Kwon; Song, Ju Yeon Genome Biology and Evolution, Vol. 5, Issue 1 https://doi.org/10.1093/gbe/evs134	journal	January 2013
Genome sequence of the Antarctic rhodopsins-containing flavobacterium Gillisia limnaea type strain (R-8282T) Riedel, Thomas; Held, Brittany; Nolan, Matt Standards in Genomic Sciences, Vol. 7, Issue 1 https://doi.org/10.4056/sigs.3216895	journal	October 2012
The mechanism of rotating proton pumping ATPases Nakanishi-Matsui, Mayumi; Sekiya, Mizuki; Nakamoto, Robert K. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1797, Issue 8 https://doi.org/10.1016/j.bbabio.2010.02.014	journal	August 2010
The infrared absorption of amino acid side chains Barth, Andreas Progress in Biophysics and Molecular Biology, Vol. 74, Issue 3-5 https://doi.org/10.1016/S0079-6107(00)00021-3	journal	January 2000
Infrared Methods for Monitoring the Protonation State of Carboxylic Amino Acids in the Photocycle of Bacteriorhodopsin Dioumaev, A. K. Biochemistry (Moscow), Vol. 66, Issue 11, p. 1269-1276 https://doi.org/10.1023/A:1013135419529	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. Subramaniam, S.; Marti, T.; Khorana, H. G. Proceedings of the National Academy of Sciences, Vol. 87, Issue 3 https://doi.org/10.1073/pnas.87.3.1013	journal	February 1990
Crystallographic Structure of the K Intermediate of Bacteriorhodopsin: Conservation of Free Energy after Photoisomerization of the Retinal Schobert, Brigitte; Cupp-Vickery, Jill; Hornak, Viktor Journal of Molecular Biology, Vol. 321, Issue 4 https://doi.org/10.1016/S0022-2836(02)00681-2	journal	August 2002
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 Sasaki, Jun; Lanyi, Janos K.; Needleman, Richard Biochemistry, Vol. 33, Issue 11 https://doi.org/10.1021/bi00177a006	journal	March 1994
Light-induced changes of the pH gradient and the membrane potential in H. halobium Michel, H.; Oesterhelt, D. FEBS Letters, Vol. 65, Issue 2 https://doi.org/10.1016/0014-5793(76)80473-5	journal	June 1976
Structure and Function of Halorhodopsin Oesterhelt, Dieter Israel Journal of Chemistry, Vol. 35, Issue 3-4 https://doi.org/10.1002/ijch.199500044	journal	January 1995
The role of back-reactions and proton uptake during the N .fwdarw. O transition in bacteriorhodopsin's photocycle: a kinetic resonance Raman study Ames, James B.; Mathies, Richard A. Biochemistry, Vol. 29, Issue 31 https://doi.org/10.1021/bi00483a005	journal	August 1990
The structural basis of the functioning of bacteriorhodopsin: An overview Ovchinnikov, Yu. A.; Abdulaev, N. G.; Feigina, M. Yu. FEBS Letters, Vol. 100, Issue 2 https://doi.org/10.1016/0014-5793(79)80338-5	journal	April 1979
Breaking the Carboxyl Rule Balashov, Sergei P.; Petrovskaya, Lada E.; Imasheva, Eleonora S. Journal of Biological Chemistry, Vol. 288, Issue 29 https://doi.org/10.1074/jbc.M113.465138	journal	July 2013
Structural Changes in Bacteriorhodopsin During Ion Transport at 2 Angstrom Resolution Luecke, H. Science, Vol. 286, Issue 5438 https://doi.org/10.1126/science.286.5438.255	journal	October 1999
CLOSING IN ON BACTERIORHODOPSIN: Progress in Understanding the Molecule Haupts, Ulrich; Tittor, Jörg; Oesterhelt, Dieter Annual Review of Biophysics and Biomolecular Structure, Vol. 28, Issue 1 https://doi.org/10.1146/annurev.biophys.28.1.367	journal	June 1999
Amino acid sequence of bacteriorhodopsin. Khorana, H. G.; Gerber, G. E.; Herlihy, W. C. Proceedings of the National Academy of Sciences, Vol. 76, Issue 10 https://doi.org/10.1073/pnas.76.10.5046	journal	October 1979
Nature's toolkit for microbial rhodopsin ion pumps Beja, O.; Lanyi, J. K. Proceedings of the National Academy of Sciences, Vol. 111, Issue 18 https://doi.org/10.1073/pnas.1405093111	journal	April 2014
FTIR Spectroscopy of a Light-Driven Compatible Sodium Ion-Proton Pumping Rhodopsin at 77 K Ono, Hikaru; Inoue, Keiichi; Abe-Yoshizumi, Rei The Journal of Physical Chemistry B, Vol. 118, Issue 18 https://doi.org/10.1021/jp500756f	journal	April 2014
A light-driven sodium ion pump in marine bacteria Inoue, Keiichi; Ono, Hikaru; Abe-Yoshizumi, Rei Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms2689	journal	April 2013
Proton/sodium pumping pyrophosphatases: the last of the primary ion pumps Tsai, Jia-Yin; Kellosalo, Juho; Sun, Yuh-Ju Current Opinion in Structural Biology, Vol. 27 https://doi.org/10.1016/j.sbi.2014.03.007	journal	August 2014
Environmental Genome Shotgun Sequencing of the Sargasso Sea Venter, J. C. Science, Vol. 304, Issue 5667 https://doi.org/10.1126/science.1093857	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 Zscherp, Christian; Heberle, Joachim The Journal of Physical Chemistry B, Vol. 101, Issue 49 https://doi.org/10.1021/jp971047i	journal	December 1997
