The Non‐Photosynthetic Plastid in Malarial Parasites and Other Apicomplexans is Derived from Outside the Green Plastid Lineage¹

Abstract

The discovery of a non-photosynthetic plastid genome in Plasmodium falciparum and other apicomplexans has provided a new drug target, but the evolutionary origin of the plastid has been muddled by the lack of characters, that typically define major plastid lineages. To clarify the ancestry of the plastid, we undertook a comprehensive analysis of all genomic characters shared by completely sequenced plastid genomes. Cladistic analysis of the pattern of plastid gene loss and gene rearrangements suggests that the apicomplexan plastid is derived from an ancestor outside of the green plastid lineage. Phylogenetic analysis of primary sequence data (DNA and amino acid characters) produces results that are generally independent of the analytical method, but similar genes (i.e., rpoB and rpoC) give similar topologies. The conflicting phylogenies in primary sequence data sets make it difficult to determine the the exact origin of the apicomplexan plastid and the apparent artifactual association of apicomplexan and euglenoid sequences suggests that DNA sequence data may be an inappropriate set of characters to address this phylogenetic question. At present we cannot reject our null hypothesis that the apicomplexan plastid is derived from a shared common ancestor between apicomplexans and dinoflagellates. During the analysis, we noticed that the Plasmodium tRNA-Met is probably tRNA-fMet and the tRNA-fMet is probably tRNA-Ile. We suggest that P. falciparum has lost the elongator type tRNA-Met and that similar to metazoan mitochondria there is only one species of methionine tRNA. In P. falciparum, this has been accomplished by recruiting the fMet-type tRNA to dually function in initiation and elongation. The tRNA-Ile has an unusual stem-loop in the variable region. The insertion in this region appears to have occurred after the primary origin of the plastid and further supports the monophyletic ancestory of plastids.

Mining thePlasmodiumgenome database to define organellar function: what does the apicoplast do?

“…In other words, a common ancestor of all apicomplexan parasites 'ate' a eukaryotic alga, whose ancestor had previously engulfed a cyanobacterium, and progeny parasites retained the genome of the algal plastid! Although the tufA phylogeny suggests a green algal ancestry for this DNA, other work indicates that a red algal origin is more probable (McFadden et al 1997;Blanchard & Hicks 1999). More recent studies hint that the secondary endosymbiotic transfer of plastid DNA may have pre-dated the divergence of apicomplexans, dinoflagellates and ciliates (the Alveolata) (Fast et al 2001).…”

“…The apicoplast arose by secondary endosymbiosis: a common ancestor of apicomplexan parasites engulfed a eukaryotic alga (probably a red alga), and retained the algal plastid (Palmer & Delwiche 1996). This event may have occurred prior to the divergence of apicomplexans, dinoflagellates and ciliates (Fast et al 2001). and the plastid genomes of algae, plants, and other alveolates, it is clear that apicomplexan parasites harbour a true plastid, rather than a 'plastid-like organelle' (Kö hler et al 1997;Blanchard & Hicks 1999).…”

“…Daughter parasites are assembled and packaged within the mother, ultimately capturing the mother's plasma membrane and sloughing off a residual body consisting of indigestible components of the mother, and other products. Perhaps the strangest of all intracellular organelles is the plastida chloroplast-like organelle acquired by secondary endosymbiosis of an algal ancestor, and retention of the algal plastid as a distinct (albeit non-photosynthetic) organelle (Kö hler et al 1997;McFadden et al 1997;Wilson & Williamson 1997;Blanchard & Hicks 1999;McFadden 1999;Roos et al 1999b). The origin and function of the apicoplast has been the subject of much interest, and provides the focus of this paper, as characterizing this organelle serves as a useful case study for genome database mining efforts and effective integration of results from diverse parasites and experimental systems.…”

Plastid Origin and Evolution

“…The finding suggests the displacement of the cyanobacterial gene copy via gene duplication before the divergence of dinoflagellates and apicomplexans, therefore lending support to the idea that apicoplasts are derived from secondary plastids, similar to the other chromalveolates. Phylogenetic analysis of plastid-targeted genes (Fast et al, 2001) and a structural analysis of the apicoplast (Blanchard and Hicks, 1999) in apicomplexans have indicated the likely red algal origin of the apicoplast. The architecture of the apicoplast genome is consistent with a red algal ancestry (Blanchard and Hicks, 1999), although green algal-derived genes have also been documented (Funes et al, 2002).…”

“…Phylogenetic analysis of plastid-targeted genes (Fast et al, 2001) and a structural analysis of the apicoplast (Blanchard and Hicks, 1999) in apicomplexans have indicated the likely red algal origin of the apicoplast. The architecture of the apicoplast genome is consistent with a red algal ancestry (Blanchard and Hicks, 1999), although green algal-derived genes have also been documented (Funes et al, 2002). These organelles have subsequently lost their photosynthetic capability likely due to the transition to obligate parasitism.…”