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

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    Type
    Article
    Authors
    Gornik, Sebastian G.
    Febrimarsa,
    Cassin, Andrew M.
    MacRae, James I.
    Ramaprasad, Abhinay cc
    Rchiad, ‍Zineb cc
    McConville, Malcolm J.
    Bacic, Antony
    McFadden, Geoffrey I.
    Pain, Arnab cc
    Waller, Ross F.
    KAUST Department
    Biological and Environmental Sciences and Engineering (BESE) Division
    Bioscience Program
    Computational Bioscience Research Center (CBRC)
    Pathogen Genomics Laboratory
    Date
    2015-04-20
    Online Publication Date
    2015-04-20
    Print Publication Date
    2015-05-05
    Permanent link to this record
    http://hdl.handle.net/10754/564146
    
    Metadata
    Show full item record
    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. © 2015, National Academy of Sciences. All rights reserved.
    Citation
    Gornik, S. G., Febrimarsa, Cassin, A. M., MacRae, J. I., Ramaprasad, A., Rchiad, Z., … Waller, R. F. (2015). Endosymbiosis undone by stepwise elimination of the plastid in a parasitic dinoflagellate. Proceedings of the National Academy of Sciences, 112(18), 5767–5772. doi:10.1073/pnas.1423400112
    Sponsors
    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.
    Publisher
    Proceedings of the National Academy of Sciences
    Journal
    Proceedings of the National Academy of Sciences
    DOI
    10.1073/pnas.1423400112
    PubMed ID
    25902514
    PubMed Central ID
    PMC4426444
    Additional Links
    http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4426444
    ae974a485f413a2113503eed53cd6c53
    10.1073/pnas.1423400112
    Scopus Count
    Collections
    Articles; Biological and Environmental Science and Engineering (BESE) Division; Bioscience Program; Computational Bioscience Research Center (CBRC)

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