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Carotenoid S(1) state in a recombinant light-harvesting complex of Photosystem II.

Polivka, Tomas LU ; Zigmantas, Donatas LU ; Sundström, Villy LU ; Formaggio, Elena; Cinque, Gianfelice and Bassi, Roberto (2002) In Biochemistry 41(2). p.439-450
Abstract
The carotenoid species lutein, violaxanthin, and zeaxanthin are crucial in the xanthophyll-dependent nonphotochemical quenching occurring in photosynthetic systems of higher plants, since they are involved in dissipation of excess energy and thus protect the photosynthetic machinery from irreversible inhibition. Nonetheless, important properties of the xanthophyll cycle carotenoids, such as the energy of their S(1) electronic states, are difficult to study and were only recently determined in organic solvents [Polívka, T. (1999) Proc. Natl. Acad. Sci. U.S.A. 96, 4914. Frank, H. A. (2000) Biochemistry 39, 2831]. In the present study, we have determined the S(1) energies of three carotenoid species, violaxanthin, lutein, and zeaxanthin, in... (More)
The carotenoid species lutein, violaxanthin, and zeaxanthin are crucial in the xanthophyll-dependent nonphotochemical quenching occurring in photosynthetic systems of higher plants, since they are involved in dissipation of excess energy and thus protect the photosynthetic machinery from irreversible inhibition. Nonetheless, important properties of the xanthophyll cycle carotenoids, such as the energy of their S(1) electronic states, are difficult to study and were only recently determined in organic solvents [Polívka, T. (1999) Proc. Natl. Acad. Sci. U.S.A. 96, 4914. Frank, H. A. (2000) Biochemistry 39, 2831]. In the present study, we have determined the S(1) energies of three carotenoid species, violaxanthin, lutein, and zeaxanthin, in their LHCII (peripheral light-harvesting complex of photosystem II) protein environment by constructing recombinant Lhcb1 (Lhc = light-harvesting complex) proteins containing single carotenoid species. Within experimental error the S(1) energy is the same for all three carotenoids in the monomeric LHCII, 13,900 +/- 300 cm(-1) (720 +/- 15 nm), thus well below the Q(y)() transitions of chlorophylls. In addition, we have found that, although the S(1) lifetimes of violaxanthin, lutein, and zeaxanthin differ substantially in solution, when incorporated into the LHCII protein, their S(1) states have in fact the same lifetime of about 11 ps. Despite the similar spectroscopic properties of the carotenoids bound to the LHCII, we observed a maximal fluorescence quenching when zeaxanthin was present in the LHCII complex. On the basis of these observations, we suggest that, rather than different photochemical properties of individual carotenoid species, changes in the protein conformation induced by binding of carotenoids with distinct molecular structures are involved in the quenching phenomena associated with Lhc proteins. (Less)
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author
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Kinetics, Light, Lutein : chemistry, Photosynthetic Reaction Center Plant, Recombinant Proteins : chemistry : metabolism, Spectrometry Fluorescence, Support Non-U.S. Gov't, Spectrophotometry, beta Carotene : analogs & derivatives : chemistry, Time Factors, Electrophysiology, Carotenoids : chemistry
in
Biochemistry
volume
41
issue
2
pages
439 - 450
publisher
The American Chemical Society
external identifiers
  • wos:000173216700002
  • pmid:11781082
  • scopus:0037080012
ISSN
0006-2960
DOI
10.1021/bi011589x
language
English
LU publication?
yes
id
2aa88c9a-5d8b-4dcd-a22d-71edf00cea34 (old id 106822)
date added to LUP
2007-07-03 15:57:04
date last changed
2017-12-10 03:44:38
@article{2aa88c9a-5d8b-4dcd-a22d-71edf00cea34,
  abstract     = {The carotenoid species lutein, violaxanthin, and zeaxanthin are crucial in the xanthophyll-dependent nonphotochemical quenching occurring in photosynthetic systems of higher plants, since they are involved in dissipation of excess energy and thus protect the photosynthetic machinery from irreversible inhibition. Nonetheless, important properties of the xanthophyll cycle carotenoids, such as the energy of their S(1) electronic states, are difficult to study and were only recently determined in organic solvents [Polívka, T. (1999) Proc. Natl. Acad. Sci. U.S.A. 96, 4914. Frank, H. A. (2000) Biochemistry 39, 2831]. In the present study, we have determined the S(1) energies of three carotenoid species, violaxanthin, lutein, and zeaxanthin, in their LHCII (peripheral light-harvesting complex of photosystem II) protein environment by constructing recombinant Lhcb1 (Lhc = light-harvesting complex) proteins containing single carotenoid species. Within experimental error the S(1) energy is the same for all three carotenoids in the monomeric LHCII, 13,900 +/- 300 cm(-1) (720 +/- 15 nm), thus well below the Q(y)() transitions of chlorophylls. In addition, we have found that, although the S(1) lifetimes of violaxanthin, lutein, and zeaxanthin differ substantially in solution, when incorporated into the LHCII protein, their S(1) states have in fact the same lifetime of about 11 ps. Despite the similar spectroscopic properties of the carotenoids bound to the LHCII, we observed a maximal fluorescence quenching when zeaxanthin was present in the LHCII complex. On the basis of these observations, we suggest that, rather than different photochemical properties of individual carotenoid species, changes in the protein conformation induced by binding of carotenoids with distinct molecular structures are involved in the quenching phenomena associated with Lhc proteins.},
  author       = {Polivka, Tomas and Zigmantas, Donatas and Sundström, Villy and Formaggio, Elena and Cinque, Gianfelice and Bassi, Roberto},
  issn         = {0006-2960},
  keyword      = {Kinetics,Light,Lutein : chemistry,Photosynthetic Reaction Center Plant,Recombinant Proteins : chemistry : metabolism,Spectrometry Fluorescence,Support Non-U.S. Gov't,Spectrophotometry,beta Carotene : analogs & derivatives : chemistry,Time Factors,Electrophysiology,Carotenoids : chemistry},
  language     = {eng},
  number       = {2},
  pages        = {439--450},
  publisher    = {The American Chemical Society},
  series       = {Biochemistry},
  title        = {Carotenoid S(1) state in a recombinant light-harvesting complex of Photosystem II.},
  url          = {http://dx.doi.org/10.1021/bi011589x},
  volume       = {41},
  year         = {2002},
}