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Chemically identical chlorophyll (Chl) molecules undergo conformational changes when they are embedded in a protein matrix. The conformational changes will modulate their absorption spectra to meet the need for programmed excitation energy transfer or electron transfer. To interpret spectroscopic data using the knowledge of pigment–protein interactions requires a single pigment embedded in one polypeptide matrix. Unfortunately, most of the known photosynthetic systems contain a set of multiple pigments in each protein subunit. This makes it complicated to interpret spectroscopic data using structural data due to the potential overlapping spectra of two or more pigments. Chl–protein interactions have not been systematically studied to answer three fundamental questions: (i) What are the structural characteristics and commonly shared substructures of different types of Chl molecules (e.g., Chl a, b, c, d, and f)? (ii) How many structural groups can Chl molecules be divided into and how are different structural groups influenced by their surrounding environments? (iii) What are the structural characteristics of pigment surrounding environments? Having no clear answers to the unresolved questions is probably due to a lack of computational methods for quantifying conformational changes in individual Chls and individual surrounding amino acids. The first version of the Triangular Spatial Relationship (TSR)-based method was developed for comparing protein 3D structures. The input data for the TSR-based method are experimentally determined 3D structures from the Protein Data Bank (PDB). In this study, we take advantage of the 3D structures of Chl-binding proteins deposited in the PDB and the TSR-based method to systematically investigate the 3D structures of various types of Chls and their protein environments. The key contributions of this study can be summarized as follows: (i) Specific structural characteristics of Chl d and f were identified and are defined using the TSR keys. (ii) Two and three clusters were found for various types of Chls and Chls a, respectively. The signature structures for distinguishing their corresponding two and three clusters were identified. (iii) Histidine residues were used as an example for revealing structural characteristics of Chl-binding sites. This study provides evidence for the three unresolved questions and builds a structural foundation through quantifying Chl conformations as well as structures of their embedded protein environments for future mechanistic understanding of relationships between Chl–protein interactions and their corresponding spectroscopic data.
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Energetic robustness to large scale structural fluctuations in a photosynthetic supercomplex
Abstract Photosynthetic organisms transport and convert solar energy with near-unity quantum efficiency using large protein supercomplexes held in flexible membranes. The individual proteins position chlorophylls to tight tolerances considered critical for fast and efficient energy transfer. The variability in protein organization within the supercomplexes, and how efficiency is maintained despite variability, had been unresolved. Here, we report on structural heterogeneity in the 2-MDa cyanobacterial PSI-IsiA photosynthetic supercomplex observed using Cryo-EM, revealing large-scale variances in the positions of IsiA relative to PSI. Single-molecule measurements found efficient IsiA-to-PSI energy transfer across all conformations, along with signatures of transiently decoupled IsiA. Structure based calculations showed that rapid IsiA-to-PSI energy transfer is always maintained, and even increases by three-fold in rare conformations via IsiA-specific chls. We postulate that antennae design mitigates structural fluctuations, providing a mechanism for robust energy transfer in the flexible membrane.
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- Award ID(s):
- 2034021
- PAR ID:
- 10438018
- Publisher / Repository:
- Nature Publishing Group
- Date Published:
- Journal Name:
- Nature Communications
- Volume:
- 14
- Issue:
- 1
- ISSN:
- 2041-1723
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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