Alternating syn-anti bacteriochlorophylls form concentric helical nanotubes in chlorosomes

Swapna Ganapathy, Gert T. Oostergetel, Piotr K. Wawrzyniak, Michael Reus, Aline Gomez Maqueo Chew, Francesco Buda, Egbert J. Boekema, Donald A. Bryant, Alfred R. Holzwarth, Huub J.M. De Groot

Research output: Contribution to journalArticle

203 Citations (Scopus)

Abstract

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 resolvehowthe 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, solidstate 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 π-π 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.

Original languageEnglish (US)
Pages (from-to)8525-8530
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume106
Issue number21
DOIs
StatePublished - May 26 2009

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Bacteriochlorophylls
Nanotubes
Light
Chlorobi
Organelles
bacteriochlorophyll d
bacteriochlorophyll c
LDS 751

All Science Journal Classification (ASJC) codes

  • General

Cite this

Ganapathy, S., Oostergetel, G. T., Wawrzyniak, P. K., Reus, M., Chew, A. G. M., Buda, F., ... De Groot, H. J. M. (2009). Alternating syn-anti bacteriochlorophylls form concentric helical nanotubes in chlorosomes. Proceedings of the National Academy of Sciences of the United States of America, 106(21), 8525-8530. https://doi.org/10.1073/pnas.0903534106
Ganapathy, Swapna ; Oostergetel, Gert T. ; Wawrzyniak, Piotr K. ; Reus, Michael ; Chew, Aline Gomez Maqueo ; Buda, Francesco ; Boekema, Egbert J. ; Bryant, Donald A. ; Holzwarth, Alfred R. ; De Groot, Huub J.M. / Alternating syn-anti bacteriochlorophylls form concentric helical nanotubes in chlorosomes. In: Proceedings of the National Academy of Sciences of the United States of America. 2009 ; Vol. 106, No. 21. pp. 8525-8530.
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Ganapathy, S, Oostergetel, GT, Wawrzyniak, PK, Reus, M, Chew, AGM, Buda, F, Boekema, EJ, Bryant, DA, Holzwarth, AR & De Groot, HJM 2009, 'Alternating syn-anti bacteriochlorophylls form concentric helical nanotubes in chlorosomes', Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 21, pp. 8525-8530. https://doi.org/10.1073/pnas.0903534106

Alternating syn-anti bacteriochlorophylls form concentric helical nanotubes in chlorosomes. / Ganapathy, Swapna; Oostergetel, Gert T.; Wawrzyniak, Piotr K.; Reus, Michael; Chew, Aline Gomez Maqueo; Buda, Francesco; Boekema, Egbert J.; Bryant, Donald A.; Holzwarth, Alfred R.; De Groot, Huub J.M.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 106, No. 21, 26.05.2009, p. 8525-8530.

Research output: Contribution to journalArticle

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T1 - Alternating syn-anti bacteriochlorophylls form concentric helical nanotubes in chlorosomes

AU - Ganapathy, Swapna

AU - Oostergetel, Gert T.

AU - Wawrzyniak, Piotr K.

AU - Reus, Michael

AU - Chew, Aline Gomez Maqueo

AU - Buda, Francesco

AU - Boekema, Egbert J.

AU - Bryant, Donald A.

AU - Holzwarth, Alfred R.

AU - De Groot, Huub J.M.

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Y1 - 2009/5/26

N2 - 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 resolvehowthe 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, solidstate 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 π-π 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.

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