Photosynthetic Vesicle Architecture and Constraints on Efficient Energy Harvesting

Overview

Journal Biophys J

Publisher Cell Press

Specialty Biophysics

Date 2010 Jul 27

PMID 20655834

Citations 22

Authors

Melih Sener

Johan Strumpfer

John A Timney

Arvi Freiberg

C Neil Hunter

Klaus Schulten

Affiliations

Soon will be listed here.

Abstract

Photosynthetic chromatophore vesicles found in some purple bacteria constitute one of the simplest light-harvesting systems in nature. The overall architecture of chromatophore vesicles and the structural integration of vesicle function remain poorly understood despite structural information being available on individual constituent proteins. An all-atom structural model for an entire chromatophore vesicle is presented, which improves upon earlier models by taking into account the stoichiometry of core and antenna complexes determined by the absorption spectrum of intact vesicles in Rhodobacter sphaeroides, as well as the well-established curvature-inducing properties of the dimeric core complex. The absorption spectrum of low-light-adapted vesicles is shown to correspond to a light-harvesting-complex 2 to reaction center ratio of 3:1. A structural model for a vesicle consistent with this stoichiometry is developed and used in the computation of excitonic properties. Considered also is the packing density of antenna and core complexes that is high enough for efficient energy transfer and low enough for quinone diffusion from reaction centers to cytochrome bc(1) complexes.

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References

Koepke J, Hu X, Muenke C, Schulten K, Michel H . The crystal structure of the light-harvesting complex II (B800-850) from Rhodospirillum molischianum. Structure. 1996; 4(5):581-97. DOI: 10.1016/s0969-2126(96)00063-9. View

Xiong J, FISCHER W, Inoue K, Nakahara M, Bauer C . Molecular evidence for the early evolution of photosynthesis. Science. 2000; 289(5485):1724-30. DOI: 10.1126/science.289.5485.1724. View

Noy D . Natural photosystems from an engineer's perspective: length, time, and energy scales of charge and energy transfer. Photosynth Res. 2007; 95(1):23-35. DOI: 10.1007/s11120-007-9269-7. View

Scheuring S, Sturgis J . Dynamics and diffusion in photosynthetic membranes from rhodospirillum photometricum. Biophys J. 2006; 91(10):3707-17. PMC: 1630482. DOI: 10.1529/biophysj.106.083709. View

Sener M, Schulten K . General random matrix approach to account for the effect of static disorder on the spectral properties of light harvesting systems. Phys Rev E Stat Nonlin Soft Matter Phys. 2002; 65(3 Pt 1):031916. DOI: 10.1103/PhysRevE.65.031916. View

Emerson R, Arnold W . THE PHOTOCHEMICAL REACTION IN PHOTOSYNTHESIS. J Gen Physiol. 2009; 16(2):191-205. PMC: 2141200. DOI: 10.1085/jgp.16.2.191. View

Frese R, Siebert C, Niederman R, Hunter C, Otto C, van Grondelle R . The long-range organization of a native photosynthetic membrane. Proc Natl Acad Sci U S A. 2004; 101(52):17994-9. PMC: 539794. DOI: 10.1073/pnas.0407295102. View

Jamieson S, Wang P, Qian P, Kirkland J, Conroy M, Hunter C . Projection structure of the photosynthetic reaction centre-antenna complex of Rhodospirillum rubrum at 8.5 A resolution. EMBO J. 2002; 21(15):3927-35. PMC: 125403. DOI: 10.1093/emboj/cdf410. View

Bahatyrova S, Frese R, Siebert C, Olsen J, van der Werf K, van Grondelle R . The native architecture of a photosynthetic membrane. Nature. 2004; 430(7003):1058-62. DOI: 10.1038/nature02823. View

10.

Scheuring S, Goncalves R, Prima V, Sturgis J . The photosynthetic apparatus of Rhodopseudomonas palustris: structures and organization. J Mol Biol. 2006; 358(1):83-96. DOI: 10.1016/j.jmb.2006.01.085. View

11.

Xia D, Yu C, Kim H, Xia J, Kachurin A, Zhang L . Crystal structure of the cytochrome bc1 complex from bovine heart mitochondria. Science. 1997; 277(5322):60-6. DOI: 10.1126/science.277.5322.60. View

12.

Arnold W, Oppenheimer J . Internal conversion in the photosynthetic mechanism of blue-green algae. J Gen Physiol. 1950; 33(4):423-35. PMC: 2147196. DOI: 10.1085/jgp.33.4.423. View

13.

Freiberg A, Allen J, Williams J, Woodbury N . Energy trapping and detrapping by wild type and mutant reaction centers of purple non-sulfur bacteria. Photosynth Res. 2013; 48(1-2):309-19. DOI: 10.1007/BF00041022. View

14.

Allen J, Feher G, Yeates T, Komiya H, Rees D . Structure of the reaction center from Rhodobacter sphaeroides R-26: the protein subunits. Proc Natl Acad Sci U S A. 1987; 84(17):6162-6. PMC: 299029. DOI: 10.1073/pnas.84.17.6162. View

15.

Frese R, Olsen J, Branvall R, Westerhuis W, Hunter C, van Grondelle R . The long-range supraorganization of the bacterial photosynthetic unit: A key role for PufX. Proc Natl Acad Sci U S A. 2000; 97(10):5197-202. PMC: 25805. DOI: 10.1073/pnas.090083797. View

16.

Karrasch S, Bullough P, Ghosh R . The 8.5 A projection map of the light-harvesting complex I from Rhodospirillum rubrum reveals a ring composed of 16 subunits. EMBO J. 1995; 14(4):631-8. PMC: 398126. DOI: 10.1002/j.1460-2075.1995.tb07041.x. View

17.

Strumpfer J, Schulten K . Light harvesting complex II B850 excitation dynamics. J Chem Phys. 2009; 131(22):225101. PMC: 2802260. DOI: 10.1063/1.3271348. View

18.

Scheuring S, Sturgis J, Prima V, Bernadac A, Levy D, Rigaud J . Watching the photosynthetic apparatus in native membranes. Proc Natl Acad Sci U S A. 2004; 101(31):11293-7. PMC: 509197. DOI: 10.1073/pnas.0404350101. View

19.

Monger T, Parson W . Singlet-triplet fusion in Rhodopseudomonas sphaeroides chromatophores. A probe of the organization of the photosynthetic apparatus. Biochim Biophys Acta. 1977; 460(3):393-407. DOI: 10.1016/0005-2728(77)90080-9. View

20.

Tucker J, Siebert C, Escalante M, Adams P, Olsen J, Otto C . Membrane invagination in Rhodobacter sphaeroides is initiated at curved regions of the cytoplasmic membrane, then forms both budded and fully detached spherical vesicles. Mol Microbiol. 2010; 76(4):833-47. DOI: 10.1111/j.1365-2958.2010.07153.x. View