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

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.

Fig. 1.

Search strategy for plastid-encoded genes and nucleus-encoded genes for plastid-targeted (or mitochondrial-targeted) proteins. Gene query sets were from predicted apicoplast-targeted proteins common to Plasmodium (A); predicted P. falciparum mitochondrion-targeted proteins (B); and plastid-encoded genes common to apicomplexans, dinoflagellates, and chromerids (C). A list of genes and full search results are shown in Datasets S1–S3. FL, full length; mTP, mitochondrial targeting peptide.

Fig. 2.

Reconstructed metabolic pathways in the common ancestor of apicomplexans and dinoflagellates at the time of plastid gain (A) and in Hematodinium sp. (B), from transcriptomic data. Cytosolic MVA pathway is not present in any apicomplexan or dinoflagellate, but is present in ciliates and is inferred to be present at the time of plastid gain. Dashed lines indicate apicomplexan hybrid tetrapyrrole pathways; dashed circles indicate enzymes currently unidentified in transcriptomes. Enzyme color represents typical location and origin as follows: green, plastid; yellow, cytosol; red, mitochondrion. Hatched (green/white) DAP pathway indicates uncertain origin of this typically plastid-located pathway in Hematodinium. MVA, mevalonate IPP pathway; DOXP, 1-deoxy-d-xylulose-5-phosphate IPP pathway; C15/20, isoprene chains 15 and 20 carbons long derived from IPP (an external source of IPP/isoprenoids for Hematodinium sp. is predicted); SUF, plastid-type iron-sulfur cluster pathway; DAP, diaminopimelate lysine pathway; C4/C5 pathways for tetrapyrrole (TP) synthesis differ only by the reactions to δ-aminolevulinic acid (ALA) and their location.

Fig. 3.

HemD (uroporphyrinogen III synthase) phylogeny showing a plastid-derived protein in Hematodinium sp. Presence/absence of targeting leader sequences for the plastid clade is indicated. Support values (ML bootstraps/Bayesian posterior probabilities) are shown only for major clades. Wedges indicate collapsed clades shown in full in Fig. S3.