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Endosymbiosis: Double-Take on Plastid Origins

2006; Elsevier BV; Volume: 16; Issue: 17 Linguagem: Inglês

10.1016/j.cub.2006.08.006

1879-0445

John M. Archibald,

Genomics and Phylogenetic Studies

Plastids — the light-harvesting machines of plant and algal cells — evolved from cyanobacteria inside a eukaryotic host more than a billion years ago. New data reveal that a mysterious unicellular alga acquired its photosynthetic apparatus much more recently than other eukaryotes, affording a second look at the primary endosymbiotic origin of plastids. Plastids — the light-harvesting machines of plant and algal cells — evolved from cyanobacteria inside a eukaryotic host more than a billion years ago. New data reveal that a mysterious unicellular alga acquired its photosynthetic apparatus much more recently than other eukaryotes, affording a second look at the primary endosymbiotic origin of plastids. "I call this experiment 'replaying life's tape.' You press the rewind button and, making sure you thoroughly erase everything that actually happened, let the tape run again and see if the repetition looks at all like the original."Stephen J. Gould (Wonderful Life) In his famous treatise on the Cambrian fossils of British Columbia's Burgess Shale, Stephen J. Gould [1Gould S.J. Wonderful Life.The Burgess Shale and the Nature of History. First Edition. W.W. Norton and Company, New York1989Google Scholar] considered the role of chance in evolution and posed the 'thought experiment' quoted above. Would life ever evolve the same way twice? The largely historical nature of evolutionary biology makes this an extremely difficult question, yet on rare occasions evolution provides us with the means to glimpse an answer. Such is the case with the origin of eukaryotic photosynthesis. In this issue, Yoon et al.[2Yoon H.S. Reyes-Prieto A. Bhattacharya D. Minimal plastid genome evolution in the Paulinella endosymbiont.Curr. Biol. 2006; 16: R670-R672Abstract Full Text Full Text PDF PubMed Scopus (78) Google Scholar] report evidence that the unicellular alga Paulinella chromatophora acquired its light-harvesting abilities through the uptake of a Synechococcus-type cyanobacterium completely independent of — and much more recently than — the endosymbiosis that gave rise to the plastids of all other eukaryotes. Detailed genomic studies of P. chromatophora promise to elucidate the molecular processes underlying the transition from free-living bacterium to fully integrated eukaryotic organelle. Oxidative photosynthesis first evolved in cyanobacteria [3Blankenship R.E. Protein structure, electron transfer and evolution of prokaryotic photosynthetic reaction centers.Ant. Van Leeuwen. 1994; 65: 311-329Crossref PubMed Scopus (46) Google Scholar] and its subsequent spread to eukaryotes via 'primary' endosymbiosis ranks as one of the most important events in the history of life. Three eukaryotic lineages — green algae (and their multi-cellular cousins, land plants), red algae, and glaucophytes — harbor plastids whose ancestry can be traced directly back to the cyanobacterial endosymbiont [4Keeling P.J. Diversity and evolutionary history of plastids and their hosts.Am. J. Bot. 2004; 91: 1481-1493Crossref PubMed Scopus (282) Google Scholar, 5Palmer J.D. The symbiotic birth and spread of plastids: how many times and whodunnit?.J. Phycol. 2003; 39: 4-11Crossref Scopus (192) Google Scholar]. While green and red algal plastids are known to have diffused across the eukaryotic tree by 'secondary' (eukaryote–eukaryote) endosymbiosis [6Bhattacharya D. Yoon H.S. Hackett J.D. Photosynthetic eukaryotes unite: endosymbiosis connects the dots.Bioessays. 2003; 26: 50-60Crossref Scopus (232) Google Scholar], it is widely believed that primary plastids evolved from cyanobacteria only once in life's history (for example [7Rodriguez-Ezpeleta N. Brinkmann H. Burey S.C. Roure B. Burger G. Loffelhardt W. Bohnert H.J. Philippe H. Lang B.F. Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes.Curr. Biol. 2005; 15: 1325-1330Abstract Full Text Full Text PDF PubMed Scopus (401) Google Scholar]). Or did they? Mounting evidence suggests that the photosynthetic organelles of the enigmatic fresh-water amoeba P. chromatophora (Figure 1) represent a second primary endosymbiosis in its early stages. First isolated by the German biologist Robert Lauterborn in 1894 [8Lauterborn R. Protozoenstudien II. Paulinella chromatophora nov. gen., nov. spec., ein beschalter Rhizopode des Süßwassers mit blaugrünen chromatophorenartigen Einschlüssen.Z. Wiss. Zool. 1895; 59: 537-544Google Scholar, 9Melkonian M. Mollenhauer D. Robert Lauterborn (1869–1952) and his Paulinella chromatophora.Protist. 2005; 156: 253-262Crossref PubMed Scopus (30) Google Scholar], this organism has a long but sporadic history in the scientific literature, having been discovered at a time when the evolutionary connections between cyanobacteria and plastids were far from clear. Remarkably, in his initial description of P. chromatophora, Lauterborn [8Lauterborn R. Protozoenstudien II. Paulinella chromatophora nov. gen., nov. spec., ein beschalter Rhizopode des Süßwassers mit blaugrünen chromatophorenartigen Einschlüssen.Z. Wiss. Zool. 1895; 59: 537-544Google Scholar] is said to have touched "on the possible endosymbiotic origin of the chromatophores (plastids) without explicitly advancing this hypothesis (as did Mereschkovsky 10 years later)" [9Melkonian M. Mollenhauer D. Robert Lauterborn (1869–1952) and his Paulinella chromatophora.Protist. 2005; 156: 253-262Crossref PubMed Scopus (30) Google Scholar]. The rarity of P. chromatophora in nature and its resistance to stable culturing has meant that progress towards understanding the significance of its endosymbiont has been slow. Why is P. chromatophora so interesting? Each cell has one or two cytoplasmic bodies, historically known as cyanelles, which resemble free-living cyanobacteria much more so than they resemble canonical plastids. The bodies themselves cannot be cultured in isolation, do not appear to reside within a food vacuole, and divide synchronously with their host [10Hoogenraad H.R. Zur Kenntnis der Fortpflanzung von Paulinella chromatophora Lauterb.Zool. Anz. 1927; 72: 140-150Google Scholar, 11Johnson P.W. Hargraves P.E. Sieburth J.M. Ultrastructure and ecology of Calycomonas ovalis Wulff, 1919, (Chrysophyceae) and its redescription as a testate rhizopod, Paulinella ovalis n. comb. (Filosea: Euglyphina).J. Protozool. 1988; 35: 618-626Crossref Scopus (42) Google Scholar, 12Kies L. Elektronenmikroskopische Untersuchungen an Paulinella chromatophora Lauterborn, einer Thekamöbe mit blaugrünen Endosymbionten (Cyanellen).Protoplasma. 1974; 80: 69-89Crossref PubMed Scopus (78) Google Scholar, 13Kies L. Kremer B.P. Function of cyanelles in the Tecamoeba Paulinella chromatophora.Naturewissenschaften. 1979; 66: 578-579Crossref Scopus (36) Google Scholar], suggesting at least a certain level of host–endosymbiont integration. Most intriguingly, a close relative of P. chromatophora, P. ovalis, is not photosynthetic but actively feeds on cyanobacteria that are similar to members of the genus Synechococcus[11Johnson P.W. Hargraves P.E. Sieburth J.M. Ultrastructure and ecology of Calycomonas ovalis Wulff, 1919, (Chrysophyceae) and its redescription as a testate rhizopod, Paulinella ovalis n. comb. (Filosea: Euglyphina).J. Protozool. 1988; 35: 618-626Crossref Scopus (42) Google Scholar]. Molecular data brought to bear on the question of the origin of P. chromatophora have confirmed its unusual evolutionary history. Like the plastids of glaucophytes, the P. chromatophora endosymbiont possesses a cyanobacterial-like peptidoglycan wall, and it initially seemed possible that the endosymbionts of these two groups shared a common origin. However, phylogenetic analyses of the nucleus-encoded 18S ribosomal DNA (rDNA) gene revealed that the host component of P. chromatophora is not related to glaucophytes, but is instead allied with testate amoebae, chlorarachniophytes, and other members of the super-assemblage of eukaryotes collectively known as Cercozoa [14Bhattacharya D. Helmchen T. Melkonian M. Molecular evolutionary analyses of nuclear-encoded small subunit ribosomal RNA identify an independent rhizopod lineage containing the Euglyphidae and the Chlorarachniophyta.J. Eukaryot. Microbiol. 