Trends in Ecology & Evolution
ReviewSomething borrowed, something green: lateral transfer of chloroplasts by secondary endosymbiosis
Abstract
New molecular data confirm what electron microscopists long suspected — fusion of two different eukaryotic cells into a single more-complex cell created novel groups of protists. By engulfing an algal cell and putting it to work as a solar-powered food factory, heterotrophic protozoans became autotrophic. Drastically reduced, the engulfed cell now exists as an organelle in the host cell. Such blending of lineages was perhaps a driving force in early eukaryotic diversification.
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Cited by (75)
Endosymbiosis, cell evolution, and speciation
2005, Theory in BiosciencesIn 1905, the Russian biologist C. Mereschkowsky postulated that plastids (e.g., chloroplasts) are the evolutionary descendants of endosymbiotic cyanobacteria-like organisms. In 1927, I. Wallin explicitly postulated that mitochondria likewise evolved from once free-living bacteria. Here, we summarize the history of these endosymbiotic concepts to their modern-day derivative, the “serial endosymbiosis theory”, which collectively expound on the origin of eukaryotic cell organelles (plastids, mitochondria) and subsequent endosymbiotic events. Additionally, we review recent hypotheses about the origin of the nucleus. Model systems for the study of “endosymbiosis in action” are also described, and the hypothesis that symbiogenesis may contribute to the generation of new species is critically assessed with special reference to the secondary and tertiary endosymbiosis (macroevolution) of unicellular eukaryotic algae.
The apicoplast: A plastid in plasmodium falciparum and other apicomplexan parasites
2003, International Review of CytologyApicomplexan parasites cause severe diseases such as malaria, toxoplasmosis, and coccidiosis (caused by Plasmodium spp., Toxoplasma, and Eimeria, respectively). These parasites contain a relict plastid—termed “apicoplast”—that originated from the engulfment of an organism of the red algal lineage. The apicoplast is indispensable but its exact role in parasites is unknown. The apicoplast has its own genome and expresses a small number of genes, but the vast majority of the apicoplast proteome is encoded in the nuclear genome. The products of these nuclear genes are posttranslationally targeted to the organelle via the secretory pathway courtesy of a bipartite N-terminal leader sequence. Apicoplasts are nonphotosynthetic but retain other typical plastid functions such as fatty acid, isoprenoid and heme synthesis, and products of these pathways might be exported from the apicoplast for use by the parasite. Apicoplast pathways are essentially prokaryotic and therefore excellent drug targets. Some antibiotics inhibiting these molecular processes are already in chemotherapeutic use, whereas many new drugs will hopefully spring from our growing understanding of this intriguing organelle.
Progress with parasite plastids
2002, Journal of Molecular BiologyThis review offers a snapshot of our current understanding of the origin, biology, and metabolic significance of the non-photosynthetic plastid organelle found in apicomplexan parasites. These protists are of considerable medical and veterinary importance world-wide, Plasmodium spp., the causative agent of malaria being foremost in terms of human disease. It has been estimated that ∼8% of the genes currently recognized by the malarial genome sequencing project (now nearing completion) are of bacterial/plastid origin. The bipartite presequences directing the products of these genes back to the plastid have provided fresh evidence that secondary endosymbiosis accounts for this organelle‘s presence in these parasites. Mounting phylogenetic evidence has strengthened the likelihood that the plastid originated from a red algal cell. Most importantly, we now have a broad understanding of several bacterial metabolic systems confined within the boundaries of the parasite plastid. The primary ones are type II fatty acid biosynthesis and isoprenoid biosynthesis. Some aspects of heme biosynthesis also might take place there. Retention of the plastid‘s relict genome and its still ill-defined capacity to participate in protein synthesis might be linked to an important house-keeping process, i.e. guarding the type II fatty acid biosynthetic pathway from oxidative damage. Fascinating observations have shown the parasite plastid does not divide by constriction as in typical plants, and that plastid-less parasites fail to thrive after invading a new cell. The modes of plastid DNA replication within the phylum also have provided surprises. Besides indicating the potential of the parasite plastid for therapeutic intervention, this review exposes many gaps remaining in our knowledge of this intriguing organelle. The rapid progress being made shows no sign of slackening.
On the origin of sex as vaccination
2002, Journal of Theoretical BiologyIn the theory of the origin of sex as vaccination, I propose that the eukaryote genome accreted from prokaryan symbiont genomes in numerous rounds of lateral gene transfer during which sex diverged from unilateral parasitic infection, as an increasingly ritualized, reciprocal vaccination against superinfection. Sex-as-syngamy (fusion sex) arose when infected proto-eukaryan hosts began swapping nuclearized genomes containing coevolved, vertically transmitted (“attenuated”) symbionts that conveyed protection against horizontal superinfection by more virulent symbionts. Sex-as-meiosis (fission sex) evolved as a host strategy to uncouple (and thereby emasculate) the acquired symbiont genomes. The chimeric nature, distribution over discrete chromosomes, and mosaic composition of the eukaryan nuclear genome derive from multiple rounds of acquiring and uncoupling prokaryan genomes. Genome compatibility-based recognition of self and mates came to define sex, mate choice, and the biological species. By generating unique individuality, sex now persists as an elaborate (hence tamper-proof) periodic device for an organism to thwart both endo- and exogenous challengers, and stay ahead of an environment whose capriciousness may largely result from the success of its own forebears.
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Bella gerant alii—
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Tu felix Austria nube!
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May all others make war –
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You, lucky Austria, marry!
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(in reference to the House of Habsburg's way of amassing an empire)
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Divide et impera!
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Divide and rule!
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(attributed to Louis XI of France by Prosper Mé rimée)
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Translocation of proteins across the multiple membranes of complex plastids
2001, Biochimica et Biophysica Acta - Molecular Cell ResearchSecondary endosymbiosis describes the origin of plastids in several major algal groups such as dinoflagellates, euglenoids, heterokonts, haptophytes, cryptomonads, chlorarachniophytes and parasites such as apicomplexa. An integral part of secondary endosymbiosis has been the transfer of genes for plastid proteins from the endosymbiont to the host nucleus. Targeting of the encoded proteins back to the plastid from their new site of synthesis in the host involves targeting across the multiple membranes surrounding these complex plastids. Although this process shows many overall similarities in the different algal groups, it is emerging that differences exist in the mechanisms adopted.
One of the most citated characteristics of eukaryotic cells are mitochondria and in the case of phototrophic cells, the plastids. These organelles are of eubacterial origin and contain a remnant genome. Here, we present hypotheses concerning the origin of the first mitochondrium-harboring cell and show the evolution of primary, secondary and tertiary plastids. Furthermore we discuss models explaining why plastids have to maintain their own genome.