Multiple Independent Origins of Apicomplexan-Like Parasites

Mathur, Varsha; Kolísko, Martin; Hehenberger, Elisabeth; Irwin, Nicholas A. T.; Leander, Brian S.; Kristmundsson, Árni; Freeman, Mark; Keeling, Patrick J.

doi:10.1016/j.cub.2019.07.019

Cited by 94 publications

(94 citation statements)

References 52 publications

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“…All of the aforementioned pathogens are obligatory intracellular parasites and share a variety of common features. Among them, one which deserves distinctive attention is the apical complex, the hallmark of the Apicomplexa phylum, an indispensable structure for the recognition and subsequent invasion of host cells [25]. Most of these parasites also contain the apicoplast, an essential plastid organelle derived from an endosymbiotic process with a seaweed, which is crucial for the biosynthesis of essential parasitic biomolecules, like fatty acids (type II fatty acid pathway), iron-sulfur clusters, the heme group, and isoprenoid precursors (the non-mevalonate pathway) [25,26].…”

Section: Can Antimalarials Treat Toxoplasmosis?mentioning

confidence: 99%

Antimalarial Agents as Therapeutic Tools Against Toxoplasmosis—A Short Bridge between Two Distant Illnesses

et al. 2020

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Toxoplasmosis is an infectious disease with paramount impact worldwide, affecting many vulnerable populations and representing a significant matter of concern. Current therapies used against toxoplasmosis are based essentially on old chemotypes, which fail in providing a definitive cure for the disease, placing the most sensitive populations at risk for irreversible damage in vital organs, culminating in death in the most serious cases. Antimalarial drugs have been shown to possess key features for drug repurposing, finding application in the treatment of other parasite-borne illnesses, including toxoplasmosis. Antimalarials provide the most effective therapeutic solutions against toxoplasmosis and make up for the majority of currently available antitoxoplasmic drugs. Additionally, other antiplasmodial drugs have been scrutinized and many promising candidates have emanated in recent developments. Available data demonstrate that it is worthwhile to explore the activity of classical and most recent antimalarial chemotypes, such as quinolines, endoperoxides, pyrazolo[1,5-a]pyrimidines, and nature-derived peptide-based parasiticidal agents, in the context of toxoplasmosis chemotherapy, in the quest for encountering more effective and safer tools for toxoplasmosis control or eradication.

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Section: Can Antimalarials Treat Toxoplasmosis?mentioning

confidence: 99%

Antimalarial Agents as Therapeutic Tools Against Toxoplasmosis—A Short Bridge between Two Distant Illnesses

et al. 2020

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“…Cavalier-Smith [56] proposed, based on SSU rRNA genes and morphology, that Platyproteum is related to Perkinsida. Interestingly, a recent phylogenomic analysis [57] resolved these species as two independent lineages, separate from Apicomplexa. Piridium forms a branch sister to Vitrella , and Platyproteum is a sister lineage to the whole clade of Apcomplexa-Chrompodellida.…”

Section: Apicomplexan Relatives and The Origins And Evolution Of Tmentioning

confidence: 99%

“…For example, there are approximately 200–250 genes in a standard photosynthetic red algal plastid [62], and even the recently described reduced plastids of non-photosynthetic parasitic red algae retain 70–85 genes [63,64]. Interestingly, Piridium , which is a parasitic lineage sister to Vitrella to the exclusion of apicomplexans, contains a plastid genome that is almost indistinguishable from the plastid genome of Apicomplexa, suggesting very strong evolutionary constraints and convergence in the genome reduction process [57].…”

Section: Plastid Genome Evolution Within the Platyproteum-chrompodmentioning

confidence: 99%

“…Apicoplast genomes also contain inverted repeats that mainly consist of an rRNA operon that appears to be ancestral since they are characteristic of many plastid genomes [30,32,60,65]. These inverted repeats have likely been lost twice independently in the evolution of this lineage, once in Chromera , which has also lost the typical circular structure and exists as a linear molecule that possesses inverted repeats of three genes at the end ( orf 264, psb A, and atp H2) [15], and in Piridium , where a potential remnant of the inverted repeat can be detected as a putative ribosomal large subunit (LSU) pseudogene [57].…”

Section: Plastid Genome Evolution Within the Platyproteum-chrompodmentioning

confidence: 99%

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There Is Treasure Everywhere: Reductive Plastid Evolution in Apicomplexa in Light of Their Close Relatives

