Evolution

Evidence points to a single origin for mitochondria, with an a-proteobacterial ancestor (reviewed in Lang et al., 1999). Despite earlier suggestions that there might be more than one origin of chloroplasts, the most recent data now point to a single endosym-biotic event there as well, with the engulfed organism being a photosynthetic cyanobacterium (reviewed in Gray, 1993; McFadden and van Dooren, 2004). The characteristic double membranes of both mitochondria and chloroplasts are believed to reflect the endosymbiotic event that produced them. As the relationship evolved to symbiosis, many genes in the engulfed partner were transferred to the nucleus, and those gene products essential to organellar function were translated in the cytosol and subsequently imported across two membranes into the organelle. However, a number of organisms have not just two, but three or four bounding membranes around their chloroplasts. To explain this, the endosymbiont hypothesis was expanded to include secondary endosymbiosis (Figure 9.3), in

FIGURE 9.3 Secondary endosymbiosis entails engulfment of an algal cell by a eukaryote (A); loss of genes from the algal cell, with some transferred to the host nucleus (B); and finally loss of the algal nucleus, leaving behind an organelle bounded by four membranes (C). Further steps may reduce the number of bounding membranes to three. If plastid; M, mitochondrion; N, nucleus. Blue, host cell; green algal cell. This figure is reproduced in color in the color plate section.

FIGURE 9.3 Secondary endosymbiosis entails engulfment of an algal cell by a eukaryote (A); loss of genes from the algal cell, with some transferred to the host nucleus (B); and finally loss of the algal nucleus, leaving behind an organelle bounded by four membranes (C). Further steps may reduce the number of bounding membranes to three. If plastid; M, mitochondrion; N, nucleus. Blue, host cell; green algal cell. This figure is reproduced in color in the color plate section.

which both partners are eukaryotes (reviewed in Archibald and Keeling, 2002). All cases known to date involve engulfment of a photosynthetic alga which already bears a chloroplast. The two inner membranes are believed to be the original chloro-plast membranes, the third membrane representing the outer membrane of the algal cell, and the outermost membrane deriving from the host endomem-brane system. Loss of one membrane has occurred in some organisms. Euglenoids (three membranes), dinoflagellates (usually three membranes), chlor-arachniophyte algae (four membranes), and cryptomonad algae (four membranes with the outermost appearing fused to the host rough ER) are prominent examples of organisms with secondary chloroplasts.

The plethora of other membranous structures in T. gondii and P falciparum cells has made it challenging to determine the number of membranes surrounding the apicoplast. Numerous electron micrographs show four membranes surrounding the T. gondii apicoplast, and that number is generally accepted (Köhler et al., 1997; McFadden and Roos, 1999). In a recent paper Köhler (2005) has argued, based on transmission electron micrographs, that the T. gondii apicoplast has only two bounding membranes, and is in fact a primary rather than secondary plastid. However, this suggestion is inconsistent with the trafficking mechanism employed to target nuclearly encoded proteins into the apicoplast (see section 9.2.7). Reports for Plasmodium are mixed. Hopkins et al. (1999) described three bounding membranes and numerous adjacent membrane whorls, while McFadden and Roos (1999) reported four membranes, as in T. gondii and several other apicomplexans (reviewed in Waller and McFadden, 2005). Methods of sample preparation for electron microscopy can affect preservation of membrane structure and may explain the differences reported.

Cryptomonad and chlorarachniophyte algae are especially intriguing. Not only are their chloro-plasts surrounded by four membranes, but a remnant nucleus, the nucleomorph, nestles between the second and third membranes. Nucleomorph genomes are much reduced, with just three small chromosomes totaling a few hundred kb of DNA (Gilson and McFadden, 1996; Douglas et al., 2001). Despite their small size, these genomes encode components for their own perpetuation and expression plus a few other proteins, including some destined for import to the chloroplast (Gilson and McFadden, 1996, 1997; Zauner et al., 2000). Most of the genes needed for photosynthesis have been shifted to the nucleus, and their protein products are trafficked across all four membranes. In contrast to these algae, apicomplexans have lost the endosymbiont nucleus and photosynthesis-related genes, which they no longer need as intracellular parasites. However, they continue to employ the apicoplast as a synthetic compartment (see section 9.2.9).

The movement of foreign genes into a host's nucleus is called lateral gene transfer (reviewed in Doolittle et al., 2003; Bapteste et al., 2004). As noted above, some transferred genes encode products that are trafficked back to the organelle. Others may provide the host with new synthetic capabilities in the cytosol or other compartments. Still others may be redundant, allowing for the evolution of new functions, while some may simply replace the corresponding endogenous genes. The rapidly increasing pool of genome sequences has greatly accelerated our understanding of lateral gene transfer, showing it to be widespread and of considerable scope. Secondary endosymbiosis permits additional lateral gene transfer, from both the nucleus and the chloroplast of the endosym-biont to the nucleus of the host. Importantly, that means that genes from the endosymbiont's nucleus, which may have no relationship to plastid function, may still provide insights useful for deciphering the history of secondary endosymbionts. Phylogenetic analyses of apicomplexans have considered genes encoded by the apicoplast genome, nuclear genes encoding apicoplast-targeted proteins, and genes not related to apicoplast function.

A recurring question in analyses of apicom-plexan evolution is the identity of the secondary endosymbiont: whether it was a red or a green alga. This question has not been resolved, since data supporting both contentions have been gathered (Table 9.1). Initial analyses showed that rpoB (Gardner et al., 1994b) and rpoC1 (Howe, 1992)

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