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  • Endosymbiosis undone by ste...
    Gornik, Sebastian G.; Febrimarsa; Cassin, Andrew M.; MacRae, James I.; Ramaprasad, Abhinay; Rchiad, Zineb; McConville, Malcolm J.; Bacic, Antony; McFadden, Geoffrey I.; Pain, Arnab; Waller, Ross F.

    Proceedings of the National Academy of Sciences - PNAS, 05/2015, Letnik: 112, Številka: 18
    Journal Article

    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. Significance Endosymbiotic organelles are a defining feature of eukaryotes—the last common ancestor and all extant eukaryotes possess at least a mitochondrial derivative. Although mitochondria and plastids are identified with aerobic ATP synthesis and photosynthesis, respectively, their retention by their host cells requires the merging and integration of many, often redundant, metabolic pathways. As a result, complex metabolic interdependencies arise between these formerly independent cells. Complete loss of endosymbiotic organelles, even where aerobic respiration or photosynthesis is lost, is exceedingly difficult, as demonstrated by persistence of organelles throughout secondary anaerobes and parasites. Here, we identify a rare but clear case of plastid loss in a parasitic alga and detail the metabolic disentanglement that was required to achieve this exceptional evolutionary event.