Photosynthetic organisms have adapted to survive a myriad of extreme environments from the earth’s deserts to its poles, yet the proteins that carry out the light reactions of photosynthesis are highly conserved from the cyanobacteria to modern day crops. To investigate adaptations of the photosynthetic machinery in cyanobacteria to excessive light stress, we isolated a new strain of cyanobacteria, Cyanobacterium aponinum 0216, from the extreme light environment of the Sonoran Desert. Here we report the biochemical characterization and the 2.7 Å resolution structure of trimeric photosystem I from this high-light-tolerant cyanobacterium. The structure shows a new conformation of the PsaL C-terminus that supports trimer formation of cyanobacterial photosystem I. The spectroscopic analysis of this photosystem I revealed a decrease in far-red absorption, which is attributed to a decrease in the number of long- wavelength chlorophylls. Using these findings, we constructed two chimeric PSIs in Synechocystis sp. PCC 6803 demonstrating how unique structural features in photosynthetic complexes can change spectroscopic properties, allowing organisms to thrive under different environmental stresses.

Photosynthetic pigment–protein complexes control local chlorophyll (Chl) transition frequencies through a variety of electrostatic and steric forces. Site-directed mutations can modify this local spectroscopic tuning, providing critical insight into native photosynthetic functions and offering the tantalizing prospect of creating rationally designed Chl proteins with customized optical properties. Unfortunately, at present, no proven methods exist for reliably predicting mutation-induced frequency shifts in advance, limiting the method’s utility for quantitative applications. Here, we address this challenge by constructing a series of point mutants in the water-soluble chlorophyll protein of Lepidium virginicum and using them to test the reliability of a simple computational protocol for mutation-induced site energy shifts. The protocol uses molecular dynamics to prepare mutant protein structures and the charge density coupling model of Adolphs et al. [Photosynth. Res. 95, 197–209 (2008)] for site energy prediction; a graphical interface that implements the protocol automatically is published online at http://nanohub.org/tools/pigmenthunter. With the exception of a single outlier (presumably due to unexpected structural changes), we find that the calculated frequency shifts match the experiment remarkably well, with an average error of 1.6 nm over a 9 nm spread in wavelengths. We anticipate that the accuracy of the method can be improved in the future with more advanced sampling of mutant protein structures.

Low temperature photoluminescence spectroscopy (PL) revealed a change in vibrational coupling of mutated Water soluble chlorophyll binding protein complexes (WSCPs) with Chlorophyll a. Pigment-protein systems can adjust the range of absorbed wavelengths according to living conditions. However, the mechanism of spectral tuning is unclear. A study of point mutations in the Q57 site of the Lepidium virginicum (Lv) WSCP is expected to shed light on how hydrogen bonds and electrostatic interactions influence the emission spectrum of Chlorophyll a (Chl a) bound to WSCP. Steady state PL revealed the change of the electron-phonon coupling strength within the mutants at 7 K. Time-resolved (TR) PL detected the difference in the lifetimes of the WSCP mutants at 7 K. Both PL and TRPL results cannot be ascribed to the charge difference in the Q57 site of Lv WSCP alone. The influence of hydrogen bonding together with electrostatic interactions and geometry changes should be considered to correctly describe the mechanism of tuning of vibrational coupling in WSCP bound with Chl a complex.

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