Chlorophylls (Chl) play pivotal roles in energy capture, transfer and charge separation in photosynthesis. Among Chls functioning in oxygenic photosynthesis, Chl f is the most red-shifted type first found in a cyanobacterium Halomicronema hongdechloris. The location and function of Chl f in photosystems are not clear. Here we analyzed the high-resolution structures of photosystem I (PSI) core from H. hongdechloris grown under white or far-red light by cryo-electron microscopy. The structure showed that, far-red PSI binds 83 Chl a and 7 Chl f, and Chl f are associated at the periphery of PSI but not in the electron transfer chain. The appearance of Chl f is well correlated with the expression of PSI genes induced under far-red light. These results indicate that Chl f functions to harvest the far-red light and enhance uphill energy transfer, and changes in the gene sequences are essential for the binding of Chl f.

/pdf/structural-basis-for-the-adaptation-and-function-of-3jiloqcuua.pdf

Structural basis for the adaptation and function of chlorophyll f in photosystem I

Phototrophic organisms are superbly adapted to different light environments but often must acclimate to challenging competition for visible light wavelengths in their niches. Some cyanobacteria overcome this challenge by expressing paralogous photosynthetic proteins and by synthesizing and incorporating ~8% chlorophyll f into their Photosystem I (PSI) complexes, enabling them to grow under far-red light (FRL). We solved the structure of FRL-acclimated PSI from the cyanobacterium Fischerella thermalis PCC 7521 by single-particle, cryo-electron microscopy to understand its structural and functional differences. Four binding sites occupied by chlorophyll f are proposed. Subtle structural changes enable FRL-adapted PSI to extend light utilization for oxygenic photosynthesis to nearly 800 nm. This structure provides a platform for understanding FRL-driven photosynthesis and illustrates the robustness of adaptive and acclimation mechanisms in nature.

https://advances.sciencemag.org/content/advances/6/6/eaay6415.full.pdf

The structure of Photosystem I acclimated to far-red light illuminates an ecologically important acclimation process in photosynthesis

Evidence that chlorophyll f functions solely as an antenna pigment in far-red-light photosystem I from Fischerella thermalis PCC 7521

Plants and cyanobacteria use the chlorophylls embedded in their photosystems to absorb photons and perform charge separation, the first step of converting solar energy to chemical energy. While oxygenic photosynthesis is primarily based on chlorophyll a photochemistry, which is powered by red light, a few cyanobacterial species can harness less energetic photons when growing in far-red light. Acclimatization to far-red light involves the incorporation of a small number of molecules of red-shifted chlorophyll f in the photosystems, whereas the most abundant pigment remains chlorophyll a. Due to its different energetics, chlorophyll f is expected to alter the excited-state dynamics of the photosynthetic units and, ultimately, their performances. Here we combined time-resolved fluorescence measurements on intact cells and isolated complexes to show that chlorophyll f insertion slows down the overall energy trapping in both photosystems. While this marginally affects the efficiency of photosystem I, it substantially decreases that of photosystem II. Nevertheless, we show that despite the lower energy output, the insertion of red-shifted chlorophylls in the photosystems remains advantageous in environments that are enriched in far-red light and therefore represents a viable strategy for extending the photosynthetically active spectrum in other organisms, including plants. However, careful design of the new photosynthetic units will be required to preserve their efficiency.

Far-red absorption and light-use efficiency trade-offs in chlorophyll f photosynthesis

The accurate assignment of cofactors in cryo-electron microscopy maps is crucial in determining protein function. This is particularly true for chlorophylls (Chls), for which small structural differences lead to important functional differences. Recent cryo-electron microscopy structures of Chl-containing protein complexes exemplify the difficulties in distinguishing Chl b and Chl f from Chl a. We use these structures as examples to discuss general issues arising from local resolution differences, properties of electrostatic potential maps, and the chemical environment which must be considered to make accurate assignments. We offer suggestions for how to improve the reliability of such assignments. In this Perspective, Christopher Gisriel et al. discuss the challenges in accurate assignment of co-factors in cryo-EM, particularly for chlorophylls. They explore the factors that lead to misassignment and offer suggestions for improving reliability of cryo-EM-based assignments.

/pdf/opportunities-and-challenges-for-assigning-cofactors-in-cryo-5z13si7hy4.pdf

Opportunities and challenges for assigning cofactors in cryo-EM density maps of chlorophyll-containing proteins.

Quinones in the A1 binding site in photosystem I studied using time-resolved FTIR difference spectroscopy.

Fourier transform visible and infrared difference spectroscopy for the study of P700 in photosystem I from Fischerella thermalis PCC 7521 cells grown under white light and far-red light: Evidence that the A -1 cofactor is chlorophyll f

Leyla Rohani

Papers

Quinones in the A1 binding site in photosystem I studied using time-resolved FTIR difference spectroscopy.

Fourier transform visible and infrared difference spectroscopy for the study of P700 in photosystem I from Fischerella thermalis PCC 7521 cells grown under white light and far-red light: Evidence that the A -1 cofactor is chlorophyll f

Calculated vibrational properties of semiquinones in the A1 binding site in photosystem I.

Experimental and Calculated Infrared Spectra of Disubstituted Naphthoquinones

Assessment of the orientation and conformation of pigments in protein binding sites from infrared difference spectra.