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

Taro Maeda,Tomoaki Nishiyama,Jun Minagawa,Mitsuyasu Hasebe,Shigeru Shimamura,Junichi Obokata,Yutaka Suzuki,Yoshihiro Takaki,Yukiko Nagai,Shuji Shigenobu,Atsushi Toyoda,Takao Yoshida,Hisaki Ishii,Nori Satoh,Tadashi Maruyama,Asuka Arimoto,Shunichi Takahashi

doi:10.7554/elife.60176

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.

Highlights

Since the Hershey–Chase experiment (Hershey and Chase, 1952), which proved that DNA is the material transferred to bacteria in phage infections, horizontal gene transfer (HGT) has been considered essential for cross-species transformation (Arber, 2014)
It was demonstrated that (1) kleptoplast photosynthesis extends the lifetime of PoB under starvation, (2) the PoB genome encodes no algal nucleus-derived genes, and (3) PoB individuals up-regulate genes for carbohydrate metabolism, proteolysis, and immune response in their DG
The whole kleptoplast DNA (kpDNA) sequence indicated that PoB kleptoplasts could produce some proteins involved in photosynthesis (e.g., PsbA, a core protein in photosystem II (PSII); Figure 3) if gene expression machinery is sufficiently active, as reported in E. chlorotica (Green et al, 2000; Pierce et al, 2007)

Summary

Introduction

Since the Hershey–Chase experiment (Hershey and Chase, 1952), which proved that DNA is the material transferred to bacteria in phage infections, horizontal gene transfer (HGT) has been considered essential for cross-species transformation (Arber, 2014). The prion hypothesis has rekindled the interest in proteins as an element of phenotype propagation (Crick, 1970; Wickner et al, 2015), HGT is still assumed to be the cause of transformation. In a secondary plastid acquisition scenario in dinoflagellates, (1) a non-phototrophic eukaryote sequesters a unicellular archaeplastid; (2) the endogenous gene transfer to the non-phototrophic eukaryote leads to the shrinkage of the archaeplastidan nuclear DNA (nucDNA); and (3) the archaeplastidan nucleus disappears, and its plastid becomes a secondary plastid in the host (Reyes-Prieto et al, 2007)

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Results

Conclusion