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

Koji Kato,Fusamichi Akita,Naoshi Dohmae,Suleyman I Allakhverdiev,Seiji Akimoto,Ryo Nagao,Takehiro Suzuki,Min Chen,Jian-Ren Shen,Tatsuya Tomo,Naoyuki Miyazaki,Toshiyuki Shinoda

doi:10.1038/s41467-019-13898-5

Abstract

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.

Highlights

Chlorophylls (Chl) play pivotal roles in energy capture, transfer and charge separation in photosynthesis
Some cyanobacteria have been found to undergo extensive remodeling regarding the expression of some photosynthetic genes upon transfer from white light to far-red light, which is accompanied by the synthesis of Chl f and its incorporation and functioning in the photosystems[3,4,5,21,22,23,24,29,31]
These subunits were not resolved in the cryo-electron microscopy (cryo-EM) structure of both white and farred photosystem I (PSI), owing to either weak densities or almost absence of their densities

Summary

Introduction

Chlorophylls (Chl) play pivotal roles in energy capture, transfer and charge separation in photosynthesis. 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. Chls b and c are associated with the antennas but not the photosystem cores in different lineages of organisms These Chl variations are important for adaptation of oxyphototrophs to various living environments, leading to the acquisition of every ecological niche[1]. During FaRLiP, cells synthesize Chl f and extensively remodel their photosynthetic apparatus by changing the expressions of core subunits of PSI, PSII, and the phycobilisome This switch allows cyanobacteria to grow under far-red light, and the Chl f synthase has been found to be located in the FaRLiP gene cluster[23]. Combining with our previous functional analyses[20,27,28], we conclude that Chl f functions in enhancing excitation energy transfer to the RC Chls rather than being involved in the ETC directly

Methods

Results

Conclusion