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Received April 30, 2001; Revision received June 2, 2001
Phoborhodopsin (pR or sensory rhodopsin II, sRII) is a photoreceptor of the negative phototaxis of Halobacterium salinarum, and pharaonis phoborhodopsin (ppR or pharaonis sensory rhodopsin II, psRII) is a corresponding protein of Natronobacterium pharaonis. The photocycle of ppR is essentially as follows: ppR(498) --> ppRK(~540) --> ppRKL(512) --> ppRL(488) --> ppRM(390) --> ppRO(560) --> ppR (numbers in parenthesis denote the maximum absorbance). The photocycle is very similar to that of bacteriorhodopsin, but the rate of initial pigment recovery is about two-orders of magnitude slower. By low-temperature spectroscopy, two K-intermediates were found but the L intermediate was not detected. The lack of L indicates extraordinary stability of K at low temperature. ppRM is photoactive similar to M of bR. The ground state ppR contains only all-trans retinal whereas ppRM and ppRO contain 13-cis and all-trans, respectively. ppR has the ability of light-induced proton transport from the inside to the outside. Proton uptake occurs at the formation of ppRO and the release at its decay. ppR associates with its transducer and this complex transmits a signal to the cytoplasm. The proton transport ability is lost when the complex forms, but the proton uptake and release still occur, suggesting that the proton movement is non-electrogenic (release and uptake occur from the same side). The stoichiometry of the complex between ppR and the transducer is 1 : 1. ppR or pR has absorption maximum at ~500 nm, which is blue-shifted from those of other archaeal rhodopsins. The molecular mechanism of this color regulation is not yet solved.
KEY WORDS: phoborhodopsin, photocycle, photoinduced proton transfer
Abbreviations: bR) bacteriorhodopsin; DM) n-dodecyl-beta-maltoside; hR) halorhodopsin; pR) phoborhodopsin (sensory rhodopsin II, sRII); ppR) pharaonis phoborhodopsin (pharaonis sRII, psRII); ppRK, ppRL, ppRM and ppRO) K-, L-, M-, and O-like intermediate of ppR, respectively; sR) sensory rhodopsin; lambdamax) absorption maximum; FTIR) infrared Fourier spectroscopy.
Halobacteria contain four retinal proteins (archaeal rhodopsins) which
are bacteriorhodopsin (bR) [1-3], halorhodopsin (hR) [4, 5], sensory rhodopsin I (sRI) [6,
7] and phoborhodopsin (pR; also called sensory
rhodopsin II, sRII) [8, 9]. The
former two are light-driven ion pumps; bR works as an outward proton
pump and hR as an inward halogen ion pump. The latter two are
photoreceptors of this bacterium. Three photosystems (PS) of
Halobacterium salinarum (former halobium) were pointed
out [10], and they are PS570 (or PS565), PS370,
and PS470 where the numbers represent the maximum wavelength of the
halobacterial photoresponses. PS570 causes the cells to be attracted to
green-orange light whereas PS370 and PS470 cause avoidance behavior
(negative phototaxis) from near UV blue light and from blue-green
light, respectively. Spudich and Bogomolni [6]
proved that the photoreceptor of PS570 is the ground state of sRI
(absorption maximum lambdamax of sRI is 587 nm;
see [11] for the difference between 570 (565) and
587 nm maxima). It was also shown that a long-lived
photointermediate of sRI whose absorption maximum is 373 nm is the
receptor of PS370 [12, 13].
What is the receptor of PS470? Takahashi et al. [8]
isolated a mutant that showed only negative phototaxis whose action
maximum is located at ~475 nm. The retinoid receptor of this
negative phototaxis system was named phoborhodopsin (pR; also sensory
rhodopsin II, sRII) whose absorption maximum was 487 nm [14, 15]. Similar reports were
published later from other laboratories [16-18].
The primary structure of this pigment was solved by Zhang et al. [19]. sRI and pR (sRII) transmit their signals through integral membrane transducer proteins named HtrI and HtrII, which are considered to form a signaling complex firmly with respective receptors [7]. By these signaling systems, these bacteria move toward longer wavelength light (lambda > 520 nm) where bR and hR work, while they avoid shorter wavelength light (lambda < 520 nm), which contains harmful near-UV light [14].
