Factors mediating plastid dependency and the origins of parasitism in apicomplexans and their close relatives

Abstract

Apicomplexans are a major lineage of parasites, including causative agents of malaria and toxoplasmosis. How such highly adapted parasites evolved from free-living ancestors is poorly understood, particularly because they contain nonphotosynthetic plastids with which they have a complex metabolic dependency. Here, we examine the origin of apicomplexan parasitism by resolving the evolutionary distribution of several key characteristics in their closest free-living relatives, photosynthetic chromerids and predatory colpodellids. Using environmental sequence data, we describe the diversity of these apicomplexan-related lineages and select five species that represent this diversity for transcriptome sequencing. Phylogenomic analysis recovered a monophyletic lineage of chromerids and colpodellids as the sister group to apicomplexans, and a complex distribution of retention versus loss for photosynthesis, plastid genomes, and plastid organelles. Reconstructing the evolution of all plastid and cytosolic metabolic pathways related to apicomplexan plastid function revealed an ancient dependency on plastid isoprenoid biosynthesis, predating the divergence of apicomplexan and dinoflagellates. Similarly, plastid genome retention is strongly linked to the retention of two genes in the plastid genome, sufB and clpC, altogether suggesting a relatively simple model for plastid retention and loss. Lastly, we examine the broader distribution of a suite of molecular characteristics previously linked to the origins of apicomplexan parasitism and find that virtually all are present in their free-living relatives. The emergence of parasitism may not be driven by acquisition of novel components, but rather by loss and modification of the existing, conserved traits.A picomplexans are globally important parasites of humans and animals that include Plasmodium (malaria), Toxoplasma (toxoplasmosis), and Cryptosporidium (cryptosporidiosis). Their success as parasites rests on several highly specialized structures and systems that enable them to gain entry to and divide within cells or tissues of their hosts. These structures include the multimembrane pellicle, a relict nonphotosynthetic plastid (absent in Cryptosporidium), and the apical complex, which is made up of cytoskeletal and secretory elements (e.g., the conoid and rhoptries, respectively). Many specific characteristics of apicomplexans make attractive drug targets, and others may have played a key role in the origin of parasitism. Indeed, the question of apicomplexan origins has been of interest in general but is challenged by a paucity of comparable information from free-living relatives. Several apicomplexan relatives are known, some photosynthetic and others predatory (1, 2), but we lack a comprehensive understanding of their biology because they have either been discovered only recently, or are difficult to establish and maintain in culture. In general, photosynthetic apicomplexan relatives are referred to as chromerids (including Chromera and Vitrella) (1, 3) whereas predators...

Major transitions in dinoflagellate evolution unveiled by phylotranscriptomics

“…The pattern of plastid dependency in dinoflagellates parallels that in apicomplexans and chrompodellids [chromerids and colpodellids (47)] and reinforces conclusions that their common ancestor had a plastid (46) and was reliant on it for isoprenoid units after it lost the capability to synthesize them in the cytosol (47). Despite rare secondary losses of plastids in certain parasites (50,57) and ongoing uncertainties about plastid presence in some organisms (e.g., gregarines, Psammosa, Eudubosquella), plastids are indispensable in all free-living members of this group yet examined (Fig.…”

“…Despite rare secondary losses of plastids in certain parasites (50,57) and ongoing uncertainties about plastid presence in some organisms (e.g., gregarines, Psammosa, Eudubosquella), plastids are indispensable in all free-living members of this group yet examined (Fig. 3A) (47,48), including multiple uncultured forms (58). This pattern suggests that the metabolic dependency on plastids in free-living species cannot be bypassed by obtaining the relevant compounds from the environment or ingested prey (Fig.…”

“…The other half contains a photosynthetic peridinin-pigmented plastid that, in some lineages, has been replaced by other types of plastids. The peridinin plastid was inherited from the plastid in the common photosynthetic ancestor of dinoflagellates and apicomplexans (46,47), but whether cryptic, nonpigmented plastids have been retained in nonphotosynthetic dinoflagellates remains contentious: Crypthecodinium and Oxyrrhis appear to contain plastid-derived genes (48,49), whereas Hematodinium lacks all traces of the organelle (50). We investigated whether plastid and cytosolic pathways for isoprenoid, tetrapyrrole, and fatty acid biosynthesis were present in two distantly related nonphotosynthetic dinoflagellates, N. scintillans and O. marina, as well as in Dinophysis acuminata, a fundamentally nonphotosynthetic species that nevertheless carries kleptoplastids.…”

“…ClpC have essential functions in plastids, but, in apicomplexans, they also constitute key barriers to the loss of the plastid genome (47,55). SufB carries a bipartite plastid-targeting signature in Oxyrrhis (SI Appendix, Table S6), an apparently incomplete N-terminal extension in Dinophysis, and is encoded on GC-rich contigs in all three species (55-66.7% GC), all typical of a nuclear but not plastidial localization.…”

“…Similarly to sufB, all three nonphotosynthetic dinoflagellates contain plastid-like clpC fragments on GC-rich, likely nuclear contigs (SI Appendix, SI Materials and Methods). SufB and clpC are also nucleus-encoded in Perkinsus and Symbiodinium (47,56), and this indicates that both genes were relocated from the plastid genome early in their evolution. Because plastids in photosynthetic dinoflagellates encode only photosystem genes (7,56) and ancestral reconstruction identifies no additional barriers to genome loss (47), evidence increasingly indicates that plastid genomes in nonphotosynthetic dinoflagellates and Perkinsus were lost with the loss of photosynthesis.…”