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The Evolution, Metabolism and Functions of the Apicoplast Downloaded from rstb.royalsocietypublishing.org on March 31, 2010 The evolution, metabolism and functions of the apicoplast Liting Lim and Geoffrey Ian McFadden Phil. Trans. R. Soc. B 2010 365, 749-763 doi: 10.1098/rstb.2009.0273 References This article cites 122 articles, 50 of which can be accessed free http://rstb.royalsocietypublishing.org/content/365/1541/749.full.html#ref-list-1 This article is free to access Rapid response Respond to this article http://rstb.royalsocietypublishing.org/letters/submit/royptb;365/1541/749 Subject collections Articles on similar topics can be found in the following collections biogeochemistry (10 articles) bioinformatics (83 articles) cellular biology (59 articles) evolution (1569 articles) Receive free email alerts when new articles cite this article - sign up in the box at the top Email alerting service right-hand corner of the article or click here To subscribe to Phil. Trans. R. Soc. B go to: http://rstb.royalsocietypublishing.org/subscriptions This journal is © 2010 The Royal Society Downloaded from rstb.royalsocietypublishing.org on March 31, 2010 Phil. Trans. R. Soc. B (2010) 365, 749–763 doi:10.1098/rstb.2009.0273 Review The evolution, metabolism and functions of the apicoplast Liting Lim and Geoffrey Ian McFadden* School of Botany, University of Melbourne, Parkville, Victoria 3010, Australia The malaria parasite, Plasmodium falciparum, harbours a relict plastid known as the ‘apicoplast’. The discovery of the apicoplast ushered in an exciting new prospect for drug development against the para- site. The eubacterial ancestry of the organelle offers a wealth of opportunities for the development of therapeutic interventions. Morphological, biochemical and bioinformatic studies of the apicoplast have further reinforced its ‘plant-like’ characteristics and potential as a drug target. However, we are still not sure why the apicoplast is essential for the parasite’s survival. This review explores the ori- gins and metabolic functions of the apicoplast. In an attempt to decipher the role of the organelle within the parasite we also take a closer look at the transporters decorating the plastid to better understand the metabolic exchanges between the apicoplast and the rest of the parasite cell. Keywords: plastid; apicoplast; parasite; apicomplexan; evolution; metabolism 1. INTRODUCTION effective in fighting malaria, and resistance will hope- The apicoplast is a vestigial plastid present in most fully take longer to erode their utility, it is imperative parasites of the Phylum Apicomplexa. The group to discover more drug targets to manage the disease derives its name from the apical complex, a collection before any more drugs lose clinical relevance. of anterior structures that allow the parasite to invade Indeed, we need to identify as many new drug leads host cells and establish themselves therein. Apicom- as possible to expand our repertoire of drugs to use plexans are responsible for a wide range of serious in combination therapies and also to allow rotation diseases of humans, livestock, wild animals and invert- to minimize resistance. ebrates and there are an estimated 5000 species of The discovery of the apicoplast ushered in an exciting parasites in the group. Human apicomplexan diseases new prospect for drug development against Plasmo- include malaria and toxoplasmosis; babesiosis, theiler- dium falciparum. The eubacterial ancestry of the iosis and coccidiosis are common problems in organelle offers a wealth of opportunities for the devel- livestock. Malaria is a major global health problem opment of therapeutic interventions (McFadden et al. with 3.3 billion at risk of infection and an estimated 1996; McFadden & Roos 1999). Morphological, bio- 250 million cases per year that resulted in nearly a chemical and bioinformatic studies of the apicoplast million deaths in 2006 (WHO world malaria report have further reinforced its ‘plant-like’ characteristics 2008). Malaria is endemic in tropical areas owing to and potential as a drug target. However, we are still warm temperatures and high humidity, which are con- totally ignorant about why the apicoplast is essential ducive to transmission by the mosquito vectors. Most to the parasite’s survival (Fichera & Roos 1997; He of the disease burden lies in Africa, where treatment et al. 2001). This review explores the origins and meta- accessibility is the greatest limiting factor. Conse- bolic functions of the apicoplast. In an attempt to quently, malaria is often considered a ‘poor man’s decipher the role of the organelle within the parasite disease’ and, unlike most diseases, the malaria we also take a closer look at the transporters decorating problem is becoming worse rather than better. the plastid