The origin of the red shift of the absorption spectra of aggregated chlorophylls

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The role of a special dimer (D) of bacteriochlorophyll molecules in bacterial photosynthesis was examined by calculations of the rates of electron transfer reactions in a system of the dimer and a bacteriopheophytin (BPh) molecule. It was found that the dependence of the potential surfaces of D on the distance between the monomers allows a fast lightinduced electron transfer from D to BPh but only a slow back reaction (reduction of D+ by BPhf) The same potential surfaces allow efficient reduction of D+ by cytochrome c. Possible advantages of greatly different values of the electronic matrix elements for. the forward and back reactions are pointed out. It is suggested that the electrostatic interaction between D+ and an ionized group of the protein might play an important role in the photosynthetic reaction.The first step in bacterial photosynthesis involves absorption of light by a special dimer (D) of bacteriochlorophyll (BChl) molecules and transfer of an electron from the excited dimer (D*) to a primary acceptor (I), probably a bacteriopheophytin (BPh) molecule, to form the system D+I-. The electron is then transferred to a secondary acceptor, Q, and D+ is reduced by cytochrome c (C) (for recent views see refs. 1 and 2). The measured rates of the various competing processes involved in these reactions (2) provide a kinetic description of an extremely efficient system (see Fig. 1). The excited dimer ejects an electron before its deactivation by radiative and radiationless processes, while the back reaction, D+I--DI, is blocked so that it does not compete with electron transfer from I-to Q. This kinetic information does not reveal the molecular basis of the photosynthetic reaction and does not explain why nature chose a dimer as the primary acceptor.This work examines the role of the special dimer by model calculations of the rate of light-induced electron transfer from the BChl dimer to a BPh molecule. The calculations indicate that the weak noncovalent bond between the two BChl monomers provides an efficient "trap" for the excitation energy and may account for the rate difference between the forward and back reactions. The possible role of the electrostatic interaction between the dimer and an ionized group of the protein is also considered. It is pointed out that such interaction may slow the back reaction by polarizing D+ and shifting the center of positive charge further from 1-. Theoretical treatment of electron transfer reactions The theory of electron transfer processes (3-6) is illustrated in Fig. 2. The figure describes the potential surfaces of the combined donor, A, and acceptor, B. system. In the quadratic approximation the potential surfaces of the reactants AB (V1) and the products A+B-(V2) can be represented by: where v and A are, respectively, the average vibration frequencies (in cm'1) and origin shifts of the dimensionless normal cordinates Q[Q = (47r2v/h)I/2q, where q is the massscaled Cartesian normal mode]. In the high temperature limit, when the thermal energy is larger than hcT,...

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confidence: 58%

Section: Discussionmentioning

confidence: 99%

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Role of the chlorophyll dimer in bacterial photosynthesis

Warshel

1980

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“…One mechanism for the in vivo red shifts that has only recently been considered involves electrostatic interactions between bound Chl and charged amino acids on the protein (8,9). A rationale for this suggestion is the recent demonstration that charged amino acids are responsible for the 2,700-cm-1 red shift involved in the formation of bovine rhodopsin (10) and the 5,000-cm-1 red shift involved in the formation of bacteriorhodopsin (11).…”

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confidence: 99%

Charged amino acids as spectroscopic determinants for chlorophyll in vivo

Eccles

Honig

1983

112

In this paper we propose that the large spectroscopic red shifts observed for chlorophyll (Chl) and bacteriochlorophyll (BChl) in vivo may be due to charged amino acids in the binding site. Molecular orbital calculations of the transition energies of Chl in the field of external charges are carried out. The calculated wavelength shifts induced by these charges are comparable in magnitude to those observed in vivo. Moreover the size of the shifts increases in the order BChl b > BChl a > Chl a, which is the observed trend. The ability of the calculations to account for both the absolute and relative magnitudes of the wavelength shifts argues for the validity of the model. Further indirect support comes from the recent demonstration that charged amino acids are responsible for the colors of visual pigments and bacteriorhodopsin. In addition to their effects on spectra the presence of external charges induces large changes in the ionization potential of Chl molecules and thus might explain the in vivo alteration of the oxidation potentials in reaction centers.The difference between the properties of chlorophyll (Chl) molecules in solution and identical molecules in vivo has been a subject of great interest, extensive investigation, and much conjecture. It is clear that its local environment endows Chl in vivo with special physical and chemical properties, yet little is known about the nature of the interactions that produce these effects. Because it now appears that most if not all of the Chl in photosynthetic systems is intimately associated with proteins (1), it seems appropriate to consider how specific amino acids might affect the behavior of bound Chl. Properties that are strongly influenced by the protein environment include redox potentials, photochemically induced electron transfer, and absorption maxima. Of these, the latter are easiest to characterize and interpret because spectroscopic transition energies for conjugated systems may be calculated theoretically with considerable accuracy.Chl in vivo and in isolated lipoprotein complexes absorbs light at longer wavelengths than does monomeric Chl in simple organic solvents (2). The magnitude of the shift varies considerably among species and somewhat less for different pigments within a single organism (comparing, for example, reaction center with antenna Chl). In green plants the magnitude of the wavelength shift is between 300 and 800 cm-'. In the case of photosynthetic bacteria the shifts are often much larger, reaching 1,500 cm-' for bacteriochlorophyll (BChl) a-containing species and as much as 2,700 cm-1 for the antenna complex of the BChl b-containing species Rhodopseudomnonas (Rps.) viridis (2).Although the origin of these shifts is a question of some interest in its own right, its more general relevance owes to the possibility that the shift is due to highly specific and functionally important Chl-protein interactions. Thus, identifying the source of the large in vivo red shifts may be an important step in elucidating the mechanism of elec...

