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

Author:

Maeda Taro1ORCID,Takahashi Shunichi2,Yoshida Takao3,Shimamura Shigeru3,Takaki Yoshihiro3,Nagai Yukiko3,Toyoda Atsushi4ORCID,Suzuki Yutaka5,Arimoto Asuka6,Ishii Hisaki7,Satoh Nori8ORCID,Nishiyama Tomoaki9,Hasebe Mitsuyasu110,Maruyama Tadashi11,Minagawa Jun110ORCID,Obokata Junichi712,Shigenobu Shuji110ORCID

Affiliation:

1. National Institute for Basic Biology, Okazaki, Japan

2. Sesoko Station, Tropical Biosphere Research Center, University of the Ryukyu, Okinawa, Japan

3. Japan Agency for Marine-Earth Science and Technology, Yokosuka, Japan

4. National Institute of Genetics, Shizuoka, Japan

5. The University of Tokyo, Tokyo, Japan

6. Marine Biological Laboratory, Hiroshima University, Hiroshima, Japan

7. Kyoto Prefectural University, Kyoto, Japan

8. Okinawa Institute of Science and Technology Graduate University, Okinawa, Japan

9. Research Center for Experimental Modeling of Human Disease, Kanazawa University, Kanazawa, Japan

10. SOKENDAI, the Graduate University for Advanced Studies, Okazaki, Japan

11. Kitasato University, Tokyo, Japan

12. Setsunan Universiy, Hirakata, Japan

Abstract

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.

Funder

Japan Society for the Promotion of Science

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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