The publications on the study of pR from H. salinarium (spR, ssRII) were not so many because its purification was not achieved at that time (see below) and because the amounts of the protein in the cell membrane were very small. Nevertheless, several investigations were performed. On millisecond time scale at room temperature, two photointermediates were found which corresponded to M- and O-intermediates of bR [14]. The presence of another intermediate, which corresponded to K intermediate of bR, was shown by low-temperature spectrophotometry [20, 21]. At present, the expression system of ssRII has been achieved and the pigment was purified to investigate the primary events in its photocycle [22]. It was reported that a haloalkaliphilic bacterium (Natronobacterium pharaonis) had retinal pigments [23]. The absorption spectrum of one of the pigments was very similar in shape to that of pR except for a 10-nm red shift (lambdamax at about 500 nm). In addition, it was shown that this pR-like pigment in N. pharaonis worked as a photoreceptor of the negative phototactic response of this bacterium [24, 25]. We named this pR-like pigment pharaonis phoborhodopsin (ppR), which is also called pharaonis sensory rhodopsin II (psRII). We succeeded in its purification with small amounts of impurities (maybe from heme proteins) and studied its photochemistry [26]. At almost the same time, Scharf et al. [27] also investigated the photochemical conversions of ppR and described the stability of ppR in lower salt concentration while ssRI loses its activity gradually in low salt concentration [28]. The primary structure of ppR (psRII) was given by Seidel et al. [29]. Later we developed an expression system of ppR in Escherichia coli cells [30], and using this system, various mutant proteins were prepared for the characterization of ppR. In the present mini-review, we describe the photochemistry, the photoinduced proton transfer, and the color regulation of ppR. Results described here are mainly from our laboratory.
PHOTOCHEMISTRY OF WILD-TYPE ppR
Photochemistry was studied by low-temperature spectrophotometry [26] and by flash photolysis at room temperature [31]. Irradiation of ppR below -100°C produced an intermediate corresponding to the K-intermediate of bR (ppRK), and this intermediate was a composite of two components. The existence of two K-like intermediates was confirmed also by a recent FTIR study using a ppR sample expressed in E. coli [32]. The original ppR and ppRK were perfectly photoreversible as is true also for other retinal proteins.
On warming, ppRK was directly converted to an M-like intermediate (ppRM) without formation of the L-like intermediate (ppRL). The temperature where the conversion occurred was -70 or -90°C. This temperature is relative high, suggesting that ppRK is relatively stable at low temperature. Molecular interpretation of the existence of two stable K's awaits further investigation. The lack of ppRL was also shown in low temperature experiments of pR [21]. Note that this does not mean the lack of a L-like intermediate of ppR or pR: flash photolysis experiments at room temperature [31] revealed the existence of ppRL. Room-temperature flash photolysis experiments were done and we [31] proposed the following photocycle:
ppR(498) --> ppRK(~540) --> ppRKL(512) --> ppRL(488) --> ppRM(390) --> ppRO(560) --> ppR.
Here, ppRO is an O-like intermediate; lambdamax are given in parentheses. This photocycle resembles that of bR except that the N-intermediate was not found. The intermediates were named in analogy to those in the photocycle of bR. The species ppRKL was not detected at low temperature. An intermediate corresponding to the N-intermediate was difficult to observe. Chizhov et al. [33] measured flash photolysis under various conditions (temperature and pH) with 10 nsec resolution. The proposed scheme was much more complicated than that described above. They identified eight photochemically distinct kinetic states during the photocycle and some kinetic states were composed of an equilibrium mixture of intermediates including an N-like intermediate. Large changes in both the conformation and the molar volume were reported [34] upon the formation of ppRK. The quantum yield of the K-intermediate was found to be 0.51 ± 0.06 [34]. The largest difference in sensor archaeal rhodopsins (sRI, pR or ppR) from ion-transporting ones (bR and hR) is the slowness of the photocycle. The decay time constants of ppRM are ~20 sec-1 (pH 5) and 1 sec-1 (pH 9), and those of ppRO are 3-4 sec-1 which are almost independent of pH for the n-dodecyl-beta-maltoside (DM) solubilized sample suspended in 400 mM NaCl. The salt concentration affects the photocycling rate only to a small extent. Although this large pH dependence of the M-decay was not observed by Chizhov et al. [33], this dependence [35] helped to determine the steps in the photocycle that are coupled to proton uptake and release. As in the case of M of bR, the retinal configuration of ppRM is 13-cis and the Schiff base is deprotonated. The ppRO has all-trans chromophore and protonated Schiff base [36]. The ground state ppR contained only all-trans retinal (all-trans, 6S-trans for pR [37]), meaning that there is no light-dark adaptation [38]. When 13-cis retinal was added to ppR-opsin, two phases of the absorbance change were observed with half-times 5.9*103 and 104 sec. The lambdamax shifted gradually to the longer wavelength during the reconstitution with 13-cis retinal. After no shift was observed, only all-trans retinal was extracted. These observations were interpreted as [38]: 13-cis retinal can bind ppR-opsin very slowly and lambdamax of the 13-cis pigment is blue shifted from that of the all-trans retinal pigment by ~10 nm. After the binding, the chromophore isomerizes spontaneously to all-trans. On the other hand, reconstitution with all-trans retinal was rapid with a halftime of ~3 min [39]. This implies that the chromophore binding pocket has no space which can easily accommodate 13-cis retinal. This may be a reason for the lack of light-dark adaptation. Reconstitution experiments using retinal analogs showed that the space of the retinal binding site is restricted to the plane of the cyclohexenyl ring of the chromophore [39].
