Phylogeny and evolution of apicoplasts and apicomplexan parasites

https://doi.org/10.1016/j.parint.2014.10.005Get rights and content

Highlights

  • The apicoplast has evolved through secondary endosymbiosis of a red alga.

  • The apicoplast has a genome around 30–40 kb.

  • The repertoire and arrangement of the apicoplast genes are different among genera.

  • Genes in the apicoplast genome can be useful markers for phylogeny of Plasmodium.

Abstract

The phylum Apicomplexa includes many parasitic genera of medical and veterinary importance including Plasmodium (causative agent of malaria), Toxoplasma (toxoplasmosis), and Babesia (babesiosis). Most of the apicomplexan parasites possess a unique, essential organelle, the apicoplast, which is a plastid without photosynthetic ability. Although the apicoplast is considered to have evolved through secondary endosymbiosis of a red alga into the common ancestral cell of apicomplexans, its evolutionary history has been under debate until recently. The apicoplast has a genome around 30–40 kb in length. Repertoire and arrangement of the apicoplast genome-encoded genes differ among apicomplexan genera, although within the genus Plasmodium these are almost conserved. Genes in the apicoplast genome may be useful markers for Plasmodium phylogeny, because these are single copy (except for the inverted repeat region) and may have more phylogenetic signal than the mitochondrial genome that have been most commonly used for Plasmodium phylogeny. This review describes recent studies concerning the evolutionary origin of the apicoplast, presents evolutionary comparison of the primary structures of apicoplast genomes from apicomplexan parasites, and summarizes recent findings of malaria phylogeny based on apicoplast genome-encoded genes.

Introduction

Most members of the phylum Apicomplexa are obligate parasites with some members being causative agents for diseases in vertebrates. Malaria, which is caused by members of the genus Plasmodium, is one of the most threatening infectious diseases of man, and is a serious public health concern in the tropics and subtropics with an estimated 219 million cases and 660,000 malaria deaths in 2010 [1]. Other important apicomplexan human parasites are Toxoplasma gondii and Cryptosporidium parvum. T. gondii is a zoonotic protozoan that infects more than 200 species of mammals and birds. Most of the infections in humans are asymptomatic; however it can cause severe diseases in the fetus during pregnancy [2]. C. parvum is a major public health concern causing diarrheal outbreaks of cryptosporidiosis even in urban areas through parasites in the water supply [3], [4]. Further, numerous infectious diseases in wild and domesticated animals are caused by members of the apicomplexan genera Babesia, Eimeria, Theileria, and Sarcocystis. Diseases caused by these apicomplexan parasites can result in serious economic loss. Although these disease-causing species have been extensively studied (e.g., [5], [6], [7], [8]), little is known about the diversity and evolution of apicomplexans and their photosynthetic relatives.

Apicomplxans are phylogenetically positioned in the large protist group Alveolata together with ciliates and dinoflagellates, with the latter being closely related to apicomplexans (e.g., [9], [10], [11]). Apicomplexans are characterized by the presence of an assembly of organelles called the apical complex at the anterior apex of the cell that is responsible for the invasion of the parasite into host cells [12]. Most apicomplexan parasites are believed to possess the apicoplast, a plastid with no photosynthetic ability, which is essential for cell survival (e.g., [13], [14]). The apicoplast has its own genome that mainly encodes the transcription and translation related genes necessary for plastid gene expression. Based on the analyses of the nuclear-encoded, apicoplast targeted proteins and by analogy to plastids, functions of the P. faiciparum apicoplast were proven or predicted to be for fatty acid synthesis, isoprenoid synthesis, heme synthesis in collaboration with the mitochondrion, and others (e.g., [15]). Since the apicoplast must contribute to these metabolic pathways of plastid origin which are different from those in host cells, such pathways have attracted attention as potential drug targets.

The apicoplast is likely to have evolved through secondary endosymbiosis; that is, a common ancestor of apicomplexans engulfed a eukaryotic alga as an endosymbiont and enslaved it as a plastid surrounded by more than two membranes (Fig. 1) (e.g., [16]). The endosymbiont that gave rise to the apicoplast has recently been shown to have a red algae origin based on the discovery of photosynthetic relatives of apicomplexan parasites [17], [18], [19]. On the other hand, in some apicoplast-lacking apicomplexan lineages including the genus Cryptosporidium [20], the apicoplast is likely to have been secondarily lost (Fig. 1). From 1996 through 2014, sequences of the apicoplast genomes from various apicomplexan parasites have been reported [21], [22], [23], [24], [25], [26]. These data are important for tracing the evolutionary history of apicoplasts and apicomplexan parasites. Elucidation of the phylogeny, evolution, and biology of the apicomplexan parasites is essential for better understanding the pathophysiology and epidemiology of these medically and veterinarily important parasites.

Here, we review recent phylogenetic studies on the evolution of apicoplasts and apicomplexan parasites. First, we briefly describe phylogenetic studies concerning the evolutionary origin of the apicoplast. Then, we evolutionarily compare apicoplast genomes of apicomplexan parasites. Finally, we summarize recent findings from phylogeny of malaria parasites inferred from apicoplast genome-encoded genes.

Section snippets

Evolutionary origin of apicoplasts

Apicoplast DNA was first isolated from avian malaria parasite, Plasmodium lophurae, as a 35-kb extrachromosomal DNA fragment [27], [28], but was initially considered as a mitochondrial DNA (mtDNA). More than 10 years later, other extrachromosomal linear DNA fragments, those around 6 kb in length, were isolated from other Plasmodium spp., and demonstrated to be genuine mtDNA [29], [30]. Further characterization of the 35-kb DNA molecule showed that it was circular and sequence similarity and

Structure of apicoplast genomes

The complete gene map of the apicoplast genome was first reported for P. falciparum [21], followed by reports for T. gondii (submitted to EMBL, U87145) and for Eimeria tenella [22]. In both the Theileria parva [23] and Babesia bovis [24] whole genome databases and apicoplast genome sequences have been reported. The genome of each species commonly encodes rRNAs, tRNAs, ribosomal proteins, bacterial-type RNA polymerase subunits, EF-Tu, and ClpC protein. Apicoplast genomes for which sequences are

Phylogeny of malaria parasites inferred from apicoplast genome-encoded genes

Genes encoded in the apicoplast genome (− 35 kb) can be one of the useful markers for resolving the phylogeny of Plasmodium species, because these genes are single copy, except for the inverted repeat region, and most importantly, have greater phylogenetic signal than the mitochondrial genome (− 6 kb) that have been most commonly used for Plasmodium phylogeny [53], [54], [55], [56]. In addition, no significant compositional heterogeneity for any genes was detected among Plasmodium species [57],

Conclusion

Accumulation of the genome sequence data of apicoplast and discovery of photosynthetic ancestral lineages closely related to apicomplexan parasites have led us to understand evolutionary process of the apicoplast and apicomplexan parasites. Since the apicoplast genome encodes more genes than does the mitochondrial genome, it could be a good phylogenetic marker for analyzing inter-species relationships within genera, as already shown for the genus Plasmodium. In order to elucidate the evolution

Acknowledgments

We thank Dr. Nirianne M. Q. Palacpac (Osaka Univ.) for providing language help and proof reading the article.

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