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Genome analysis of Parmales, the sister group of diatoms, reveals the evolutionary specialization of diatoms from phago-mixotrophs to photoautotrophs

Ban, Hiroki Sato, Shinya Yoshikawa, Shinya Yamada, Kazumasa Nakamura, Yoji Ichinomiya, Mutsuo Sato, Naoki Blanc-Mathieu, Romain Endo, Hisashi Kuwata, Akira Ogata, Hiroyuki 京都大学 DOI:10.1038/s42003-023-05002-x

2023.07.07

概要

The order Parmales (class Bolidophyceae) is a minor group of pico-sized eukaryotic marine phytoplankton that contains species with cells surrounded by silica plates. Previous studies revealed that Parmales is a member of ochrophytes and sister to diatoms (phylum Bacillariophyta), the most successful phytoplankton group in the modern ocean. Therefore, parmalean genomes can serve as a reference to elucidate both the evolutionary events that differentiated these two lineages and the genomic basis for the ecological success of diatoms vs. the more cryptic lifestyle of parmaleans. Here, we compare the genomes of eight parmaleans and five diatoms to explore their physiological and evolutionary differences. Parmaleans are predicted to be phago-mixotrophs. By contrast, diatoms have lost genes related to phagocytosis, indicating the ecological specialization from phago-mixotrophy to photoautotrophy in their early evolution. Furthermore, diatoms show significant enrichment in gene sets involved in nutrient uptake and metabolism, including iron and silica, in comparison with parmaleans. Overall, our results suggest a strong evolutionary link between the loss of phago-mixotrophy and specialization to a silicified photoautotrophic life stage early in diatom evolution after diverging from the Parmales lineage.

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Acknowledgements

This work was supported by JSPS/KAKENHI (No. 22657027, 23370046, 26291085,

221S0002, 16K07489, 16H06279 (PAGS), 17H03724), the Canon Foundation, the Collaborative Research Program of Institute for Chemical Research, Kyoto University (No.

2016-30, 2015-39), and the JST “Establishment of University Fellowships Towards The

Creation of Science Technology Innovation” Grant Number JPMJFS2123. Computational

time was provided by the SuperComputer System, Institute for Chemical Research, Kyoto

University. We thank Gabe Yedid, Ph.D., from Edanz (https://jp.edanz.com/englishediting-b) for editing a draft of this manuscript. We thank Drs. Adriana Lopes dos Santos

and Daniel Vaulot for valuable suggestions.

Author contributions

H.B. performed most of the bioinformatics analyses presented in this work and wrote

initial version of the manuscript. R.B.-M., H.E., and H.O. supervised the bioinformatics

part of the study. Y.N. performed genome assembly and gene prediction for Triparma

laevis f. inornata. A.K. coordinated the genome sequencing part of the study. S.S., S.Y.,

K.Y., M.I., and A.K. contributed to culture and DNA/RNA sequencing. N.S. contributed

to functional interpretation of the genomes. All authors contributed to the interpretation

of the results and the finalization of the manuscript.

Competing interests

The authors declare no competing interests.

Additional information

Supplementary information The online version contains supplementary material

available at https://doi.org/10.1038/s42003-023-05002-x.

Correspondence and requests for materials should be addressed to Akira Kuwata or

Hiroyuki Ogata.

Peer review information Communications Biology thanks Muhua Wang and the other

anonymous reviewer(s) for their contribution to the peer review of this work. Primary

Handling Editors: Linn Hoffmann and David Favero. A peer review file is available.

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© The Author(s) 2023

COMMUNICATIONS BIOLOGY | (2023)6:697 | https://doi.org/10.1038/s42003-023-05002-x | www.nature.com/commsbio

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