Eye-like ocelloids are built from different endosymbiotically acquired components

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.

a, Illustration of Nematodinium showing the basic components of the ocelloid with their putative organellar origins. b, TEM of the ocelloid of Erythropsidinium, including the lens (L) and retinal body (r). c, TEM of the ocelloid of Nematodinium, depicting the edge of the lens (L) where it is overlain by a cornea-like layer of mitochondria (m). d, Genomic reads amplified from five whole cells of Nematodinium; arrow, retinal body. e, Genomic reads amplified from five retinal bodies (arrow) after they were micro-dissected from individual cells of Nematodinium.

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