Photoactivity of M. In bR, photoexcitation of the M-intermediate causes fast reprotonation of the Schiff base [40, 41] from the counterion Asp85 [41-44] and transformation of the pigment back to its initial state through a non pumping pathway. Phototransformation of M involves the formation of two primary photoproducts, P421 and P433 [42, 44], also called M´ [45], and several subsequent thermal intermediates, which are in turn photoactive [44]. The analogous photo-transformation of ppRM was found [46]. Several new intermediates are formed during phototransformation of ppRM back to the initial ppR as was revealed by a low temperature study [46]. The scheme is as follows: ppRM(390) --> M´(404) --> ppR´(496) --> ppR´(504) --> ppR. Reversible phototransformations ppR <--> ppRM were observed at -60°C. They were accompanied by the perturbation of tryptophan(s) and probably tyrosine(s) residues, as reflected by changes in the UV absorption band [46]. The phototransformations of ppRM at room temperature is now being investigated.
Acceleration of M decay by azide. The decay of M was strongly accelerated by addition of azide, similar to that in the D96N mutant of bR in which Asp96 was substituted by Asn [47] and M-decay rate was very slow due to the lack of an internal proton-donating group (Asp96) to the deprotonated Schiff base of M. In ppR, the analogous donor is also absent: a residue corresponding to Asp96 of bR is Phe86, which probably explains at least partially the slow decay of ppRM. The addition of azide (500 mM) at pH 7.0 increased the rate of ppRM-decay by 300-fold [48]. Arrhenius analysis revealed decreases in the activation energy and a further decrease in the activation entropy. In other words, the increase in the rate originates from the decrease in the activation energy while the entropy (the frequency factor) has a negative effect. This is supposed to be related to the narrow chromophore binding pocket [39] as described above.
PHOTOCHEMISTRY OF MUTANT ppR
In the M-state of bacteriorhodopsin, the Schiff base is deprotonated and the decay of M coincides with the reprotonation of the Schiff base by the hydrogen-bonding chain that includes Asp96 and Thr46. In ppR these amino acids are replaced by Phe(F86) and Leu(L40) [29]. The absence of these internal proton donors in ppR may account for the slow decay of ppRM. The M-decay of F86D mutant was not significantly accelerated. However, in a double mutant (F86D/L40T) in which the internal proton donor and possibly hydrogen-bonding network was restored, the M-decay was accelerated as much as approximately 36-fold at pH 5.0 and 130-fold at pH 7.0 [49]. On the other hand, a mutant in which O-decay becomes faster than the wild-type has not been found yet.
