Discovery of a kleptoplastic \u2018dinotom\u2019 dinoflagellate and the unique nuclear dynamics of converting kleptoplastids to permanent plastids

Norico Yamada,Ryo Onuma,Andrzej Witkowski,Rosa Trobajo,John J Bolton,David G Mann,Takeo Horiguchi,Przemysław Dąbek,Peter G Kroth

doi:10.1038/s41598-019-46852-y

Abstract

A monophyletic group of dinoflagellates, called ‘dinotoms’, are known to possess evolutionarily intermediate plastids derived from diatoms. The diatoms maintain their nuclei, mitochondria, and the endoplasmic reticulum in addition with their plastids, while it has been observed that the host dinoflagellates retain the diatoms permanently by controlling diatom karyokinesis. Previously, we showed that dinotoms have repeatedly replaced their diatoms. Here, we show the process of replacements is at two different evolutionary stages in two closely related dinotoms, Durinskia capensis and D. kwazulunatalensis. We clarify that D. capensis is a kleptoplastic protist keeping its diatoms temporarily, only for two months. On the other hand, D. kwazulunatalensis is able to keep several diatoms permanently and exhibits unique dynamics to maintain the diatom nuclei: the nuclei change their morphologies into a complex string-shape alongside the plastids during interphase and these string-shaped nuclei then condense into multiple round nuclei when the host divides. These dynamics have been observed in other dinotoms that possess permanent diatoms, while they have never been observed in any other eukaryotes. We suggest that the establishment of this unique mechanism might be a critical step for dinotoms to be able to convert kleptoplastids into permanent plastids.

Highlights

A monophyletic group of dinoflagellates, called ‘dinotoms’, are known to possess evolutionarily intermediate plastids derived from diatoms
Since there are no available cultured strains of Durinskia capensis, all experiments in this study were performed using cells isolated directly from field samples collected in the type locality of D. capensis, rocky tidal pools at Kommetjie, Western Cape, South Africa[37]
The endosymbiotic diatoms (ESDs) of D. capensis used in this study was closely related but a different species from the type ESD of D. capensis[37]

Summary

Introduction

A monophyletic group of dinoflagellates, called ‘dinotoms’, are known to possess evolutionarily intermediate plastids derived from diatoms The diatoms maintain their nuclei, mitochondria, and the endoplasmic reticulum in addition with their plastids, while it has been observed that the host dinoflagellates retain the diatoms permanently by controlling diatom karyokinesis. Because of a lack of synchronous cell division between host and the ingested organelles, or due to digestion of the ingested organelles, kleptoplastic protists lose the kleptoplastids and have to feed on free-living microalgae or protists[21] In contrast to these kleptoplastic species, the haptophyte-derived plastids of all members of the family Kareniaceae[22], except for the undescribed Antarctic dinoflagellate mentioned above[15], are established as permanent genuine organelles of host dinoflagellates and so are equivalent to the peridinin-type plastids. The diatoms in dinotoms are not strictly endosymbionts[7], because they lack silica frustules[27,28,29], but here we use the word ‘endosymbiotic’ to describe them, in accordance with previous studies of dinotoms

Methods

Results

Conclusion