Genomic reduction and evolution of novel genetic membranes and protein-targeting machinery in eukaryote-eukaryote chimaeras (meta-algae)

Abstract

Chloroplasts originated just once, from cyanobacteria enslaved by a biciliate protozoan to form the plant kingdom (green plants, red and glaucophyte algae), but subsequently, were laterally transferred to other lineages to form eukaryote-eukaryote chimaeras or meta-algae. This process of secondary symbiogenesis (permanent merger of two phylogenetically distinct eukaryote cells) has left remarkable traces of its evolutionary role in the more complex topology of the membranes surrounding all non-plant (meta-algal) chloroplasts. It took place twice, soon after green and red algae diverged over 550 Myr ago to form two independent major branches of the eukaryotic tree (chromalveolates and cabozoa), comprising both meta-algae and numerous secondarily non-photosynthetic lineages. In both cases, enslavement probably began by evolving a novel targeting of endomembrane vesicles to the perialgal vacuole to implant host porter proteins for extracting photosynthate. Chromalveolates arose by such enslavement of a unicellular red alga and evolution of chlorophyll c to form the kingdom Chromista and protozoan infrakingdom Alveolata, which diverged from the ancestral chromalveolate chimaera. Cabozoa arose when the common ancestor of euglenoids and cercozoan chlorarachnean algae enslaved a tetraphyte green alga with chlorophyll a and b. I suggest that in cabozoa the endomembrane vesicles originally budded from the Golgi, whereas in chromalveolates they budded from the endoplasmic reticulum (ER) independently of Golgi-targeted vesicles, presenting a potentially novel target for drugs against alveolate Sporozoa such as malaria parasites and Toxoplasma. These hypothetical ER-derived vesicles mediated fusion of the perialgal vacuole and rough ER (RER) in the ancestral chromist, placing the former red alga within the RER lumen. Subsequently, this chimaera diverged to form cryptomonads, which retained the red algal nucleus as a nucleomorph (NM) with approximately 464 protein-coding genes (30 encoding plastid proteins) and a red or blue phycobiliprotein antenna pigment, and the chromobiotes (heterokonts and haptophytes), which lost phycobilins and evolved the brown carotenoid fucoxanthin that colours brown seaweeds, diatoms and haptophytes. Chromobiotes transferred the 30 genes to the nucleus and lost the NM genome and nuclear-pore complexes, but retained its membrane as the periplastid reticulum (PPR), putatively the phospholipid factory of the periplastid space (former algal cytoplasm), as did the ancestral alveolate independently. The chlorarachnean NM has three minute chromosomes bearing approximately 300 genes riddled with pygmy introns. I propose that the periplastid membrane (PPM, the former algal plasma membrane) of chromalveolates, and possibly chlorarachneans, grows by fusion of vesicles emanating from the NM envelope or PPR. Dinoflagellates and euglenoids independently lost the PPM and PPR (after diverging from Sporozoa and chlorarachneans, respectively) and evolved triple chloroplast envelopes comprising the original plant do...

The excavate protozoan phyla Metamonada Grasse emend. (Anaeromonadea, Parabasalia, Carpediemonas, Eopharyngia) and Loukozoa emend. (Jakobea, Malawimonas): their evolutionary affinities and new higher taxa

“…1 is correct, at least nine plastid losses must be inferred within excavates, but, as molecular evidence independent of the cabozoan hypothesis (and arising since its proposal) suggests that the ancestral excavate may have been photosynthetic, these are no longer additional assumptions of the theory; indeed, this independent evidence goes some way to corroborate the theory. Fourteen plastid losses within the cabozoa is similar to the number of mitochondrial 'losses' (or, more properly, conversions to hydrogenosomes or mitosomes) that have occurred in eukaryotes and is therefore a rather weak disadvantage of the theory compared with the advantage of assuming a common origin for protein-targeting into the plastid of euglenoids and chlorarachneans (Cavalier-Smith, 2003). If we had a chlorarachnean chloroplast genome sequence, it might help us to decide whether or not the cabozoan theory is correct.…”

“…This gene is of key significance for excavate phylogeny, as the presence in the percolozoan Naegleria of a version of this gene that is most closely related to that of plant and chromist chloroplasts (and more distantly to cyanobacteria) strongly indicates that the common ancestor of discicristates had a plastid. Whether this was the secondary symbiogenetic ancestor of the euglenoid chloroplast, as I contend (Cavalier-Smith, 2002c, 2003, or reflects an earlier primary origin of chloroplasts from cyanobacteria than usually supposed, as Andersson & Roger (2002) tend to think, is irrelevant to the fact that it provides evidence that at least one of the two excavate superphyla was ancestrally photosynthetic. Both on the cabozoan theory (Cavalier-Smith, 1999) and on the theory of a primary origin of plastids before the divergence of Plantae and Excavata (Andersson & Roger, 2002) Fig.…”

“…Very probably, the ancestral chlorarachneans were benthic (Ishida et al, 1999), as are most heterotrophic Cercozoa, making it likely that the cabozoan ancestor was a benthic photophagotroph. There is increasing evidence that Cercozoa and Retaria (Foraminifera and Radiolaria) are a clade designated 'core Rhizaria' (see Cavalier-Smith, 2003;Cavalier-Smith & Chao, 2003b). Thus, on the cabozoan theory, all excavates, Cercozoa and Retaria are cabozoans; these taxa do form a clade on a recent rRNA tree (Cavalier-Smith, 2002a).…”

“…I consider that the origin of all three enzymes discussed above is more simply explained by the cabozoan theory of secondary symbiogenesis, which I have recently revised in the light of new evidence from protein targeting and genome sequencing (Cavalier-Smith, 2003), rather than by three independent lateral gene transfers. One limitation in using the glucokinase and GPI gene transfers as arguments for the holophyly of Trichozoa is that, on the cabozoan theory, they must have entered the cabozoan chimaera prior to the divergence of Metamonada from Loukozoa and might also be present in some other cabozoan lineages, which are very poorly sampled for these genes or their enzymes.…”

“…The latter is much more likely, as tetraphyte green algae are the very group that donated the green plastid to the ancestor of the euglenoids, the only excavate group currently with photosynthetic members (Cavalier-Smith, 1993a). According to the cabozoan theory, this lateral transfer of green algal plastids took place not within the euglenoids, as commonly assumed (Gibbs, 1978;Delwiche, 1999), but in the common ancestor of Euglenozoa and Cercozoa, the phylum containing chlorarachnean algae, which also have green chloroplasts of secondary symbiogenetic origin (probably also from a tetraphyte source: Cavalier-Smith, 1999, 2003. On this hypothesis, for which there are strong arguments based on considerations of parsimony in the evolution of protein targeting (Cavalier-Smith, 1999, 2003, all excavates must be derived from a photosynthetic common ancestor by plastid losses.…”