Upon the formation of M of bR, the proton from the Schiff base is transferred to the proton acceptor, Asp85. The corresponding Asp of ppR is Asp75 [29]. This residue is considered, to be a proton acceptor from the protonated Schiff base [50]. Therefore, the D75N mutant does not form ppRM upon illumination, and this mutant has along-lived K-like intermediate [51]. This mutant, however, shows a photoinduced absorption band whose lambdamax is 330 nm, and this band appears also in the photocycle of the wild-type ppR when careful inspections of the flash-induced difference spectra were done [52]. If an intermediate responsible for this absorption band is another M-intermediate judging from the location of lambdamax, a question arises which residue works as the proton acceptor. Another possibility is that this absorption band is a beta-band of an intermediate. The decay constant of this band does not match that of M and O. Therefore, it might be a beta-band of the N intermediate which is hard to detect as described above. The beta-band of N of bR has a maximum at 330 nm (see review [53] and papers cited therein). The protonation state of Asp75 influences the lambdamax of ppR [33], as is similar to bR; this Asp is considered to be a counterion to the Schiff base. Upon acidification in the absence of chloride, lambdamax shifted to 522 nm. This bathochromic shift is thought to be caused by the protonation of Asp75. The D75N mutant has its lambdamax at approximately 520 nm, supporting this mechanism of the bathochromic shift. A titration of the shift yielded a pKa of 3.5 for Asp75. In the presence of chloride, the spectral shifts were different: with a decrease in pH, a bathochromic shift was first observed, followed by a hypsochromic shift on further acidification. This was interpreted [54] as the disappearance of a negative charge upon protonation of Asp75 being compensated by the binding of chloride, but it is worth noting that the binding of chloride required the protonation of Asp75 and of a second group other than Asp75. This was supported by the observation that in the presence of chloride, upon acidification, the lambdamax of D75N showed a blue shift, indicating that the protonation of a proton-associable group leads to the chloride binding that gives rise to a blue shift. Identification of these groups needs further work.
LIGHT-INDUCED ELECTROGENIC PROTON TRANSPORT
The SnO2 electrode is considered to monitor the pH change. Iwamoto et al. [55] constructed a photo-electrochemical cell composed of SnO2/thin ppR solution (~50 µM)/400 mM NaCl/SnO2. Photo-induced potential differences between two SnO2 transparent electrodes were measured. They were caused by changes in pH close to the SnO2 electrode surface. The signal was time-differentiated to envisage the direction of pH change and proton movement. A positive signal was due to a decrease in the local pH, i.e., proton release from ppR, and a negative signal was caused by the proton uptake. Immediately upon irradiation with continuous light, the transient negative on-response was observed for all pH values examined. The shape of the off-response to turning off the light was pH-dependent: at alkaline or neutral pH, a negative component was observed followed by a positive component. Another experiment on the off-response was done; the off-response was measured after the photo-steady state was attained. The shape of the off-response under varying pH well correlated with the ratio of contents of ppRM and ppRO at the steady state. Note that the ppRM decay is pH-dependent. It is concluded that the proton uptake occurs during ppRM --> ppRO and the proton release during ppRO --> ppR transitions. Illumination of ppR-containing membrane vesicles showed the sustained pH deflection in the medium, meaning the photo-induced membranous transport of proton whose direction is the same as that of bR [56].
Engelhard, Bamberg, and their colleagues [57, 58] using black lipid membranes or the oocyte system showed that ppR can transport protons upon illumination. They observed a small photocurrent at pH 5.0, and an increased current for the F86D mutant. Addition of azide increased the pump efficiency (the photocurrent) significantly. On the other hand, azide increases the ppRM decay but has no effect on ppRO decay, which is slower than ppRM decay. This means that the time required for the completion of the photocycle does not change significantly by the addition of azide. Why does addition of azide increase the photocurrent but not change in the time for the photocycle completion? They proposed a hypothesis of two-photon process suggesting that O-intermediate is photoactive which accelerates the photocycling rate under constant illumination [58]. The experimental proof is not yet obtained. Sudo et al. [56] and Schmies et al. [58] showed that the photo-induced proton transport ceased when ppR associates with the transducer while the photocycling rate was not significantly changed when they were co-expressed in membranes [56, 59]. Light-induced proton uptake and release were still observable even when ppR and the transducer formed the complex [56], although the vectorial nature of the proton movements was inhibited. Therefore, proton circulation (proton release and uptake from the same side) might occur, which was observed for the pR-transducer complex by Sasaki and Spudich [9, 60]. Sudo et al. [56] interpreted their results as the closure of the cytoplasmic channel caused by the association with its cognate transducer. This had been proposed by Spudich and his colleagues for pR and sR [9, 61]. Experimental verification for this is necessary.
