Letter | Published:

Eye-like ocelloids are built from different endosymbiotically acquired components

Nature volume 523, pages 204207 (09 July 2015) | Download Citation

Abstract

Multicellularity is often considered a prerequisite for morphological complexity, as seen in the camera-type eyes found in several groups of animals. A notable exception exists in single-celled eukaryotes called dinoflagellates, some of which have an eye-like ‘ocelloid’ consisting of subcellular analogues to a cornea, lens, iris, and retina1. These planktonic cells are uncultivated and rarely encountered in environmental samples, obscuring the function and evolutionary origin of the ocelloid. Here we show, using a combination of electron microscopy, tomography, isolated-organelle genomics, and single-cell genomics, that ocelloids are built from pre-existing organelles, including a cornea-like layer made of mitochondria and a retinal body made of anastomosing plastids. We find that the retinal body forms the central core of a network of peridinin-type plastids, which in dinoflagellates and their relatives originated through an ancient endosymbiosis with a red alga2. As such, the ocelloid is a chimaeric structure, incorporating organelles with different endosymbiotic histories. The anatomical complexity of single-celled organisms may be limited by the components available for differentiation, but the ocelloid shows that pre-existing organelles can be assembled into a structure so complex that it was initially mistaken for a multicellular eye3. Although mitochondria and plastids are acknowledged chiefly for their metabolic roles, they can also be building blocks for greater structural complexity.

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Accessions

Primary accessions

Data deposits

Transcriptomic data from Warnowia sp. and Erythropsidinium sp. have been deposited in GenBank under accession numbers KR632763KR632773. Plastid genomic data from Nematodinium sp. have been deposited in GenBank under accession numbers KP765301KP765306.

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Acknowledgements

This work was supported by grants from the Natural Sciences and Engineering Research Council of Canada (2014-05258 to B.S.L., and 227301 to P.J.K.) and the Tula Foundation (Centre for Microbial Diversity and Evolution). We thank G. Owen for his operation of the FIB-SEM and G. Martens for preparing our samples for tomography. G.S.G. thanks S. Maslakova, C. Young, A. Lehman, and D. Blackburn for training in developmental biology, marine systems, electron microscopy, and ultrastructure, respectively. C.A.S., P.J.K. and B.S.L. are Senior Fellows of the Canadian Institute for Advanced Research.

Author information

Author notes

    • Richard A. White III

    Present address: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington 99354, USA.

Affiliations

  1. Department of Zoology, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada

    • Gregory S. Gavelis
    • , Shiho Hayakawa
    •  & Brian S. Leander
  2. Department of Botany, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada

    • Shiho Hayakawa
    • , Curtis A. Suttle
    • , Patrick J. Keeling
    •  & Brian S. Leander
  3. Center for Information Biology, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan

    • Shiho Hayakawa
    •  & Takashi Gojobori
  4. Department of Microbiology and Immunology, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada

    • Richard A. White III
    •  & Curtis A. Suttle
  5. Computational Bioscience Research Center, King Abdullah University of Science and Technology, Thuwal 23955-6900, Saudi Arabia

    • Takashi Gojobori
  6. Department of Earth, Ocean and Atmospheric Sciences, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada

    • Curtis A. Suttle
  7. Canadian Institute for Advanced Research, Toronto, Ontario M5G 1Z8, Canada

    • Curtis A. Suttle
    • , Patrick J. Keeling
    •  & Brian S. Leander

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Contributions

G.S.G., S.H., P.J.K. and B.S.L. designed the experiments. G.S.G. performed light microscopy, TEM, FIB-SEM, dissected-organelle and single-cell genomics, and phylogenetic analyses on specimens he collected in Canada, with resources and funding from B.S.L. and P.J.K. S.H. performed light microscopy, TEM, and transcriptomics on specimens she collected in Japan with resources and funding from T.G., and was supported in Canada by P.J.K. and B.S.L. R.A.W. prepared genomic libraries for sequencing and participated in single-cell genomics with funding from C.A.S. G.S.G. and B.S.L. wrote the manuscript and all authors participated in the drafting process.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Gregory S. Gavelis.

Extended data

Supplementary information

Videos

  1. 1.

    Erythropsidinium sp. in vivo.

    Video of an Erythropsidinium cell moving with its characteristic “piston” appendage.

  2. 2.

    Warnowia sp. in vivo.

    Video of a Warnowia cell moving.

  3. 3.

    FIB-SEM reconstruction of the ocelloid from Nematodinium sp.

    From a stack of two-dimensional FIB-SEM images, the mitochondria (blue), lens (yellow), plastids (red), and flagellum (grey) were reconstructed as three-dimensional surfaces in Amira.

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DOI

https://doi.org/10.1038/nature14593

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