Chloroplast acquisition without the gene transfer in kleptoplastic sea slugs, Plakobranchus ocellatus

Some sea slugs sequester chloroplasts from algal food in their intestinal cells and photosynthesize for months. This phenomenon, kleptoplasty, poses a question of how the chloroplast retains its activity without the algal nucleus. There have been debates on the horizontal transfer of algal genes to...

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Main Authors: Taro Maeda, Shunichi Takahashi, Takao Yoshida, Shigeru Shimamura, Yoshihiro Takaki, Yukiko Nagai, Atsushi Toyoda, Yutaka Suzuki, Asuka Arimoto, Hisaki Ishii, Nori Satoh, Tomoaki Nishiyama, Mitsuyasu Hasebe, Tadashi Maruyama, Jun Minagawa, Junichi Obokata, Shuji Shigenobu
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-04-01
Series:eLife
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Online Access:https://elifesciences.org/articles/60176
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spelling doaj-c44c9679db2c492a91f483d307397bb62021-05-05T23:00:15ZengeLife Sciences Publications LtdeLife2050-084X2021-04-011010.7554/eLife.60176Chloroplast acquisition without the gene transfer in kleptoplastic sea slugs, Plakobranchus ocellatusTaro Maeda0https://orcid.org/0000-0003-4185-0135Shunichi Takahashi1Takao Yoshida2Shigeru Shimamura3Yoshihiro Takaki4Yukiko Nagai5Atsushi Toyoda6https://orcid.org/0000-0002-0728-7548Yutaka Suzuki7Asuka Arimoto8Hisaki Ishii9Nori Satoh10https://orcid.org/0000-0002-4480-3572Tomoaki Nishiyama11Mitsuyasu Hasebe12Tadashi Maruyama13Jun Minagawa14https://orcid.org/0000-0002-3028-3203Junichi Obokata15Shuji Shigenobu16https://orcid.org/0000-0003-4640-2323National Institute for Basic Biology, Okazaki, JapanSesoko Station, Tropical Biosphere Research Center, University of the Ryukyu, Okinawa, JapanJapan Agency for Marine-Earth Science and Technology, Yokosuka, JapanJapan Agency for Marine-Earth Science and Technology, Yokosuka, JapanJapan Agency for Marine-Earth Science and Technology, Yokosuka, JapanJapan Agency for Marine-Earth Science and Technology, Yokosuka, JapanNational Institute of Genetics, Shizuoka, JapanThe University of Tokyo, Tokyo, JapanMarine Biological Laboratory, Hiroshima University, Hiroshima, JapanKyoto Prefectural University, Kyoto, JapanOkinawa Institute of Science and Technology Graduate University, Okinawa, JapanResearch Center for Experimental Modeling of Human Disease, Kanazawa University, Kanazawa, JapanNational Institute for Basic Biology, Okazaki, Japan; SOKENDAI, the Graduate University for Advanced Studies, Okazaki, JapanKitasato University, Tokyo, JapanNational Institute for Basic Biology, Okazaki, Japan; SOKENDAI, the Graduate University for Advanced Studies, Okazaki, JapanKyoto Prefectural University, Kyoto, Japan; Setsunan Universiy, Hirakata, JapanNational Institute for Basic Biology, Okazaki, Japan; SOKENDAI, the Graduate University for Advanced Studies, Okazaki, JapanSome sea slugs sequester chloroplasts from algal food in their intestinal cells and photosynthesize for months. This phenomenon, kleptoplasty, poses a question of how the chloroplast retains its activity without the algal nucleus. There have been debates on the horizontal transfer of algal genes to the animal nucleus. To settle the arguments, this study reported the genome of a kleptoplastic sea slug, Plakobranchus ocellatus, and found no evidence of photosynthetic genes encoded on the nucleus. Nevertheless, it was confirmed that light illumination prolongs the life of mollusk under starvation. These data presented a paradigm that a complex adaptive trait, as typified by photosynthesis, can be transferred between eukaryotic kingdoms by a unique organelle transmission without nuclear gene transfer. Our phylogenomic analysis showed that genes for proteolysis and immunity undergo gene expansion and are up-regulated in chloroplast-enriched tissue, suggesting that these molluskan genes are involved in the phenotype acquisition without horizontal gene transfer.https://elifesciences.org/articles/60176Plakobranchus ocellatusElysia marginatakleptoplastygenometranscriptomeHalimeda borneensis