1995; 42: 64-68Google Scholar, 15Cavalier-Smith T. Chao E.E. Phylogeny and classification of phylum Cercozoa (Protozoa).Protist. 2003; 154: 341-358Crossref PubMed Scopus (228) Google Scholar]. More recently, Marin et al.[16Marin B. Nowack E.C.M. Melkonian M. A plastid in the making: evidence for a second primary endosymbiosis.Curr. Biol. 2005; 15: 425-432Abstract Full Text Full Text PDF Scopus (38) Google Scholar] sequenced the complete rDNA operon of the P. chromatophora endosymbiont and convincingly showed, as has long been suspected, a robust phylogenetic connection between it and modern-day cyanobacteria, more specifically with members of the Synechococcus/Prochlorococcus clade [16Marin B. Nowack E.C.M. Melkonian M. A plastid in the making: evidence for a second primary endosymbiosis.Curr. Biol. 2005; 15: 425-432Abstract Full Text Full Text PDF Scopus (38) Google Scholar]. While it is now clear that P. chromatophora acquired its photosynthetic apparatus independent of the endosymbiotic origin of all other plastids [16Marin B. Nowack E.C.M. Melkonian M. A plastid in the making: evidence for a second primary endosymbiosis.Curr. Biol. 2005; 15: 425-432Abstract Full Text Full Text PDF Scopus (38) Google Scholar, 17Rodriguez-Ezpeleta N. Philippe H. Plastid origin: replaying the tape.Curr. Biol. 2006; 16: R53-R56Abstract Full Text Full Text PDF PubMed Scopus (29) Google Scholar], an important question remains: to what extent can the P. chromatophora endosymbiont be considered a bona fide organelle? More specifically, what is the extent of the genetic integration between the host and endosymbiont components of P. chromatophora? One of the hallmarks of canonical plastid genomes is their diminutive size relative to those of free-living cyanobacteria. Sequenced cyanobacterial genomes range from ∼1.7 to >7 megabase-pairs (Mbp) in size and possess thousands of genes, whereas plastid genomes rarely have more than 200 genes (http://www.ncbi.nlm.nih.gov/genomes/lproks.cgi). During the early stages of the association between endosymbiont and host, many of the cyanobacterial genes no longer essential for intracellular life were presumably lost, and many more were transferred to the host's nuclear genome where they acquired the primary sequence information necessary to target their protein products back to the endosymbiont. The nuts-and-bolts of the targeting process are reasonably well understood in a wide range of plants and algae [18McFadden G.I. Plastids and protein targeting.J. Eukaryot. Microbiol. 1999; 46: 339-346Crossref PubMed Scopus (107) Google Scholar, 19Soll J. Schleiff E. Protein import into chloroplasts.Nat. Rev. Mol. Cell. Biol. 2004; 5: 198-208Crossref PubMed Scopus (322) Google Scholar]. Concomitant with the evolution of the protein import system itself, the initial surrender of essential genes to the host nucleus is thought to represent the 'click of the ratchet' beyond which the autonomy of the endosymbiont is lost. Unfortunately, the evolutionary gulf between modern-day plastids and cyanobacteria is so vast that most of the evolutionary information about the early stages of primary endosymbiosis has been erased. Where does the P. chromatophora endosymbiont lie on the continuum between food particle and plastid, and what can it tell us about this evolutionary transition? To address this issue, Yoon et al.