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Retention of transcriptionally active cryptophyte nuclei by the ciliate Myrionecta rubra

Abstract

It is well documented that organelles can be retained and used by predatory organisms, but in most cases such sequestrations are limited to plastids of algal prey1. Furthermore, sequestrations of prey organelles are typically highly ephemeral2 as a result of the inability of the organelle to remain functional in the absence of numerous nuclear-encoded genes involved in its regulation, division and function3. The marine photosynthetic ciliate Myrionecta rubra (Lohmann 1908) Jankowski 1976 (the same as Mesodinium rubrum)4 is known to possess organelles of cryptophyte origin5,6,7,8,9, which has led to debate concerning their status as permanent symbiotic or temporary sequestered fixtures5,6,7,8,9,10,11,12,13. Recently, M. rubra has been shown to steal plastids (that is, chloroplasts) from the cryptomonad, Geminigera cryophila, and prey nuclei were observed to accumulate after feeding10. Here we show that cryptophyte nuclei in M. rubra are retained for up to 30 days, are transcriptionally active and service plastids derived from multiple cryptophyte cells. Expression of a cryptophyte nuclear-encoded gene involved in plastid function declined in M. rubra as the sequestered nuclei disappeared from the population. Cytokinesis, plastid performance and their replication are dependent on recurrent stealing of cryptophyte nuclei. Karyoklepty (from Greek karydi, kernel; kleftis, thief) represents a previously unknown evolutionary strategy for acquiring biochemical potential.

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Figure 1: Micrographs of Myrionecta rubra with Geminigera cryophila nuclei.
Figure 2: Expression of the cryptophyte nuclear-encoded gene for the plastid-targeted protein LHCC10 in Myrionecta rubra , and the presence of cryptophyte nuclei during starvation.

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Acknowledgements

We thank T. Kana, D.W. Coats, K. Bidle and P. Falkowski for comments on this manuscript; D. Gustafson, S. Heyward and H. Bowers for advice and/or technical assistance; T. Kana for use of his PAM fluorimeter; and C. Scholin for assistance with FISH protocols. This project was funded by a National Science Foundation grant (to D.K.S.).

Author Contributions M.D.J. and D.K.S. conceived of the project. M.D.J. conducted all laboratory experiments and data analysis for the paper. D.K.S., D.O. and C.F.D. provided methodological expertise and contributed to the interpretation of data. M.D.J. wrote most of the paper, with contributions and advice from D.K.S., D.O. and C.F.D.

The sequences for the β-tubulin gene, CbbX, LHCC10 and psbA are deposited in GenBank under accession numbers EF151014, EF151015, EF151016 and EF151017.

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Correspondence to Matthew D. Johnson.

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The sequences for the β-tubulin gene, CbbX, LHCC10 and psbA are deposited in GenBank under accession numbers EF151014, EF151015, EF151016 and EF151017. Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.

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Johnson, M., Oldach, D., Delwiche, C. et al. Retention of transcriptionally active cryptophyte nuclei by the ciliate Myrionecta rubra. Nature 445, 426–428 (2007). https://doi.org/10.1038/nature05496

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