“…The red shifts of these BCh1 a-protein complexes (as well as similar shifts in chlorophyll a-protein complexes) are as yet only partly understood and subject to much theoretical, spectroscopic, and synthetic work. They have been related to aggregation (5)(6)(7)(8)(9)(10)(11)(12)(13)(14) or hydration (or both) (5,6,(12)(13)(14)(15), enolization of the chlorophyll groups (16)(17)(18)(19), point charges in their environment (20), and charge-transfer complexes (21). In particular, the primary donor P870 in BChl a-containing reaction centers has been suggested to be a "special pair" of BChl a, with their exact relationship still under discussion (22)(23)(24)(25)(26)(27).…”

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confidence: 99%

Long-wavelength-absorbing forms of bacteriochlorophyll a in solutions of Triton X-100

Gottstein

Scheer

1983

At least three forms of Triton X-100-solubilized bacteriochlorophyll a (BChI a) have been characterized by UV/ visible/near-IR absorption and CD spectra. One, absorbing at 770 nm, is similar to a monomeric solution in methanol. The two others have strongly red-shifted absorption peaks (860 nm and 930, 835 nm) and intense and complex CD bands in this region, indicative of strong interaction of at least two and three molecules of BChl a, respectively.Triton X-100 (II, m = 9 or 10) is next to dodecyldimethylamineoxide the most commonly used detergent for the isolation of bacterial reaction center and light-harvesting complexes.The understanding of bacterial photosynthesis has greatly advanced with the isolation and characterization of well-defined complexes of bacteriochlorophyll a (BChl a, I) with proteins ( (Fig. 2). The red shifts of these BCh1 a-protein complexes (as well as similar shifts in chlorophyll a-protein complexes) are as yet only partly understood and subject to much theoretical, spectroscopic, and synthetic work. They have been related to aggregation (5-14) or hydration (or both) (5,6,(12)(13)(14)(15), enolization of the chlorophyll groups (16)(17)(18)(19), point charges in their environment (20), and charge-transfer complexes (21). In particular, the primary donor P870 in BChl a-containing reaction centers has been suggested to be a "special pair" of BChl a, with their exact relationship still under discussion (22-27). IIWe noticed, during the isolation of reaction centers from Rhodospirillum rubrum G9 and Rhodopseudmownas spheroides R26 with Triton X-100, fractions that looked superficially like reaction centers contaminated with solubilized BChl a and bacteriopheophytin a. The 805-nm band was, however, small or even absent, and the 870-nm band was somewhat blue shifted and did not show any reversible bleaching. By systematic solubilization studies of BCh1 a with detergents, we have now shown that Triton X-100 induces strongly red-shifted absorption peaks in solubilized BChl a, with maxima around 830, 860, and 930 nm, and we here present our results on the BChl a species present in these solutions. EXPERIMENTALRs. rubrum G9 and Rp. spheroides R26 were grown in Hutner's medium (28) at 270C. BChl a was isolated by a modification of the method of Sato and Murata (29), which principally involves solvent extraction, precipitation of BChl a as a dioxane complex (30), and chromatography on DEAE-cellulose (29). The chromatography was alternatively also done on sugar columns (30). Triton X-100 was purchased from Serva (Heidelberg, Federal Republic of Germany) and used as received. All solvents were distilled or purified over alumina (Woelm, Eschwege, Federal Republic of Germany) prior to use. UV/visible/near-IR absorption spectra were recorded on a DMR 22 (Zeiss, Toberkochen, Federal Republic of Germany) spectrophotometer equipped for cross-illumination with suitable interference and cutoff filters. CD spectra were recorded with a dichrograph Mark V (Yvon-Jobin, Longjumeau, France) equipped w...