Eye-like ocelloids are built from different endosymbiotically acquired components

Handle URI:
http://hdl.handle.net/10754/566109
Title:
Eye-like ocelloids are built from different endosymbiotically acquired components
Authors:
Gavelis, Gregory S.; Hayakawa, Shiho; White, Richard A.; Gojobori, Takashi ( 0000-0001-7850-1743 ) ; Suttle, Curtis A.; Keeling, Patrick J.; Leander, Brian S.
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.
KAUST Department:
Computational Bioscience Research Center (CBRC); Biological and Environmental Sciences and Engineering (BESE) Division; Bioscience Program
Publisher:
Nature Publishing Group
Journal:
Nature
Issue Date:
1-Jul-2015
DOI:
10.1038/nature14593
Type:
Article
ISSN:
0028-0836; 1476-4687
Appears in Collections:
Articles; Bioscience Program; Computational Bioscience Research Center (CBRC); Biological and Environmental Sciences and Engineering (BESE) Division

Full metadata record

DC FieldValue Language
dc.contributor.authorGavelis, Gregory S.en
dc.contributor.authorHayakawa, Shihoen
dc.contributor.authorWhite, Richard A.en
dc.contributor.authorGojobori, Takashien
dc.contributor.authorSuttle, Curtis A.en
dc.contributor.authorKeeling, Patrick J.en
dc.contributor.authorLeander, Brian S.en
dc.date.accessioned2015-08-12T09:28:35Zen
dc.date.available2015-08-12T09:28:35Zen
dc.date.issued2015-07-01en
dc.identifier.issn0028-0836en
dc.identifier.issn1476-4687en
dc.identifier.doi10.1038/nature14593en
dc.identifier.urihttp://hdl.handle.net/10754/566109en
dc.description.abstractMulticellularity 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.en
dc.publisherNature Publishing Groupen
dc.titleEye-like ocelloids are built from different endosymbiotically acquired componentsen
dc.typeArticleen
dc.contributor.departmentComputational Bioscience Research Center (CBRC)en
dc.contributor.departmentBiological and Environmental Sciences and Engineering (BESE) Divisionen
dc.contributor.departmentBioscience Programen
dc.identifier.journalNatureen
kaust.authorGojobori, Takashien
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