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


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Type

Article

Change log

Authors

Gornik, Sebastian G 
Febrimarsa 
Cassin, Andrew M 
MacRae, James I 
Ramaprasad, Abhinay 

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.

Description

Keywords

diaminopimelate aminotransferase, endosymbiosis, organelle loss, plastid loss, plastid metabolism, Adenosine Triphosphate, Amino Acid Oxidoreductases, Animals, Cell Nucleus, Crustacea, Cytosol, Dinoflagellida, Fatty Acid Synthases, Fatty Acids, Mitochondria, Molecular Sequence Data, Parasites, Photosynthesis, Phylogeny, Plasmodium, Plastids, RNA, Symbiosis, Transcriptome

Journal Title

Proc Natl Acad Sci U S A

Conference Name

Journal ISSN

0027-8424
1091-6490

Volume Title

112

Publisher

Proceedings of the National Academy of Sciences
Sponsorship
We thank Nick Katris for assistance with Toxoplasma transformation and Ellen Nisbet for critically reading this report. This work was supported by Australian Research Council (ARC) Grants DP130100572 and DP1093395; a King Abdullah University of Science and Technology Faculty Baseline Research Fund; and Victorian Life Sciences Computation Initiative Grant VR0254. S.G.G. was supported by Science Foundation Ireland Grant 13/SIRG/2125; F. was supported by an Australia Award; A.M.C. and A.B. were supported by ARC Centre of Excellence in Plant Cell Walls Grant CE110001007; and M.J.M. was supported by the National Health and Medical Research Council as a Principal Research Fellow.