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Genome evolution of a non-parasitic secondary heterotroph, the diatom Nitzschia putrida

Ryoma Kamikawa, Takako Mochizuki, Mika Sakamoto, Yasuhiro Tanizawa, Takuro Nakayama, Ryo Onuma, Ugo Cenci, Daniel Moog, Samuel Speak, Krisztina Sarkozi, Andrew Toseland, Cock van Oosterhout, Kaori Oyama, Misako Kato, Keitaro Kume, Motoki Kayama, Tomonori Azuma, Ken-ichiro Ishii, Hideaki Miyashita, Bernard Henrissat, Vincent Lombard, Joe Win, Sophien Kamoun, Yuichiro Kashiyama, Shigeki Mayama, Shin-ya Miyagishima, Goro Tanifuji, Thomas Mock, Yasukazu Nakamura
doi: https://doi.org/10.1101/2021.01.24.427197
Ryoma Kamikawa
1Graduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan
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  • For correspondence: kamikawa.ryoma.7v@kyoto-u.ac.jp
Takako Mochizuki
2Department of Informatics, National Institute of Genetics, Research Organization of Information and Systems, Shizuoka 411-8540, Japan
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Mika Sakamoto
2Department of Informatics, National Institute of Genetics, Research Organization of Information and Systems, Shizuoka 411-8540, Japan
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Yasuhiro Tanizawa
2Department of Informatics, National Institute of Genetics, Research Organization of Information and Systems, Shizuoka 411-8540, Japan
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Takuro Nakayama
3Graduate School of Life Sciences, Tohoku University, Sendai 980-8578, Japan
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Ryo Onuma
4Department of Gene Function and Phenomics, National Institute of Genetics, Shizuoka 411-8540, Japan
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Ugo Cenci
5Univ. Lille, CNRS, UMR 8576 – UGSF – Unité de Glycobiologie Structurale et Fonctionnelle, F-59000 Lille, France
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Daniel Moog
6Laboratory for Cell Biology, Philipps University Marburg, Karl-von-Frisch-Str. 8, SYNMIKRO Research Center, Hans-Meerwein-Str. 6, 35032, Marburg, Germany
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Samuel Speak
7School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich, UK
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Krisztina Sarkozi
7School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich, UK
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Andrew Toseland
7School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich, UK
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Cock van Oosterhout
7School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich, UK
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Kaori Oyama
8Graduate School of Humanities and Sciences, Ochanomizu University, Tokyo, Japan
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Misako Kato
8Graduate School of Humanities and Sciences, Ochanomizu University, Tokyo, Japan
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Keitaro Kume
9Department of Clinical Medicine, Faculty of Medicine, University of Tsukuba, Ibaraki 305-8572, Japan
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Motoki Kayama
10Graduate School of Human and Environmental Studies, Kyoto University, Kyoto 606-8501, Japan
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Tomonori Azuma
10Graduate School of Human and Environmental Studies, Kyoto University, Kyoto 606-8501, Japan
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Ken-ichiro Ishii
10Graduate School of Human and Environmental Studies, Kyoto University, Kyoto 606-8501, Japan
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Hideaki Miyashita
10Graduate School of Human and Environmental Studies, Kyoto University, Kyoto 606-8501, Japan
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Bernard Henrissat
11Architecture et Fonction des Macromolécules Biologiques (AFMB), CNRS, Université Aix-Marseille, 163 Avenue de Luminy, 13288 Marseille, France
12INRA, USC 1408 AFMB, 13288, Marseille, France
13Department of Biological Sciences, King Abdulaziz University, Jeddah, 21589, Saudi Arabia
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Vincent Lombard
11Architecture et Fonction des Macromolécules Biologiques (AFMB), CNRS, Université Aix-Marseille, 163 Avenue de Luminy, 13288 Marseille, France
12INRA, USC 1408 AFMB, 13288, Marseille, France
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Joe Win
14The Sainsbury Laboratory, University of East Anglia, Norwich Research Park, Norwich, UK
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Sophien Kamoun
14The Sainsbury Laboratory, University of East Anglia, Norwich Research Park, Norwich, UK
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Yuichiro Kashiyama
15Graduate School of Engineering, Fukui University of Technology, Fukui, Japan
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Shigeki Mayama
16Advanced Support Center for Science Teachers, Tokyo Gakugei University, Koganei, Tokyo, Japan
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Shin-ya Miyagishima
4Department of Gene Function and Phenomics, National Institute of Genetics, Shizuoka 411-8540, Japan
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Goro Tanifuji
17Department of Zoology, National Museum of Nature and Science, Tsukuba 305-0005, Japan
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Thomas Mock
7School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich, UK
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Yasukazu Nakamura
2Department of Informatics, National Institute of Genetics, Research Organization of Information and Systems, Shizuoka 411-8540, Japan
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Abstract

Secondary loss of photosynthesis is observed across almost all plastid-bearing branches of the eukaryotic tree of life. However, genome-based insights into the transition from a phototroph into a secondary heterotroph have so far only been revealed for parasitic species. Free-living organisms can yield unique insights into the evolutionary consequence of the loss of photosynthesis, as the parasitic lifestyle requires specific adaptations to host environments. Here we report on the diploid genome of the free-living diatom Nitzschia putrida (35 Mbp), a non-photosynthetic osmotroph whose photosynthetic relatives contribute ca. 40% of net oceanic primary production. Comparative analyses with photosynthetic diatoms revealed that a combination of genes loss, the horizontal acquisition of genes involved in organic carbon degradation, a unique secretome and the rapid divergence of conserved gene families involved in cell wall and extracellular metabolism appear to have facilitated the lifestyle of a non-parasitic, free-living secondary heterotroph.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted January 24, 2021.
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Genome evolution of a non-parasitic secondary heterotroph, the diatom Nitzschia putrida
Ryoma Kamikawa, Takako Mochizuki, Mika Sakamoto, Yasuhiro Tanizawa, Takuro Nakayama, Ryo Onuma, Ugo Cenci, Daniel Moog, Samuel Speak, Krisztina Sarkozi, Andrew Toseland, Cock van Oosterhout, Kaori Oyama, Misako Kato, Keitaro Kume, Motoki Kayama, Tomonori Azuma, Ken-ichiro Ishii, Hideaki Miyashita, Bernard Henrissat, Vincent Lombard, Joe Win, Sophien Kamoun, Yuichiro Kashiyama, Shigeki Mayama, Shin-ya Miyagishima, Goro Tanifuji, Thomas Mock, Yasukazu Nakamura
bioRxiv 2021.01.24.427197; doi: https://doi.org/10.1101/2021.01.24.427197
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Genome evolution of a non-parasitic secondary heterotroph, the diatom Nitzschia putrida
Ryoma Kamikawa, Takako Mochizuki, Mika Sakamoto, Yasuhiro Tanizawa, Takuro Nakayama, Ryo Onuma, Ugo Cenci, Daniel Moog, Samuel Speak, Krisztina Sarkozi, Andrew Toseland, Cock van Oosterhout, Kaori Oyama, Misako Kato, Keitaro Kume, Motoki Kayama, Tomonori Azuma, Ken-ichiro Ishii, Hideaki Miyashita, Bernard Henrissat, Vincent Lombard, Joe Win, Sophien Kamoun, Yuichiro Kashiyama, Shigeki Mayama, Shin-ya Miyagishima, Goro Tanifuji, Thomas Mock, Yasukazu Nakamura
bioRxiv 2021.01.24.427197; doi: https://doi.org/10.1101/2021.01.24.427197

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