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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Transcriptomic data from Warnowia sp. and Erythropsidinium sp. have been deposited in GenBank under accession numbers KR632763–KR632773. Plastid genomic data from Nematodinium sp. have been deposited in GenBank under accession numbers KP765301–KP765306.
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.
Extended data figures
Video of an Erythropsidinium cell moving with its characteristic “piston” appendage.
Video of a Warnowia cell moving.
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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