A photosynthetic alveolate closely related to apicomplexan parasites

Moore, R. G.; Oborník, Miroslav; Janouškovec, Jan; Chrudimský, Tomáš; Vancová, Marie; Green, David H.; Wright, Simon W.; Davies, Noel W.; Bolch, Christopher J. S.; Heimann, Kirsten; Šlapeta, Jan; Høegh-Guldberg, Ove; Logsdon, John M.; Carter, Dee

doi:10.1038/nature06635

Cited by 426 publications

(404 citation statements)

References 27 publications

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“…Recent evidence suggests that apicomplexans evolved from a free-living photosynthetic ancestor (1). This ancestry is reflected in the presence of a chloroplast-like organelle, the apicoplast (2).…”

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confidence: 99%

Genetic Evidence that an Endosymbiont-derived Endoplasmic Reticulum-associated Protein Degradation (ERAD) System Functions in Import of Apicoplast Proteins

Agrawal

Dooren

Beatty

et al. 2009

Journal of Biological Chemistry

177

229

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Most apicomplexan parasites harbor a relict chloroplast, the apicoplast, that is critical for their survival. Whereas the apicoplast maintains a small genome, the bulk of its proteins are nuclear encoded and imported into the organelle. Several models have been proposed to explain how proteins might cross the four membranes that surround the apicoplast; however, experimental data discriminating these models are largely missing. Here we present genetic evidence that apicoplast protein import depends on elements derived from the ER-associated protein degradation (ERAD) system of the endosymbiont. We identified two sets of ERAD components in Toxoplasma gondii, one associated with the ER and cytoplasm and one localized to the membranes of the apicoplast. We engineered a conditional null mutant in apicoplast Der1, the putative pore of the apicoplast ERAD complex, and found that loss of Der1 Ap results in loss of apicoplast protein import and subsequent death of the parasite.Apicomplexa are a phylum of obligate parasites that include the causative agents of malaria, toxoplasmosis, and cryptosporidiosis. Recent evidence suggests that apicomplexans evolved from a free-living photosynthetic ancestor (1). This ancestry is reflected in the presence of a chloroplast-like organelle, the apicoplast (2). While no longer engaged in photosynthesis, the apicoplast is essential to parasite survival and home to several critical biosynthetic pathways. Bioinformatic and experimental evidence suggests that the apicoplast is engaged in the synthesis of fatty acids, isoprenoids, and heme (3, 4). Genetic or pharmacological ablation of these pathways blocks parasite growth and the apicoplast, therefore, is currently considered a prime target for antiparasitic drug development (5-7). The organelle was derived by secondary endosymbiosis and reflects the successful union of a red alga and a heterotrophic eukaryote (8). A large number of algal genes were transferred to the host nucleus, and their products must now be routed back into the organelle. Trafficking occurs via the secretory pathway and is guided by an N-terminal bipartite targeting sequence (9). Transport from the ER to the apicoplast is believed to be vesicle mediated and to sidestep the Golgi apparatus (10, 11). Once delivered to the apicoplast, proteins have to cross three additional membranes. Recently, we demonstrated that a homolog of Tic20, a component of the translocon of the inner chloroplast membrane (Tic) 4 complex in plants, is likely required for protein import across the innermost membrane of the apicoplast (12). To date bioinformatics searches have failed to identify a matching translocon of the outer chloroplast membrane in apicomplexans (13). Analysis of the genome of the remnant nucleus of the algal endosymbiont in cryptomonads showed the presence of an ER-associated protein degradation (ERAD) system and offered a candidate for a translocon across the third and potentially the second membrane (14). Classically, ERAD functions in the homeostasis of the secretory ...

