title: Eye-like ocelloids are built from different endosymbiotically acquired components.
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 retina. 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 alga. 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 eye. Although mitochondria and plastids are acknowledged chiefly for their metabolic roles, they can also be building blocks for greater structural complexity.
authors.affiliation: Department of Zoology, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada.
authors.forename: Gregory S
authors.initials: GS
authors.lastname: Gavelis
authors.affiliation: 1] Department of Zoology, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada [2] Department of Botany, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada [3] Center for Information Biology, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan.
authors.forename: Shiho
authors.initials: S
authors.lastname: Hayakawa
authors.affiliation: Department of Microbiology and Immunology, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada.
authors.forename: Richard A
authors.initials: RA
authors.lastname: White
authors.affiliation: 1] Center for Information Biology, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan [2] Computational Bioscience Research Center, King Abdullah University of Science and Technology, Thuwal 23955-6900, Saudi Arabia.
authors.forename: Takashi
authors.initials: T
authors.lastname: Gojobori
authors.affiliation: 1] Department of Botany, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada [2] Department of Microbiology and Immunology, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada [3] Department of Earth, Ocean and Atmospheric Sciences, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada [4] Canadian Institute for Advanced Research, Toronto, Ontario M5G 1Z8, Canada.
authors.forename: Curtis A
authors.initials: CA
authors.lastname: Suttle
authors.affiliation: 1] Department of Botany, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada [2] Canadian Institute for Advanced Research, Toronto, Ontario M5G 1Z8, Canada.
authors.forename: Patrick J
authors.initials: PJ
authors.lastname: Keeling
authors.affiliation: 1] Department of Zoology, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada [2] Department of Botany, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada [3] Canadian Institute for Advanced Research, Toronto, Ontario M5G 1Z8, Canada.
authors.forename: Brian S
authors.initials: BS
authors.lastname: Leander
mesh_terms: D004141:Dinoflagellida / Q000235:genetics* / Q000502:physiology / Q000648:ultrastructure*; D018503:Genome, Protozoan / Q000235:genetics; D008855:Microscopy, Electron, Scanning; D046529:Microscopy, Electron, Transmission; D008928:Mitochondria / Q000378:metabolism / Q000648:ultrastructure; D008969:Molecular Sequence Data; D018087:Plastids / Q000378:metabolism / Q000648:ultrastructure; D015800:Protozoan Proteins / Q000235:genetics; D000461:Rhodophyta / Q000235:genetics; D013559:Symbiosis
chemical_list: D015800:Protozoan Proteins