Alternating syn-anti bacteriochlorophylls form concentric helical nanotubes in chlorosomes

被引:258
作者
Ganapathy, Swapna [1 ]
Oostergetel, Gert T. [2 ]
Wawrzyniak, Piotr K. [1 ]
Reus, Michael [3 ]
Chew, Aline Gomez Maqueo [4 ]
Buda, Francesco [1 ]
Boekema, Egbert J. [2 ]
Bryant, Donald A. [4 ]
Holzwarth, Alfred R. [3 ]
de Groot, Huub J. M. [1 ]
机构
[1] Leiden Univ, Leiden Inst Chem, NL-2300 RA Leiden, Netherlands
[2] Univ Groningen, Groningen Biomol Sci & Biotechnol Inst, NL-9747 AG Groningen, Netherlands
[3] Max Planck Inst Bioanorgan Chem, D-45470 Mulheim, Germany
[4] Penn State Univ, Dept Biochem & Mol Biol, University Pk, PA 16802 USA
关键词
cryoEM; light-harvesting; photosynthesis; solid-state NMR; supramolecular aggregates; DIPOLAR-CORRELATION SPECTROSCOPY; CHLOROBIUM-TEPIDUM; ENERGY-TRANSFER; CHEMICAL-SHIFTS; GREEN BACTERIA; HIGH-FIELD; ORGANIZATION; LIGHT; AGGREGATION; CONSTRAINTS;
D O I
10.1073/pnas.0903534106
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Chlorosomes are the largest and most efficient light-harvesting antennae found in nature, and they are constructed from hundreds of thousands of self-assembled bacteriochlorophyll (BChl) c, d, or e pigments. Because they form very large and compositionally heterogeneous organelles, they had been the only photosynthetic antenna system for which no detailed structural information was available. In our approach, the structure of a member of the chlorosome class was determined and compared with the wild type (WT) to resolve how the biological light-harvesting function of the chlorosome is established. By constructing a triple mutant, the heterogeneous BChl c pigment composition of chlorosomes of the green sulfur bacteria Chlorobaculum tepidum was simplified to nearly homogeneous BChl d. Computational integration of two different bioimaging techniques, solid-state NMR and cryoEM, revealed an undescribed syn-anti stacking mode and showedhowligated BChl c and d self-assemble into coaxial cylinders to form tubular-shaped elements. A close packing of BChls via pi-pi stacking and helical H-bonding networks present in both the mutant and in the WT forms the basis for ultrafast, long-distance transmission of excitation energy. The structural framework is robust and can accommodate extensive chemical heterogeneity in the BChl side chains for adaptive optimization of the light-harvesting functionality in low-light environments. In addition, syn-anti BChl stacks form sheets that allow for strong exciton overlap in two dimensions enabling triplet exciton formation for efficient photoprotection.
引用
收藏
页码:8525 / 8530
页数:6
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