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Fourier Transform Infrared Difference.Spectroscopy Of Proc. NatL Acad. Sci. USA Vol. 79, pp. 4972-4976, August 1982 'Biophysics Fourier transform infrared difference. spectroscopy of bacteriorhodopsin and its photoproducts* (purple membrane/Schiff. base/conformational changes/low temperature/hydrated films) K. BAGLEYt, G. DOLLINGERt, L. EISENSTEINtt, A. K. SINGH§, AND L. ZIMANYI¶ tDepartment of Physics, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801; and §Department of Chemistry, Columbia University, New York, New York 10027 Communicated by Hans Frauenfelder, May 19, 1982 ABSTRACT Fourier transform infrared difference spectros- CH3 CH3 H CH3 H 'CH3 H copy has been used to obtain the vibrational modes. in the chro- 16 17 19 20 *mophore and apoprotein 'that change in intensity or position be- tween light-adapted bacteriorhodopsin and the K and M- inter- mediates in its photocycle and between dark-adapted and light- 3 5~L adapted bacteriorhodopsin. Our infrared' measurements provide H4 HH H~ independent verification ofresonance Raman results that in light- adapted bacteriorhodopsin the protein-chromophore linkage is a protonated Schiff base and in the M state the Schiff base is un- FIG. 1. All-trans-retinal bound to apoprotein via a protonated ,protonated. Although we cannot unambiguously identify the Schiff Schiff base linkage. In 15-deuterioretinal the hydrogen at carbon 15 base stretching frequency in the K state, the most'likely interpre- is replaced by deuterium. tation of deuterium shifts of the chromophore hydrogen out-of- plane vibrations is that the Schiff base in K is protonated. The ficult owing in part~~~Ito the large perturbation ofthe chromophore intensity of the hydrogen out-of-plane vibrations in the K state by the protein environment (12). However, it is widely accepted compared with the intensities of.those in light-adapted and'dark- retinal is shows that the conformation of the that these studies have shown that in bR's all-trans adapted bacteriorhodopsin a base and chromophore in K is considerably distorted. In addition, we find bound to the protein via protonated' Schiff linkage evidence that the conformation ofthe protein changes during the that in M the chromophore is in the 13,cis conformation and the photocycle. Schiff base linkage is-unprotonated (13-19). For other inter- mediates in the photocycle there is not such a consensus on the Bacteriorhodopsin (bR) is the light-energy transducing protein interpretation of resonance Raman results, nor is there com- found in the purple membrane (PM) of the extreme halophile plete agreement among data obtained by different groups. Sig- Halobacterium halobium (1-4). The chromophore in bacterio- nificant discrepancies between various resonance Raman data rhodopsin is a single molecule of retinal, covalently bound to occur for the K intermediate, especially in the Schiff base region the £-amino group ofa lysine (Lys-216) via a Schiffbase linkage (16, 19, 20). These discrepancies must be resolved in order to (Fig 1). Upon absorption oflight, the light-adapted form ofbR understand the mechanism ofthe primary photochemical event (bR ) undergoes a photocycle, bRLA +--* K -- L -- M -O 0 (bR ---)K). bRLA, during which protons are pumped from the inside of It has been hypothesized that the resonance Raman process the cell to the extracellular medium. The resulting proton gra- itselfdisturbs the ground state ofthe system being investigated dient is used by the cell to generate chemical energy in the form and therefore the vibrational modes measured by resonance ofATP and drive other energy-requiring processes. In the dark, Raman are not the same as would be detected by IR absorption bRLA thermally converts to the dark-adapted form of bR (bRDA). spectroscopy. In particular, Sandorfy and co-workers (21) have The mechanism of this light driven proton pump has been proposed that the Schiff base nitrogen is not fully protonated, studied by using visible and ultraviolet, resonance Raman (5), but rather is only hydrogen bonded, and that the proton is par- and infrared (IR) (6-8) spectroscopies and chemical extraction tially transferred to the Schiff base during the scattering pro- techniques. These investigations strongly suggest that during cess, giving rise to the apparent protonation. the photocycle changes occur in both the isomeric state of the Conventional IR absorption spectroscopy cannot be used to chromophore and the state ofprotonation ofthe Schiff'base. In study the conformation ofthe chromophore because the vibra- particular, chemical extraction experiments have provided evi- tional modes of the chromophore are superimposed on the dence that the chromophore in bRLA is in an all-trans config- much strongerinfrared absorption bands of H20 and the pro- uration, that in the L and M states it is in a 13-cis configuration, tein backbone. To overcome