Identification of a dual orange/far-red and blue light photoreceptor from an oceanic green picoplankton

Yuko Makita,Takashi Gojobori,Kazutoshi Yoshitake,Tomoko Sakami,Keiji Fushimi,Aya Suehisa,Tsuyoshi Watanabe,Masanobu Kawachi,Manami Hirata,Tomoko Kuriyama,Hidefumi Hamasaki,Setsuko Shimada,Masaaki Sakuta,Shigekatsu Suzuki,Emiko Okubo-Kurihara,Yukio Kurihara,Rei Narikawa,Minami Matsui,Haruyo Yamaguchi

doi:10.1038/s41467-021-23741-5

Abstract

Photoreceptors are conserved in green algae to land plants and regulate various developmental stages. In the ocean, blue light penetrates deeper than red light, and blue-light sensing is key to adapting to marine environments. Here, a search for blue-light photoreceptors in the marine metagenome uncover a chimeric gene composed of a phytochrome and a cryptochrome (Dualchrome1, DUC1) in a prasinophyte, Pycnococcus provasolii. DUC1 detects light within the orange/far-red and blue spectra, and acts as a dual photoreceptor. Analyses of its genome reveal the possible mechanisms of light adaptation. Genes for the light-harvesting complex (LHC) are duplicated and transcriptionally regulated under monochromatic orange/blue light, suggesting P. provasolii has acquired environmental adaptability to a wide range of light spectra and intensities.

Highlights

Among the candidate genes identified, we found one with PHY-like sequence at its N-terminal region similar to Arabidopsis phytochrome B (PHYB) (Fig. 1)
PpCRY showed photoconversion from the FADOX-bound form to the FAD–-bound one, and the reverse reaction occurred in the dark. This is similar to the photocycle of dCRY, a photoreceptor for circadian clock regulation in Drosophila melanogaster[14], rather than CraCRY from the green algae Chlamydomonas reinhardtii[15] and AtCRY1 and 2 from the land plant Arabidopsis thaliana[16]. These results suggest that P. provasolii DUC1 (PpDUC1) is a broadband light sensor that can detect long-wavelength light in the P. provasolii PHY (PpPHY) region and short-wavelength light (i.e., UV to blue) in the PpCRY region
We have found a bifunctional photoreceptor, PpDUC1, composed of a fusion of PHY and CRY

Summary

Introduction

Blue light penetrates deeper than red light, and blue-light sensing is key to adapting to marine environments. A search for blue-light photoreceptors in the marine metagenome uncover a chimeric gene composed of a phytochrome and a cryptochrome (Dualchrome[1], DUC1) in a prasinophyte, Pycnococcus provasolii. Different algal PHYs can sense orange, green, and even blue light[2]. They have the ability to photosense between red-absorbing Pr and far-redabsorbing Pfr, and this conformational change enables interactions with signaling partners[3]. In 2012–2014, large-scale metagenome analyses were performed in Sendai Bay, Japan, and the western subarctic Pacific Ocean after the Great East Japan Earthquake to monitor its effects on the ocean (http://marine-meta.healthscience.sci.waseda.ac.jp/ crest/metacrest/graphs/).

Methods

Results

Conclusion