Eye-like ocelloids are built from different endosymbiotically acquired components

Dinoflagellate eye-like ocelloids are built from pre-existing organelles of disparate origin, including a cornea-like layer made of mitochondria and a retinal body made of anastomosing plastids. An eye for phytoplankton The unicellular phytoplankton known as warnowiid dinoflagellates are a prime exa...

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Vydáno v:	Nature (London) Ročník 523; číslo 7559; s. 204 - 207
Hlavní autoři:	Gavelis, Gregory S., Hayakawa, Shiho, White III, Richard A., Gojobori, Takashi, Suttle, Curtis A., Keeling, Patrick J., Leander, Brian S.
Médium:	Journal Article
Jazyk:	angličtina
Vydáno:	London Nature Publishing Group UK 09.07.2015 Nature Publishing Group
Témata:	14/28 14/35 45/23 45/77 45/88 631/181/2481 631/326/325 631/535/1258/1260 631/80/642/1374 Deoxyribonucleic acid Dinoflagellates Dinoflagellida - genetics Dinoflagellida - physiology Dinoflagellida - ultrastructure DNA Genome, Protozoan - genetics Genomics Humanities and Social Sciences letter Membranes Microorganisms Microscopy, Electron, Scanning Microscopy, Electron, Transmission Mitochondria Mitochondria - metabolism Mitochondria - ultrastructure Molecular Sequence Data multidisciplinary Phylogenetics Physiological aspects Plastids Plastids - metabolism Plastids - ultrastructure Protozoan Proteins - genetics Rhodophyta - genetics Science Studies Symbiosis
ISSN:	0028-0836, 1476-4687
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Abstract	Dinoflagellate eye-like ocelloids are built from pre-existing organelles of disparate origin, including a cornea-like layer made of mitochondria and a retinal body made of anastomosing plastids. An eye for phytoplankton The unicellular phytoplankton known as warnowiid dinoflagellates are a prime example of the remarkable diversity which exists in the realm of protsists. Within their single cell, these organisms have complex eyes or 'ocelloids', complete with structures resembling cornea, lens and retina. Gregory Gavelis et al . investigate the evolutionary origin of ocelloids using a single-organelle genomics approach in Erythropsidinium sp., Warnowia sp. and Nematodinium sp. isolates from marine waters off Japan and Canada. They find that ocelloids are built from pre-existing organelles of disparate origin. The cornea is derived from mitochondria, and the retinoid is made of an anastomosing network of plastids, originally derived from a secondary red-algal endosymbiont. 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 1 . 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 2 . 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 3 . Although mitochondria and plastids are acknowledged chiefly for their metabolic roles, they can also be building blocks for greater structural complexity.
AbstractList	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. 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 (1). 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 (2). 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 preexisting organelles can be assembled into a structure so complex that it was initially mistaken for a multicellular eye (3). Although mitochondria and plastids are acknowledged chiefly for their metabolic roles, they can also be building blocks for greater structural complexity. 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 preexisting 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. Dinoflagellate eye-like ocelloids are built from pre-existing organelles of disparate origin, including a cornea-like layer made of mitochondria and a retinal body made of anastomosing plastids. An eye for phytoplankton The unicellular phytoplankton known as warnowiid dinoflagellates are a prime example of the remarkable diversity which exists in the realm of protsists. Within their single cell, these organisms have complex eyes or 'ocelloids', complete with structures resembling cornea, lens and retina. Gregory Gavelis et al . investigate the evolutionary origin of ocelloids using a single-organelle genomics approach in Erythropsidinium sp., Warnowia sp. and Nematodinium sp. isolates from marine waters off Japan and Canada. They find that ocelloids are built from pre-existing organelles of disparate origin. The cornea is derived from mitochondria, and the retinoid is made of an anastomosing network of plastids, originally derived from a secondary red-algal endosymbiont. 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 1 . 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 2 . 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 3 . Although mitochondria and plastids are acknowledged chiefly for their metabolic roles, they can also be building blocks for greater structural complexity.
Audience	Academic
Author	Suttle, Curtis A. Leander, Brian S. White III, Richard A. Hayakawa, Shiho Gojobori, Takashi Keeling, Patrick J. Gavelis, Gregory S.
Author_xml	– sequence: 1 givenname: Gregory S. surname: Gavelis fullname: Gavelis, Gregory S. email: zoark0@gmail.com organization: Department of Zoology, University of British Columbia – sequence: 2 givenname: Shiho surname: Hayakawa fullname: Hayakawa, Shiho organization: Department of Zoology, University of British Columbia, Department of Botany, University of British Columbia, Center for Information Biology, National Institute of Genetics – sequence: 3 givenname: Richard A. surname: White III fullname: White III, Richard A. organization: Department of Microbiology and Immunology, University of British Columbia, †Present address: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington 99354, USA – sequence: 4 givenname: Takashi surname: Gojobori fullname: Gojobori, Takashi organization: Center for Information Biology, National Institute of Genetics, Computational Bioscience Research Center, King Abdullah University of Science and Technology – sequence: 5 givenname: Curtis A. surname: Suttle fullname: Suttle, Curtis A. organization: Department of Botany, University of British Columbia, Department of Microbiology and Immunology, University of British Columbia, Department of Earth, Ocean and Atmospheric Sciences, University of British Columbia, Canadian Institute for Advanced Research – sequence: 6 givenname: Patrick J. surname: Keeling fullname: Keeling, Patrick J. organization: Department of Botany, University of British Columbia, Canadian Institute for Advanced Research – sequence: 7 givenname: Brian S. surname: Leander fullname: Leander, Brian S. organization: Department of Zoology, University of British Columbia, Department of Botany, University of British Columbia, Canadian Institute for Advanced Research
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Copyright	Springer Nature Limited 2015 COPYRIGHT 2015 Nature Publishing Group Copyright Nature Publishing Group Jul 9, 2015
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PublicationDate_xml	– month: 07 year: 2015 text: 2015-07-09 day: 09
PublicationDecade	2010
PublicationPlace	London
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PublicationSubtitle	International weekly journal of science
PublicationTitle	Nature (London)
PublicationTitleAbbrev	Nature
PublicationTitleAlternate	Nature
PublicationYear	2015
Publisher	Nature Publishing Group UK Nature Publishing Group
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Snippet	Dinoflagellate eye-like ocelloids are built from pre-existing organelles of disparate origin, including a cornea-like layer made of mitochondria and a retinal... Multicellularity is often considered a prerequisite for morphological complexity, as seen in the camera-type eyes found in several groups of animals. A notable...
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SubjectTerms	14/28 14/35 45/23 45/77 45/88 631/181/2481 631/326/325 631/535/1258/1260 631/80/642/1374 Deoxyribonucleic acid Dinoflagellates Dinoflagellida - genetics Dinoflagellida - physiology Dinoflagellida - ultrastructure DNA Genome, Protozoan - genetics Genomics Humanities and Social Sciences letter Membranes Microorganisms Microscopy, Electron, Scanning Microscopy, Electron, Transmission Mitochondria Mitochondria - metabolism Mitochondria - ultrastructure Molecular Sequence Data multidisciplinary Phylogenetics Physiological aspects Plastids Plastids - metabolism Plastids - ultrastructure Protozoan Proteins - genetics Rhodophyta - genetics Science Studies Symbiosis
Title	Eye-like ocelloids are built from different endosymbiotically acquired components
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