Taming chlorophylls by early eukaryotes underpinned algal interactions and the diversification of the eukaryotes on the oxygenated Earth View Full Text


Ontology type: schema:ScholarlyArticle     


Article Info

DATE

2019-02-26

AUTHORS

Yuichiro Kashiyama, Akiko Yokoyama, Takashi Shiratori, Sebastian Hess, Fabrice Not, Charles Bachy, Andres Gutierrez-Rodriguez, Jun Kawahara, Toshinobu Suzaki, Masami Nakazawa, Takahiro Ishikawa, Moe Maruyama, Mengyun Wang, Man Chen, Yingchun Gong, Kensuke Seto, Maiko Kagami, Yoko Hamamoto, Daiske Honda, Takahiro Umetani, Akira Shihongi, Motoki Kayama, Toshiki Matsuda, Junya Taira, Akinori Yabuki, Masashi Tsuchiya, Yoshihisa Hirakawa, Akane Kawaguchi, Mami Nomura, Atsushi Nakamura, Noriaki Namba, Mitsufumi Matsumoto, Tsuyoshi Tanaka, Tomoko Yoshino, Rina Higuchi, Akihiro Yamamoto, Tadanobu Maruyama, Aika Yamaguchi, Akihiro Uzuka, Shinya Miyagishima, Goro Tanifuji, Masanobu Kawachi, Yusuke Kinoshita, Hitoshi Tamiaki

ABSTRACT

Extant eukaryote ecology is primarily sustained by oxygenic photosynthesis, in which chlorophylls play essential roles. The exceptional photosensitivity of chlorophylls allows them to harvest solar energy for photosynthesis, but on the other hand, they also generate cytotoxic reactive oxygen species. A risk of such phototoxicity of the chlorophyll must become particularly prominent upon dynamic cellular interactions that potentially disrupt the mechanisms that are designed to quench photoexcited chlorophylls in the phototrophic cells. Extensive examination of a wide variety of phagotrophic, parasitic, and phototrophic microeukaryotes demonstrates that a catabolic process that converts chlorophylls into nonphotosensitive 132,173-cyclopheophorbide enols (CPEs) is phylogenetically ubiquitous among extant eukaryotes. The accumulation of CPEs is identified in phagotrophic algivores belonging to virtually all major eukaryotic assemblages with the exception of Archaeplastida, in which no algivorous species have been reported. In addition, accumulation of CPEs is revealed to be common among phototrophic microeukaryotes (i.e., microalgae) along with dismantling of their secondary chloroplasts. Thus, we infer that CPE-accumulating chlorophyll catabolism (CACC) primarily evolved among algivorous microeukaryotes to detoxify chlorophylls in an early stage of their evolution. Subsequently, it also underpinned photosynthetic endosymbiosis by securing close interactions with photosynthetic machinery containing abundant chlorophylls, which led to the acquisition of secondary chloroplasts. Our results strongly suggest that CACC, which allowed the consumption of oxygenic primary producers, ultimately permitted the successful radiation of the eukaryotes throughout and after the late Proterozoic global oxygenation. More... »

PAGES

1-12

Identifiers

URI

http://scigraph.springernature.com/pub.10.1038/s41396-019-0377-0

DOI

http://dx.doi.org/10.1038/s41396-019-0377-0

DIMENSIONS

https://app.dimensions.ai/details/publication/pub.1112396593

PUBMED

https://www.ncbi.nlm.nih.gov/pubmed/30809012


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