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Taming chlorophylls by early eukaryotes underpinned algal interactions and the diversification of the eukaryotes on the oxygenated Earth
Kashiyama, Yuichiro1,2,3,4; Yokoyama, Akiko5,6; Shiratori, Takashi5,7; Hess, Sebastian8; Not, Fabrice9; Bachy, Charles9; Gutierrez-Rodriguez, Andres9,10; Kawahara, Jun1; Suzaki, Toshinobu11; Nakazawa, Masami12; Ishikawa, Takahiro13; Maruyama, Moe1; Wang, Mengyun14; Chen, Man14; Gong, Yingchun14; Seto, Kensuke15,16; Kagami, Maiko15,16; Hamamoto, Yoko17,18; Honda, Daiske18,19; Umetani, Takahiro2; Shihongi, Akira1; Kayama, Motoki1; Matsuda, Toshiki1; Taira, Junya2; Yabuki, Akinori7; Tsuchiya, Masashi7; Hirakawa, Yoshihisa5; Kawaguchi, Akane20; Nomura, Mami20,21; Nakamura, Atsushi20; Namba, Noriaki20; Matsumoto, Mitsufumi22; Tanaka, Tsuyoshi23; Yoshino, Tomoko23; Higuchi, Rina11; Yamamoto, Akihiro2; Maruyama, Tadanobu1; Yamaguchi, Aika24; Uzuka, Akihiro25; Miyagishima, Shinya25; Tanifuji, Goro26; Kawachi, Masanobu4; Kinoshita, Yusuke3; Tamiaki, Hitoshi3
2019-08-01
Source PublicationISME JOURNAL
ISSN1751-7362
Volume13Issue:8Pages:1899-1910
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 13(2),17(3)-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.

DOI10.1038/s41396-019-0377-0
Funding OrganizationPrecursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency
Indexed BySCI
Language英语
Funding ProjectPrecursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Japan Society for the Promotion of Science (JSPS) KAKENHI[JP15H05607] ; Japan Society for the Promotion of Science (JSPS) KAKENHI[JP16K14813] ; Japan Society for the Promotion of Science (JSPS) KAKENHI[JP201242] ; Japan Society for the Promotion of Science (JSPS) KAKENHI[JP236484] ; Japan Society for the Promotion of Science (JSPS) KAKENHI[JP25281012] ; Japan Society for the Promotion of Science (JSPS) KAKENHI[JP15KK0026] ; Japan Society for the Promotion of Science (JSPS) KAKENHI[JP17H03855] ; Japan Society for the Promotion of Science (JSPS) KAKENHI[JP17H06436] ; French National Research Agency[IMPEKAB ANR-15-CE02-001] ; [NSFC31772419] ; [13J00587]
WOS Research AreaEnvironmental Sciences & Ecology ; Microbiology
WOS SubjectEcology ; Microbiology
WOS IDWOS:000475814500002
WOS KeywordRISE ; NOV ; OCEAN ; ENOL
PublisherNATURE PUBLISHING GROUP
Funding OrganizationPrecursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Precursory Research for Embryonic Science and Technology (PRESTO) of the Japan Science and Technology Agency (JST) ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Core Research of Evolutional Science and Technology program (CREST) from JST ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; Japan Society for the Promotion of Science (JSPS) KAKENHI ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency ; French National Research Agency
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Document Type期刊论文
Identifierhttp://ir.ihb.ac.cn/handle/342005/32067
Collection藻类生物技术和生物能源研发中心_期刊论文
Corresponding AuthorKashiyama, Yuichiro
Affiliation1.Fukui Univ Technol, Grad Sch Engn, Fukui, Fukui, Japan
2.Fukui Univ Technol, Fac Engn, Dept Environm & Biol Chem, Fukui, Fukui, Japan
3.Ritsumeikan Univ, Grad Sch Life Sci, Kusatsu, Shiga, Japan
4.Natl Inst Environm Studies, Ctr Environm Biol & Ecosyst Studies, Tsukuba, Ibaraki, Japan
5.Univ Tsukuba, Fac Life & Environm Sci, Tsukuba, Ibaraki, Japan
6.Natl Inst Environm Studies, Ctr Reg Environm Res, Tsukuba, Ibaraki, Japan
7.Japan Agcy Marine Earth Sci & Technol, Dept Marine Biodivers Res, Yokosuka, Kanagawa, Japan
8.Dalhousie Univ, Life Sci Ctr, Halifax, NS, Canada
9.Sorbonne Univ, CNRS, AD2M Lab, Ecol Marine Plankton Team,Stn Biol Roscoff, Pl Georges Teissier, F-29680 Roscoff, France
10.Natl Inst Water & Atmospher Res, 301 Evans Bay Parade, Wellington 6021, New Zealand
11.Kobe Univ, Grad Sch Sci, Kobe, Hyogo, Japan
12.Osaka Prefecture Univ, Grad Sch Life & Environm Sci, Div Appl Life Sci, Sakai, Osaka, Japan
13.Shimane Univ, Fac Life & Environm Sci, Dept Life Sci & Biotechnol, Matsue, Shimane, Japan
14.Chinese Acad Sci, Inst Hydrobiol, Wuhan, Hubei, Peoples R China
15.Toho Univ, Fac Sci, Dept Environm Sci, Funabashi, Chiba, Japan
16.Yokohama Natl Univ, Grad Sch Environm & Informat Sci, Yokohama, Kanagawa, Japan
17.Konan Univ, Grad Sch Nat Sci, Kobe, Hyogo, Japan
18.Konan Univ, Inst Integrat Neurobiol, Kobe, Hyogo, Japan
19.Konan Univ, Fac Sci & Engn, Kobe, Hyogo, Japan
20.Univ Tsukuba, Grad Sch Life & Environm Sci, Tsukuba, Ibaraki, Japan
21.Kyoto Univ, Grad Sch Sci, Kyoto, Japan
22.Elect Power Dev Co Ltd, Biotechnol Lab, Kitakyushu, Fukuoka, Japan
23.Tokyo Univ Agr & Technol, Inst Engn, Koganei, Tokyo, Japan
24.Kobe Univ, Res Ctr Inland Seas, Kobe, Hyogo, Japan
25.Natl Inst Genet, Dept Cell Genet, Mishima, Shizuoka, Japan
26.Natl Museum Nat & Sci, Tsukuba, Ibaraki, Japan
Recommended Citation
GB/T 7714
Kashiyama, Yuichiro,Yokoyama, Akiko,Shiratori, Takashi,et al. Taming chlorophylls by early eukaryotes underpinned algal interactions and the diversification of the eukaryotes on the oxygenated Earth[J]. ISME JOURNAL,2019,13(8):1899-1910.
APA Kashiyama, Yuichiro.,Yokoyama, Akiko.,Shiratori, Takashi.,Hess, Sebastian.,Not, Fabrice.,...&Tamiaki, Hitoshi.(2019).Taming chlorophylls by early eukaryotes underpinned algal interactions and the diversification of the eukaryotes on the oxygenated Earth.ISME JOURNAL,13(8),1899-1910.
MLA Kashiyama, Yuichiro,et al."Taming chlorophylls by early eukaryotes underpinned algal interactions and the diversification of the eukaryotes on the oxygenated Earth".ISME JOURNAL 13.8(2019):1899-1910.
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