collection DOAJ
language English
format Article
sources DOAJ
author Taro Maeda
Shunichi Takahashi
Takao Yoshida
Shigeru Shimamura
Yoshihiro Takaki
Yukiko Nagai
Atsushi Toyoda
Yutaka Suzuki
Asuka Arimoto
Hisaki Ishii
Nori Satoh
Tomoaki Nishiyama
Mitsuyasu Hasebe
Tadashi Maruyama
Jun Minagawa
Junichi Obokata
Shuji Shigenobu
spellingShingle Taro Maeda
Shunichi Takahashi
Takao Yoshida
Shigeru Shimamura
Yoshihiro Takaki
Yukiko Nagai
Atsushi Toyoda
Yutaka Suzuki
Asuka Arimoto
Hisaki Ishii
Nori Satoh
Tomoaki Nishiyama
Mitsuyasu Hasebe
Tadashi Maruyama
Jun Minagawa
Junichi Obokata
Shuji Shigenobu
Chloroplast acquisition without the gene transfer in kleptoplastic sea slugs, Plakobranchus ocellatus
eLife
Plakobranchus ocellatus
Elysia marginata
kleptoplasty
genome
transcriptome
Halimeda borneensis
author_facet Taro Maeda
Shunichi Takahashi
Takao Yoshida
Shigeru Shimamura
Yoshihiro Takaki
Yukiko Nagai
Atsushi Toyoda
Yutaka Suzuki
Asuka Arimoto
Hisaki Ishii
Nori Satoh
Tomoaki Nishiyama
Mitsuyasu Hasebe
Tadashi Maruyama
Jun Minagawa
Junichi Obokata
Shuji Shigenobu
author_sort Taro Maeda
title Chloroplast acquisition without the gene transfer in kleptoplastic sea slugs, Plakobranchus ocellatus
title_short Chloroplast acquisition without the gene transfer in kleptoplastic sea slugs, Plakobranchus ocellatus
title_full Chloroplast acquisition without the gene transfer in kleptoplastic sea slugs, Plakobranchus ocellatus
title_fullStr Chloroplast acquisition without the gene transfer in kleptoplastic sea slugs, Plakobranchus ocellatus
title_full_unstemmed Chloroplast acquisition without the gene transfer in kleptoplastic sea slugs, Plakobranchus ocellatus
title_sort chloroplast acquisition without the gene transfer in kleptoplastic sea slugs, plakobranchus ocellatus
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2021-04-01
description Some sea slugs sequester chloroplasts from algal food in their intestinal cells and photosynthesize for months. This phenomenon, kleptoplasty, poses a question of how the chloroplast retains its activity without the algal nucleus. There have been debates on the horizontal transfer of algal genes to the animal nucleus. To settle the arguments, this study reported the genome of a kleptoplastic sea slug, Plakobranchus ocellatus, and found no evidence of photosynthetic genes encoded on the nucleus. Nevertheless, it was confirmed that light illumination prolongs the life of mollusk under starvation. These data presented a paradigm that a complex adaptive trait, as typified by photosynthesis, can be transferred between eukaryotic kingdoms by a unique organelle transmission without nuclear gene transfer. Our phylogenomic analysis showed that genes for proteolysis and immunity undergo gene expansion and are up-regulated in chloroplast-enriched tissue, suggesting that these molluskan genes are involved in the phenotype acquisition without horizontal gene transfer.
topic Plakobranchus ocellatus
Elysia marginata
kleptoplasty
genome
transcriptome
Halimeda borneensis
url https://elifesciences.org/articles/60176
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