[2Yoon H.S. Reyes-Prieto A. Bhattacharya D. Minimal plastid genome evolution in the Paulinella endosymbiont.Curr. Biol. 2006; 16: R670-R672Abstract Full Text Full Text PDF PubMed Scopus (78) Google Scholar] isolated and sequenced two fragments of the P. chromatophora endosymbiont genome (9.4 and 4.3 kilobase pairs in size) and compared them to homologous regions of available cyanobacterial genomes. Their results indicate that the endosymbiont is essentially cyanobacterial in nature: the highest degree of gene order conservation is shared with Synechococcus sp. WH5701, and several of the genes identified in the P. chromatophora cyanelle genome, for example psbO, are always (or most often) located in the nuclear genomes of photosynthetic eukaryotes — they are the result of plastid-to-nucleus gene transfers. The gene order data are consistent with rDNA [2Yoon H.S. Reyes-Prieto A. Bhattacharya D. Minimal plastid genome evolution in the Paulinella endosymbiont.Curr. Biol. 2006; 16: R670-R672Abstract Full Text Full Text PDF PubMed Scopus (78) Google Scholar, 16Marin B. Nowack E.C.M. Melkonian M. A plastid in the making: evidence for a second primary endosymbiosis.Curr. Biol. 2005; 15: 425-432Abstract Full Text Full Text PDF Scopus (38) Google Scholar] and protein phylogenies [2Yoon H.S. Reyes-Prieto A. Bhattacharya D. Minimal plastid genome evolution in the Paulinella endosymbiont.Curr. Biol. 2006; 16: R670-R672Abstract Full Text Full Text PDF PubMed Scopus (78) Google Scholar] in showing a specific association between the P. chromatophora endosymbiont and members of the Synechococcus/Prochlorococcus clade. While the actual size of the genome cannot be inferred from the data in hand, Yoon et al. speculate that it could well be similar in size to that of free-living Synechococcus/Prochlorococcus-type cyanobacteria, to which it appears most closely allied. The stage is now set to explore the molecular and cell biology of P. chromatophora in much more detail. Although its photosynthetic organelle is demonstrably cyanobacterial, the degree of biochemical and cellular integration between the P. chromatophora endosymbiont and host [10Hoogenraad H.R. Zur Kenntnis der Fortpflanzung von Paulinella chromatophora Lauterb.Zool. Anz. 1927; 72: 140-150Google Scholar, 11Johnson P.W. Hargraves P.E. Sieburth J.M. Ultrastructure and ecology of Calycomonas ovalis Wulff, 1919, (Chrysophyceae) and its redescription as a testate rhizopod, Paulinella ovalis n. comb. (Filosea: Euglyphina).J. Protozool. 1988; 35: 618-626Crossref Scopus (42) Google Scholar, 12Kies L. Elektronenmikroskopische Untersuchungen an Paulinella chromatophora Lauterborn, einer Thekamöbe mit blaugrünen Endosymbionten (Cyanellen).Protoplasma. 1974; 80: 69-89Crossref PubMed Scopus (78) Google Scholar, 13Kies L. Kremer B.P. Function of cyanelles in the Tecamoeba Paulinella chromatophora.Naturewissenschaften. 1979; 66: 578-579Crossref Scopus (36) Google Scholar] leads Yoon et al.[2Yoon H.S. Reyes-Prieto A. Bhattacharya D. Minimal plastid genome evolution in the Paulinella endosymbiont.Curr. Biol. 2006; 16: R670-R672Abstract Full Text Full Text PDF PubMed Scopus (78) Google Scholar] to speculate that at least some endosymbiont-to-host-nucleus gene transfers have occurred, such as those involved in organelle division (for example ftsZ) and metabolite transport. In this sense, the sequence of the P. chromatophora nuclear genome should be as informative as that of its endosymbiont. Exploration of nucleus-encoded proteins involved in organelle protein import will be particularly interesting. In plant and algal plastids, the import apparatus comprises more than a dozen proteins [19Soll J. Schleiff E. Protein import into chloroplasts.Nat. Rev. Mol. Cell. Biol. 2004; 5: 198-208Crossref PubMed Scopus (322) Google Scholar], some of which are cyanobacterial and others that appear to be eukaryote-specific proteins 'invented' in the common ancestor of red and green algae (data are currently unavailable for glaucophytes) [20McFadden G.I. van Dooren G.G. Evolution: red algal genome affirms a common origin of all plastids.Curr. Biol. 2004; 14: R514-R516Abstract Full Text Full Text PDF PubMed Scopus (186) Google Scholar]. When it comes to predicting the composition and complexity of the protein import apparatus in P. chromatophora, all bets are off. The immediate goal will be to glean as much information about the early stages of primary endosymbiosis as possible by comparing and contrasting P. chromatophora genomic sequences with those of all available algae and cyanobacteria. Such analyses will provide a rare opportunity to assess the relative contributions of chance and necessity in the evolution of life.