Aspartate–Histidine Interaction in the Retinal Schiff Base Counterion of the Light-Driven Proton Pump of Exiguobacterium sibiricum Balashov, S. P.; Petrovskaya, L. E.; Lukashev, E. P. Biochemistry, Vol. 51, Issue 29 https://doi.org/10.1021/bi300409m	journal	July 2012
Pathways of proton release in the bacteriorhodopsin photocycle Zimanyi, Laszlo; Varo, Gyorgy; Chang, Man Biochemistry, Vol. 31, Issue 36 https://doi.org/10.1021/bi00151a022	journal	September 1992
PURPLE MEMBRANE: SURFACE CHARGE DENSITY and THE MULTIPLE EFFECT OF pH and CATIONS Jonas, Roy; Ebrey, Thomas G. Photochemistry and Photobiology, Vol. 52, Issue 6 https://doi.org/10.1111/j.1751-1097.1990.tb08455.x	journal	December 1990
Two light-transducing membrane proteins: bacteriorhodopsin and the mammalian rhodopsin. Khorana, H. G. Proceedings of the National Academy of Sciences, Vol. 90, Issue 4 https://doi.org/10.1073/pnas.90.4.1166	journal	February 1993
Bacteriorhodopsin-like proteins of eubacteria and fungi: the extent of conservation of the haloarchaeal proton-pumping mechanism Brown, Leonid S.; Jung, Kwang-Hwan Photochemical & Photobiological Sciences, Vol. 5, Issue 6 https://doi.org/10.1039/b514537f	journal	January 2006
Functions of a New Photoreceptor Membrane Oesterhelt, D.; Stoeckenius, W. Proceedings of the National Academy of Sciences, Vol. 70, Issue 10 https://doi.org/10.1073/pnas.70.10.2853	journal	October 1973
Role of Na ⁺ and K ⁺ in Enzyme Function Page, Michael J.; Di Cera, Enrico Physiological Reviews, Vol. 86, Issue 4 https://doi.org/10.1152/physrev.00008.2006	journal	October 2006
Halorhodopsin is a light-driven chloride pump. Schobert, B.; Lanyi, J. K. Journal of Biological Chemistry, Vol. 257, Issue 17 https://doi.org/10.1016/S0021-9258(18)34020-1	journal	September 1982
Eubacterial rhodopsins — Unique photosensors and diverse ion pumps Brown, Leonid S. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 5 https://doi.org/10.1016/j.bbabio.2013.05.006	journal	May 2014
Bacteriorhodopsin D85N: Three spectroscopic species in equilibrium Turner, George J.; Miercke, Larry J. W.; Thorgeirsson, Thorgeir E. Biochemistry, Vol. 32, Issue 5 https://doi.org/10.1021/bi00056a019	journal	February 1993
A model-independent approach to assigning bacteriorhodopsin's intramolecular reactions to photocycle intermediates Hessling, B.; Souvignier, G.; Gerwert, K. Biophysical Journal, Vol. 65, Issue 5 https://doi.org/10.1016/S0006-3495(93)81264-5	journal	November 1993
Ion channels versus ion pumps: the principal difference, in principle Gadsby, David C. Nature Reviews Molecular Cell Biology, Vol. 10, Issue 5 https://doi.org/10.1038/nrm2668	journal	April 2009
Predicted bacteriorhodopsin from Exiguobacterium sibiricum is a functional proton pump Petrovskaya, L. E.; Lukashev, E. P.; Chupin, V. V. FEBS Letters, Vol. 584, Issue 19 https://doi.org/10.1016/j.febslet.2010.09.005	journal	September 2010
Xanthorhodopsin: A Proton Pump with a Light-Harvesting Carotenoid Antenna Balashov, S. P. Science, Vol. 309, Issue 5743 https://doi.org/10.1126/science.1118046	journal	September 2005
Crystal Structure of Na ⁺ , K ⁺ -ATPase in the Na ⁺ -Bound State Nyblom, Maria; Poulsen, Hanne; Gourdon, Pontus Science, Vol. 342, Issue 6154 https://doi.org/10.1126/science.1243352	journal	September 2013
A Vibrational Spectral Maker for Probing the Hydrogen-Bonding Status of Protonated Asp and Glu Residues Nie, Beining; Stutzman, Jerrod; Xie, Aihua Biophysical Journal, Vol. 88, Issue 4 https://doi.org/10.1529/biophysj.104.047639	journal	April 2005

Figures / Tables (10)

Similar Records

Genome sequence of the Antarctic rhodopsins-containing flavobacterium Gillisia limnaea type strain (R-8282^T)

Journal Article · Wed Oct 10 00:00:00 EDT 2012 · Standards in Genomic Sciences · OSTI ID:1165228

Riedel, Thomas; Held, Brittany; Nolan, Matt; +29 more

Identification of the key determinant of the transport promiscuity in Na+-translocating rhodopsins

Journal Article · Tue May 15 00:00:00 EDT 2018 · Biochemical and Biophysical Research Communications · OSTI ID:1165228

Mamedov, Adalyat M.; Bertsova, Yulia V.; Anashkin, Viktor A.; +2 more

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

Journal Article · Sun Jan 01 00:00:00 EST 2012 · Standards in Genomic Sciences · OSTI ID:1165228

Riedel, Thomas; Held, Brittany; Nolan, Matt; +29 more

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
59 BASIC BIOLOGICAL SCIENCES
60 APPLIED LIFE SCIENCES

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

Citation Formats

References (61)

Figures / Tables (10)

Similar Records

Related Subjects

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