this problem infrared difference and that in bRDA the chromophore exists in two isomeric forms, spectroscopy is used, because only modes that'change intensity all-trans and 13-cis, in a ratio of approximately 1: 1 (9-11). or position during the photocycle will appear in the difference Evidence for the conformation of the chromophore in situ spectrum. Kinetic IR difference spectroscopy (8) has been ap- comes primarily from comparisons between the resonance Ra- man in both and 2H20 of native bR, Abbreviations: bR, bacteriorhodopsin bRLA, light-adapted form ofbR; vibrational spectra 'H20 bRDA, dark-adapted form of bR, bRl', 13-cis component of bRDA; bR in which analogs ofretinal have been incorporated, and ret- FMIR, Fourier transform infrared; PM, purple membrane. inal 'Schiff bases. Analysis of the results from such work is dif- * A preliminary account ofthis work was presented at-the 26th Annual Meeting of the Biophysical Society, February 1982. The publication costs ofthis article were defrayed in.part by page charge MTo whom reprint requests should be addressed. payment. This article must therefore be hereby marked "advertise- ¶ Permanent address: Institute ofBiophysics, Biological Research Cen- ment" in accordance with 18 U. S. C. §1734 solely to indicate this fact. ter, Szeged, Hungary. 4972 Downloaded by guest on September 24, 2021 Biophysics: Bagley et al. Proc. Nati. Acad. Sci. USA 79 (1982) 4973 plied to bacteriorhodopsin. The results in the Schiff base region 24X1O-3 . ... could not be correlated with those obtained in resonance Raman experiments. [ i To help resolve some of these conflicts and to provide ad- 16 ditional information on the changes in conformation of the pro- ID tein as well as the chromophore that occur during the photo- 8 a cycle, we have applied Fourier transform IR (FTIR) difference co spectroscopy to bR and some of the intermediates in its pho- o tocycle. After completing these studies, we became aware of studies carried out by Rothschild and co-workers using similar -8 l techniques (22, 23). | MATERIALS AND METHODS The sample is prepared by drying PM on an IR and visible light 24 A transmitting window (IRTRAN 2; Kodak) and adding enough water to bring the films to full hydration. The photocycle in 16x10-& - these wet films is similar to that of aqueous suspensions (24). Deuterated films were prepared by repeated drying and re- hydration of the films with 2H20. The absorbance of the films 8 was approximately 0.6 at 570 nm. Measurements were made XnC on hydrated or deuterated films of native bR and bR regener- S A ated with 15-deuterioretinal. The regeneration was done by fol- 0 - lowing standard procedures (12). < The films were vacuum sealed and mounted in a helium re- .5 frigerator (NaCl windows) that was placed in a Nicolet 7199 -8 1-0 FTIR spectrometer, equipped with an HgCdTe detector. After being light-adapted at 300 K, the sample was cooled to a tem- B perature at which the intermediate to be investigated is stable. -16 B An IR transmission spectrum of bR'A, at 2-cm- resolution in LO the region 4,900-700 cm-1 was collected and stored (2,048 28 10-3---r' _i ,. scans, collection time :'30 min). Light from a projector with a 24 narrow bandpass interference filter (AA = 10 nm) was used to create a photostationary state containing bR'A and a large 16I amount of the relevant intermediate, and the IR transmission spectrum of this photostationary state was collected. The log- 8 8 .l N arithmic difference of the two spectra was calculated. If the I' l absorbance of the intermediate at a particular wavenumber is oO greater than that of bRI, the difference spectrum has a positive peak at that frequency. Ifthe absorbance ofbR is greater, the < -8 N difference spectrum has a negative peak. For the dark-adapted N minus light-adapted experiment the sample was dark-adapted -16 at 300 K and cooled to 250 K to reduce the water vapor pressure, LO and a spectrum was taken. The sample was then light-adapted -24, '"._,_,_._, _, and another spectrum was taken. Because the chromophore in 32x10-3 co bRDA exists in two isomeric forms, all-trans and 13-cis, and O bRIA is all-trans (see above), the bRDA _ bR's difference 24 spectrum gives the vibrational modes of bR containing the 13- cis isomer of the chromophore, bR'3-n. As a control all exper- 16 LOCIJ?-2 iments were repeated with the refrigerator in a Cary 14 visible 28 M |- c - spectrophotometer. The protein bands above 2,000 cm1 were obscured by 'H20 0 or H20, therefore only data below 2,000 cm' will be pre- sented in this paper. The IR vibrational frequencies given in <s N this paper are those that occur in the difference spectra. Except1 a where specifically mentioned, no corrections have been made -16 for the distortion in the shape and location ofpeaks that occur t. D when difference spectra are calculated, nor were the spectra -24 LO smoothed.
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