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mentioning

confidence: 99%

Genetic Evidence that an Endosymbiont-derived Endoplasmic Reticulum-associated Protein Degradation (ERAD) System Functions in Import of Apicoplast Proteins

Agrawal

Dooren

Beatty

et al. 2009

Journal of Biological Chemistry

177

229

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“…Nearly a decade ago, Moore et al (2008) first reported the isolation of an apicomplexan alga, Chromera veliae , from corals. This free-living photosynthetic alga lies on the evolutionary path to non-photosythetic apicomplexans such as the malaria pathogen and is therefore a bridge between photosynthetic phytoplankton, such as the dinoflagellate Symbiodinium , and non-photosynthetic, parasitic apicoplexans.…”

Section: The Specific Ecological Roles Of Scleractinian Corals On Cormentioning

confidence: 99%

The roles of endolithic fungi in bioerosion and disease in marine ecosystems. I. General concepts

et al. 2017

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Endolithic true fungi and fungus-like microorganisms penetrate calcareous substrates formed by living organisms, cause significant bioerosion and are involved in diseases of many host animals in marine ecosystems. A theoretical interactive model for the ecology of reef-building corals is proposed in this review. This model includes five principle partners that exist in a dynamic equilibrium: polyps of a colonial coelenterate, endosymbiotic zooxanthellae, endolithic algae (that penetrate coral skeletons), endolithic fungi (that attack the endolithic algae, the zooxanthellae and the polyps) and prokaryotic and eukaryotic microorganisms (which live in the coral mucus). Endolithic fungi and fungus-like boring microorganisms are important components of the marine calcium carbonate cycle because they actively contribute to the biodegradation of shells of animals composed of calcium carbonate and calcareous geological substrates.

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“…This emergence is also influenced by light intensity, salinity, and nutrient levels (28,30). In an initial ultrastructural analysis of C. velia, internal, non-membranebound axonemes were noted (26). By analogy to its malariacausing relative Plasmodium, it was proposed that C. velia assembles its axoneme completely within the cytoplasm, most likely via an IFT-independent mechanism (26,28).…”

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confidence: 99%

“…C. velia is a photosynthetic microalga that was isolated from Australian hard corals and shows a range of genetic and morphological similarities to Apicomplexa (26)(27)(28). The life cycle of C. velia alternates between nonflagellate coccoid cells and motile biflagellate cells (26,28,29). The two flagella emerge from the anterior end of the cell, with the shorter (anterior) flagellum located to the anterior part of the longer (posterior) flagellum.…”

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confidence: 99%

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Evidence of Intraflagellar Transport and Apical Complex Formation in a Free-Living Relative of the Apicomplexa

et al. 2014

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bSince its first description, Chromera velia has attracted keen interest as the closest free-living relative of parasitic Apicomplexa. The life cycle of this unicellular alga is complex and involves a motile biflagellate form. Flagella are thought to be formed in the cytoplasm, a rare phenomenon shared with Plasmodium in which the canonical mode of flagellar assembly, intraflagellar transport, is dispensed with. Here we demonstrate the expression of intraflagellar transport components in C. velia, answering the question of whether this organism has the potential to assemble flagella via the canonical route. We have developed and characterized a culturing protocol that favors the generation of flagellate forms. From this, we have determined a marked shift in the mode of daughter cell production from two to four daughter cells per division as a function of time after passage. We conduct an ultrastructural examination of the C. velia flagellate form by using serial TEM and show that flagellar biogenesis in C. velia occurs prior to cytokinesis. We demonstrate a close association of the flagellar apparatus with a complex system of apical structures, including a micropore, a conoid, and a complex endomembrane system reminiscent of the apical complex of parasitic apicomplexans. Recent work has begun to elucidate the possible flagellar origins of the apical complex, and we show that in C. velia these structures are contemporaneous within a single cell and share multiple connections. We propose that C. velia therefore represents a vital piece in the puzzle of the origins of the apical complex.

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A photosynthetic alveolate closely related to apicomplexan parasites

Cited by 426 publications

References 27 publications

Genetic Evidence that an Endosymbiont-derived Endoplasmic Reticulum-associated Protein Degradation (ERAD) System Functions in Import of Apicoplast Proteins

Genetic Evidence that an Endosymbiont-derived Endoplasmic Reticulum-associated Protein Degradation (ERAD) System Functions in Import of Apicoplast Proteins

The roles of endolithic fungi in bioerosion and disease in marine ecosystems. I. General concepts

Evidence of Intraflagellar Transport and Apical Complex Formation in a Free-Living Relative of the Apicomplexa

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