COLOR REGULATION
The lambdamax of ppR or pR is remarkably different from those of the other three archaeal retinal proteins: bR, hR, and sR have their lambdamax at 560-590 nm while that of ppR or pR is blue-shifted to ~500 nm [62]. What is the molecular mechanism for the lambdamax of ppR or pR being different, although all archaeal rhodopsins are highly similar in their primary structure, especially in the chromophore binding site? According to the amino acid sequences of bR and ppR, retinal binding pockets of these proteins differ at only seven positions (Ile43, Ile83, Asn105, Val108, Phe127, Gly130 and Phe134 for ppR and Val49, Leu93, Asp115, Met113, Trp138, Ser141 and Met145 for bR, respectively). Furthermore, there exist three additional positions when the distance of a residue from the retinal is extended to 5 Å (Met109, Ala131, and Thr204 for ppR and Ile119, Thr142 and Ala215 for bR, respectively). To determine key residues causing different opsin-shift in ppR and bR, Shimono et al. [63-65] constructed ppR mutants in which each of the specific residues of the above sites was replaced by a corresponding residue of bR. In addition, 7- and 10-residue-substituted mutants were constructed which were expected to have the same amino acid residues as bR with respect to the retinal binding site. In spite of the amino acid arrangement around the chromophore being the same as that of bR, the red shift from the original ppR was not large (lambdamax, 524 nm for the 10-substituted mutant), suggesting that the shape of the retinal binding site in ppR differs from that in bR, and that other structural factors are more important for the difference of lambdamax between the two than the specific set of residues in the retinal binding pocket. High resolution structures by X-ray or cryo-electron crystallography [66, 67] may be needed to further analyze the color tuning.
FTIR [32, 50] and resonance Raman spectroscopy [68] showed that frequency derived from the C-C stretch of the polyene chain in ppR does not differ from that of bR. Therefore, the difference of the structure around the chromophore between ppR and bR may originate from the environment near the beta-ionone ring [32]. Furthermore, the hydrogen bond between the Schiff base and its counter-ion is stronger than that in bR. Another spectroscopic difference of ppR or pR from the other three is the existence of a shoulder in the absorbance spectrum. The origin of the shoulder was proposed by Takahashi et al. [62] to be vibrational fine structure due to the fixation of the retinal within the binding site. The beta-ionone ring was suggested to be fixed [32]. This is supported by reconstitution experiments with the retinal analog described above.
FURTHER UNSOLVED PROBLEMS
As described above, there are several unsolved questions.
1. The molecular mechanism of the photo-induced proton transport of ppR is unknown. In bR, the proton releasing group is tentatively identified as a complex of residues including Glu204, Glu194 and water molecules. What is the proton releasing group of ppR? To investigate this, we are preparing mutants whose dissociable amino acids are replaced and their proton pumping activities are going to be measured. Also, FTIR study of these mutants may be necessary to check the existence of hydrogen bonding networks or the presence of functional water within the protein.
2. How can ppR transmit signals to the transducer? On this question, Engelhard and his group published an interesting paper using EPR (electron paramagnetic resonance) [59]. They showed that similar to bR, helix F and G of ppR moves on illumination. This conformational change might be transmitted to the transducer as a signal as was suggested by Spudich [61]. Sudo et al. [69] showed that ppR binds to its truncated transducer even in the presence of a detergent, DM with a 1 : 1 stoichiometry.
3. How do the proton-transfer reactions contribute to the helix movement and transducer activation? Is the proton-transport a side effect? Or does this proton movement induce the helix movement?
4. Why is lambdamax of ppR blue-shifted? As described above, for elucidation of the color regulation, the structure, especially that of the retinal binding pocket is necessary. Spudich et al. [66] and Kunji et al. [67] succeeded in analyzing the structure, which will give an important clue to solve the mechanism of color regulation. However, their resolution was 6.9 Å, and a structure with a higher resolution might be necessary.
5. Four archaeal rhodopsins have similar structures. Seven helices constitute transmembrane portion of the protein, and a retinal chromophore is bound to a lysine residue of the seventh helix via a protonated Schiff base linkage. How are these archaeal rhodopsins differentiated into ion pumps and sensors? What are the molecular mechanisms for this differentiation?
We thank Drs. J. Hirayama, Y. Imamoto and Prof. Y. Shichida who were coauthors when our investigation of ppR was started. We also thank Drs. T. Takahashi and H. Tomioka who contributed greatly for the discovery of pR in Halobacterium salinarum.
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