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Proc Natl Acad Sci U S A. 2015 May 5;112(18):5767-72. doi: 10.1073/pnas.1423400112. Epub 2015 Apr 20.

Endosymbiosis undone by stepwise elimination of the plastid in a parasitic dinoflagellate.

Author information

1
School of Botany, University of Melbourne, Parkville, Victoria 3010, Australia; School of Natural Sciences, National University of Ireland, Galway, Ireland;
2
School of Botany, University of Melbourne, Parkville, Victoria 3010, Australia;
3
Australian Research Council Centre of Excellence in Plant Cell Walls, School of Botany, University of Melbourne, Victoria 3010, Australia;
4
The Francis Crick Institute, London, NW7 1AA, United Kingdom; Bio21 Molecular Science and Biotechnology Institute, University of Melbourne, Parkville, Victoria 3010, Australia;
5
Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology, Thuwal 23955-6900, Saudi Arabia;
6
Bio21 Molecular Science and Biotechnology Institute, University of Melbourne, Parkville, Victoria 3010, Australia;
7
School of Botany, University of Melbourne, Parkville, Victoria 3010, Australia; Australian Research Council Centre of Excellence in Plant Cell Walls, School of Botany, University of Melbourne, Victoria 3010, Australia;
8
Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology, Thuwal 23955-6900, Saudi Arabia; Global Station for Zoonosis Control, Global Institution for Collaborative Research and Education (GI-CoRE), Hokkaido University, N20 W10 Kita-ku, Sapporo, 001-0020 Japan; and.
9
School of Botany, University of Melbourne, Parkville, Victoria 3010, Australia; Department of Biochemistry, University of Cambridge, Cambridge CB2 1QW, United Kingdom rfw26@cam.ac.uk.

Abstract

Organelle gain through endosymbiosis has been integral to the origin and diversification of eukaryotes, and, once gained, plastids and mitochondria seem seldom lost. Indeed, discovery of nonphotosynthetic plastids in many eukaryotes--notably, the apicoplast in apicomplexan parasites such as the malaria pathogen Plasmodium--highlights the essential metabolic functions performed by plastids beyond photosynthesis. Once a cell becomes reliant on these ancillary functions, organelle dependence is apparently difficult to overcome. Previous examples of endosymbiotic organelle loss (either mitochondria or plastids), which have been invoked to explain the origin of eukaryotic diversity, have subsequently been recognized as organelle reduction to cryptic forms, such as mitosomes and apicoplasts. Integration of these ancient symbionts with their hosts has been too well developed to reverse. Here, we provide evidence that the dinoflagellate Hematodinium sp., a marine parasite of crustaceans, represents a rare case of endosymbiotic organelle loss by the elimination of the plastid. Extensive RNA and genomic sequencing data provide no evidence for a plastid organelle, but, rather, reveal a metabolic decoupling from known plastid functions that typically impede organelle loss. This independence has been achieved through retention of ancestral anabolic pathways, enzyme relocation from the plastid to the cytosol, and metabolic scavenging from the parasite's host. Hematodinium sp. thus represents a further dimension of endosymbiosis--life after the organelle.

KEYWORDS:

diaminopimelate aminotransferase; endosymbiosis; organelle loss; plastid loss; plastid metabolism

PMID:
25902514
PMCID:
PMC4426444
DOI:
10.1073/pnas.1423400112
[Indexed for MEDLINE]
Free PMC Article

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