Salomaki

Kolísko

2019

Biomolecules

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The phylum Apicomplexa (Alveolates) comprises a group of host-associated protists, predominately intracellular parasites, including devastating parasites like Plasmodium falciparum, the causative agent of malaria. One of the more fascinating characteristics of Apicomplexa is their highly reduced (and occasionally lost) remnant plastid, termed the apicoplast. Four core metabolic pathways are retained in the apicoplast: heme synthesis, iron–sulfur cluster synthesis, isoprenoid synthesis, and fatty acid synthesis. It has been suggested that one or more of these pathways are essential for plastid and plastid genome retention. The past decade has witnessed the discovery of several apicomplexan relatives, and next-generation sequencing efforts are revealing that they retain variable plastid metabolic capacities. These data are providing clues about the core genes and pathways of reduced plastids, while at the same time further confounding our view on the evolutionary history of the apicoplast. Here, we examine the evolutionary history of the apicoplast, explore plastid metabolism in Apicomplexa and their close relatives, and propose that the differences among reduced plastids result from a game of endosymbiotic roulette. Continued exploration of the Apicomplexa and their relatives is sure to provide new insights into the evolution of the apicoplast and apicomplexans as a whole.

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“…Coccidia are further classified within the phylum Apicomplexa along with haemosporidians including Plasmodium spp. and Babesia spp., the agents of malaria and babesiosis, respectively (4). Because T. gondii is genetically tractable, can be grown continuously in culture, and can be injected into mice for a reliable model of the disease, this parasite has become an attractive model system for other related parasites.…”

Section: Introductionmentioning

confidence: 99%

ToxoplasmaTgATG9 is critical for autophagy and long-term persistence in tissue cysts

Smith

Kannan

Coppens

et al. 2020

Preprint

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Many of the world's warm-blooded species are chronically infected with Toxoplasma gondii tissue cysts, including up to an estimated one third of the global human population. The cellular processes that permit long-term parasite persistence within the cyst are largely unknown, not only for T. gondii but also for related coccidian parasites that impact human and animal health. A previous study revealed an accumulation of autophagic material in the lysosome-like Vacuolar Compartment (VAC) of chronic stage bradyzoites lacking functional cathepsin L protease (TgCPL) activity. Furthermore, it was shown that TgCPL knockout bradyzoites have compromised viability, indicating the turnover of autophagic material could be necessary for bradyzoite survival. However, the extent to which autophagy itself contributes to bradyzoite development and fitness remained unknown. Herein we show that genetic ablation of TgATG9 substantially reduces canonical autophagy and compromises bradyzoite viability. Transmission electron microscopy revealed structural abnormalities occurring in ∆atg9 bradyzoites, including disorganization of the inner membrane complex and plasma membrane, the occurrence of multiple nuclei within a single bradyzoite cell, as well as various anomalies associated with the VAC. TgATG9-deficient bradyzoites accumulated significantly less undigested material in the VAC upon inhibition of TgCPL activity, suggesting that autophagy contributes material to the VAC for degradation. Intriguingly, abnormal mitochondria networks were observed in TgATG9deficient bradyzoites. They were thin and elongated and often adopted a horseshoe conformation. Some abnormal mitochondrial structures were found to contain numerous different cytoplasmic components and organelles. Bradyzoite fitness was found to be drastically compromised, both in vitro and in mice, with very few brain cysts identified in mice 5 weeks postinfection. Taken together, our data suggests that TgATG9, and by extension autophagy, is critical for cellular homeostasis in bradyzoites and is necessary for long-term persistence within the cyst of this coccidian parasite.

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Multiple Independent Origins of Apicomplexan-Like Parasites

Abstract: Highlights d The origin of apicomplexans from algae occurred at least three times independently d Piridium and Platyproteum form distinct lineages of obligate animal parasites d They both retain cryptic plastids that are highly convergent with apicomplexans

Cited by 94 publications

References 52 publications

Antimalarial Agents as Therapeutic Tools Against Toxoplasmosis—A Short Bridge between Two Distant Illnesses

Antimalarial Agents as Therapeutic Tools Against Toxoplasmosis—A Short Bridge between Two Distant Illnesses

There Is Treasure Everywhere: Reductive Plastid Evolution in Apicomplexa in Light of Their Close Relatives

ToxoplasmaTgATG9 is critical for autophagy and long-term persistence in tissue cysts

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