The Dark Side of the Chloroplast: Biogenesis, Metabolism and Membrane Biology of the Apicoplast

Dooren, Giel G. van; Hapuarachchi, Sanduni V.

doi:10.1016/bs.abr.2017.06.007

Cited by 14 publications

(9 citation statements)

References 176 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…In apicomplexans, like in many other plastid-bearing eukaryotes, the metabolic pathways for the biosynthesis of isoprenoids, fatty acids, and heme are localized to the plastid or apicoplast (Ralph et al. 2004; Lim and McFadden 2010; van Dooren and Hapuarachchi 2017); the heme biosynthetic pathway is only partly localized to the apicoplast. The dependency of the cytoplasm on these apicoplast biosynthetic pathways explains the persistence of these nonphotosynthetic plastids (i.e., leucoplasts) in parasitic cells and other heterotrophic eukaryotes with a photosynthetic ancestry (Janouškovec et al.…”

Section: Resultsmentioning

confidence: 99%

Nephromyces represents a diverse and novel lineage of the Apicomplexa that has retained apicoplasts

Muñoz-Gómez

Durnin

Eme

et al. 2019

Genome Biology and Evolution

View full text Add to dashboard Cite

A most interesting exception within the parasitic Apicomplexa is Nephromyces, an extracellular, probably mutualistic, endosymbiont found living inside molgulid ascidian tunicates (i.e., sea squirts). Even though Nephromyces is now known to be an apicomplexan, many other questions about its nature remain unanswered. To gain further insights into the biology and evolutionary history of this unusual apicomplexan, we aimed to (1) find the precise phylogenetic position of Nephromyces within the Apicomplexa, (2) search for the apicoplast genome of Nephromyces, and (3) infer the major metabolic pathways in the apicoplast of Nephromyces. To do this, we sequenced a metagenome and a metatranscriptome from the molgulid renal sac, the specialized habitat where Nephromyces thrives. Our phylogenetic analyses of conserved nucleus-encoded genes robustly suggest that Nephromyces is a novel lineage sister to the Hematozoa, which comprises both the Haemosporidia (e.g., Plasmodium) and the Piroplasmida (e.g., Babesia and Theileria). Furthermore, a survey of the renal sac metagenome revealed 13 small contigs that closely resemble the genomes of the non-photosynthetic reduced plastids, or apicoplasts, of other apicomplexans. We show that these apicoplast genomes correspond to a diverse set of most closely related but genetically divergent Nephromyces lineages that co-inhabit a single tunicate host. In addition, the apicoplast of Nephromyces appears to have retained all biosynthetic pathways inferred to have been ancestral to parasitic apicomplexans. Our results shed light on the evolutionary history of the only probably mutualistic apicomplexan known, Nephromyces, and provide context for a better understanding of its life style and intricate symbiosis.

show abstract

Section: Resultsmentioning

confidence: 99%

Nephromyces represents a diverse and novel lineage of the Apicomplexa that has retained apicoplasts

Muñoz-Gómez

Durnin

Eme

et al. 2019

Genome Biology and Evolution

View full text Add to dashboard Cite

show abstract

“…Our study, therefore, links apicoplast metabolism to a central function of the mitochondrion. Other products of apicoplast metabolism are also thought to be utilized in the mitochondrion, including isoprenoids (precursors of coenzyme Q) and fatty acids (precursors of lipids that are synthesized by the mitochondrion) (32). Together, these observations suggest that the apicoplast organelle plays a key "support" role for mitochondrial processes (32).…”

Section: Discussionmentioning

confidence: 99%

Characterization of the apicoplast-localized enzyme TgUroD in Toxoplasma gondii reveals a key role of the apicoplast in heme biosynthesis