to better understand the metabolic The current greatest challenge in malaria manage- exchanges between the apicoplast and the rest of the ment is the resistance of parasites to conventional parasite cell. monochemotherapies like chloroquine and sulphadox- ine-pyrimethamine. These therapies were cheap and effective but they are losing efficacy worldwide owing 2. ORIGIN AND EVOLUTION to resistance. Artemisinin-based combination thera- (a) Where did the apicoplast come from? pies are currently the most effective treatment and The apicoplast is clearly of secondary endosymbiotic patients’ drug compliance is also reasonable. Although origin, which refers to one eukaryote having engulfed combinatorial therapies are proving to be more and retained another eukaryote with a plastid obtained by primary endosymbiosis of a cyanobacterium-like prokaryote. Secondary endosymbiotic plastids * Author for correspondence ([email protected]). typically have three or four membranes, whereas One contribution of 12 to a Theme Issue ‘Evolution of organellar primary plastids invariably have only two membranes, metabolism in unicellular eukaryotes’. which are homologous to the two membranes of the 749 This journal is # 2010 The Royal Society Downloaded from rstb.royalsocietypublishing.org on March 31, 2010 750 L. Lim & G. I. McFadden Review. Apicoplast Gram-negative ancestral cyanobacterium like endo- symbiont to parasite and provides a glimpse into the symbiont. Some observers describe three membranes earliest form of the apicomplexan–animal interaction around the apicoplast but the majority see four, and (Moore et al. 2008). Ultrastructural examinations no one claims to see two, so a secondary endosymbio- and molecular phylogenetic analyses demonstrated tic origin is agreed upon. The outermost membrane of this new organism to be the closest known photosyn- the apicoplast is analogous to the phagosomal mem- thetic relative to apicomplexan parasites and the brane of the host cell, hence it is also of endosomal common origin of its plastid to the apicoplasts origin. The second outermost membrane of the apico- (Moore et al. 2008). The autotrophic nature of plast originates from the plasma membrane of the C. velia allows it to be cultivated independently of its engulfed alga cell. The inner pair of membranes is coral host, which provides a model to study apicom- equivalent to the outer and inner envelopes of the plexan evolution and what makes the apicoplast chloroplast, which evolved from the cell surface envel- essential (Moore et al. 2008). ope of the engulfed cyanobacterium by the primary host. (b) The apicoplast and the mitochondrion What is not agreed however is the nature of the sec- constitute the sticky duo ondary endosymbiont. One school contends that the One striking feature of the apicoplast is its close proxi- endosymbiont was a green alga (Kohler et al. 1997; mity to the single mitochondrion (van Dooren et al. Funes et al. 2002), whereas another school favours a 2006). Early electron micrographs of various species red algal endosymbiont. In our view, a red algal endo- of Plasmodium revealed a ‘spherical body’ in intimate symbiont is now proven beyond much doubt by the association with the single mitochondrion within the discovery of the photosynthetic apicomplexan Chro- parasites (Aikawa 1966; Hepler et al. 1966). Initially mera, which clearly has a plastid derived from a red the ‘spherical body’ was speculated to be a metabolic alga that has the same origins as the apicoplast. A store for the mitochondrion (Aikawa 1966; Hepler red algal origin for the apicoplast is also part of a et al. 1966), but we now know this body as the apico- much broader hypothesis for secondary endosymbiotic plast (McFadden et al. 1996; Kohler et al. 1997). origin of plastids in a large group of protists known as Indeed the closeness of the two organelles seems the chromalveolates. The chromalveolate theory pro- attributable to their metabolic dependences (Ralph poses that all algae belonging to Chromalveolata et al. 2004; van Dooren et al. 2006) discussed below. possess secondary red plastids acquired by a single During its life cycle the Plasmodium parasite under- common endosymbiotic event, whereby a rhodophyte goes three rounds of asexual reproduction: alga is engulfed by a heterotrophic eukaryotic host erythrocytic schizogony, sporogony within the oocyst (Cavalier-Smith 1999). This supergroup includes Api- in the mosquito’s midgut wall, and exo-erythrocytic complexa, Dinophyta, Ciliophora, Heterokonts, schizogony within the liver cell. What happens to the Haptophyta and Cryptophyta. In support of the chro- apicoplast during these cell proliferation stages? Gen- malveolate hypothesis, structural characteristics of etic manipulation and reporter constructs have the plastid
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