Tjhin

Hayward

McFadden

et al. 2020

Journal of Biological Chemistry

Self Cite

View full text Add to dashboard Cite

Apicomplexan parasites such as Toxoplasma gondii possess an unusual heme biosynthesis pathway whose enzymes localize to the mitochondrion, cytosol, or apicoplast, a nonphotosynthetic plastid present in most apicomplexans. To characterize the involvement of the apicoplast in the T. gondii heme biosynthesis pathway, we investigated the role of the apicoplast-localized enzyme uroporphyrinogen III decarboxylase (TgUroD). We found that TgUroD knockdown impaired parasite proliferation, decreased free heme levels in the parasite, and decreased the abundance of heme-containing c-type cytochrome proteins in the parasite mitochondrion. We validated the effects of heme loss on mitochondrial cytochromes by knocking down cytochrome c/c1 heme lyase 1 (TgCCHL1), a mitochondrial enzyme that catalyzes the covalent attachment of heme to c-type cytochromes. TgCCHL1 depletion reduced parasite proliferation and decreased the abundance of c-type cytochromes. We further sought to characterize the overall importance of TgUroD and TgCCHL1 for both mitochondrial and general parasite metabolism. TgUroD depletion decreased cellular ATP levels, mitochondrial oxygen consumption, and extracellular acidification rates. By contrast, depletion of TgCCHL1 neither diminished ATP levels in the parasite nor impaired extracellular acidification rate, but resulted in specific defects in mitochondrial oxygen consumption. Together, our results indicate that the apicoplast has a key role in heme biology in T. gondii and is important for both mitochondrial and general parasite metabolism. Our study highlights the importance of heme and its synthesis in these parasites.

show abstract

“…In corallicolids, the LIPOR complex may perform a different role that uses its Fe-S centers as active sites, such as the synthesis of isoprenoids or lipoic acid. These compounds are synthesized by other enzymes with Fe-S centers in the apicoplasts of apicomplexans and are essential for their survival in their hosts [51].…”

Section: Role Of the Symbiontmentioning

confidence: 99%

Deep-sea corals provide new insight into the ecology, evolution, and the role of plastids in widespread apicomplexan symbionts of anthozoans

et al. 2020

View full text Add to dashboard Cite

Background: Apicomplexans are the causative agents of major human diseases such as malaria and toxoplasmosis. A novel group of apicomplexans, recently named corallicolids, have been detected in corals inhabiting tropical shallow reefs. These apicomplexans may represent a transitional lifestyle between free-living phototrophs and obligate parasites. To shed light on the evolutionary history of apicomplexans and to investigate their ecology in association with corals, we screened scleractinians, antipatharians, alcyonaceans, and zoantharians from shallow, mesophotic, and deep-sea communities. We detected corallicolid plastids using 16S metabarcoding, sequenced the nuclear 18S rRNA gene of corallicolids from selected samples, assembled and annotated the plastid and mitochondrial genomes from a corallicolid that associates with a deep-sea coral, and screened the metagenomes of four coral species for corallicolids. Results: We detected 23 corallicolid plastotypes that were associated with 14 coral species from three orders and depths down to 1400 m. Individual plastotypes were restricted to coral hosts within a single depth zone and within a single taxonomic order of corals. Some clusters of closely related corallicolids were revealed that associated with closely related coral species. However, the presence of divergent corallicolid lineages that associated with similar coral species and depths suggests that corallicolid/coral relations are flexible over evolutionary timescales and that a large diversity of apicomplexans may remain undiscovered. The corallicolid plastid genome from a deep-sea coral contained four genes involved in chlorophyll biosynthesis: the three genes of the LIPOR complex and acsF. Conclusions: The presence of corallicolid apicomplexans in corals below the photic zone demonstrates that they are not restricted to shallow-water reefs and are more general anthozoan symbionts. The presence of LIPOR genes in the deep-sea corallicolid precludes a role involving photosynthesis and suggests they may be involved in a different function. Thus, these genes may represent another set of genetic tools whose function was adapted from photosynthesis as the ancestors of apicomplexans evolved towards parasitic lifestyles.

show abstract

The Dark Side of the Chloroplast: Biogenesis, Metabolism and Membrane Biology of the Apicoplast

Cited by 14 publications

References 176 publications

Nephromyces represents a diverse and novel lineage of the Apicomplexa that has retained apicoplasts

Nephromyces represents a diverse and novel lineage of the Apicomplexa that has retained apicoplasts

Characterization of the apicoplast-localized enzyme TgUroD in Toxoplasma gondii reveals a key role of the apicoplast in heme biosynthesis

Deep-sea corals provide new insight into the ecology, evolution, and the role of plastids in widespread apicomplexan symbionts of anthozoans

Contact Info

Product

Resources

About