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A Phylogenomic Falsification of the Chromalveolate Hypothesis

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A Phylogenomic Falsification of the Chromalveolate Hypothesis On the origin of chlorophyll c-containing algae A phylogenomic falsification of the Chromalveolate hypothesis Denis BAURAIN Université de Montréal / Université de Liège Cologne – April 20, 2010 Acknowledgments Do ‘Chromalveolates’ really? exist? Outline of the Talk Do ‘Chromalveolates’ really exist? 1. What are ‘Chromalveolates’? 2. How to test the Chromalveolate hypothesis? 3. How to check the assumptions of our test? 4. Can we specify an alternative hypothesis? What are ‘Chromalveolates’?1 ANRV329-GE41-08 ARI 27 September 2007 14:38 INTRODUCTION (e.g., cercomonads, foraminifera), and ‘Ex- cavata’ (e.g., diplomonads, parabasalids). Al- The Eukaryotic Tree of Life as though the supergroups broadly capture the Protist: microbial Backdrop for Plastid Origin eukaryote not diversity of eukaryotes, there are in fact including plants and Multigene phylogenetics and genome data only two that currently have robust sup- fungi from microbial eukaryote (protist) lineages port from molecular phylogenetic analyses, Algae: have provided a renewed impetus to resolv- the ‘Opisthokonta’ and the ‘Amoebozoa’ (71). photosynthetic ing the eukaryotic tree of life (e.g., 11, 71, Therefore in this review all supergroups are eukaryotes (protists) 90), culminating recently in a formal classi- marked with ‘ ’ to denote their provisional na- not including plants fication of eukaryotes into 6 “supergroups” ture. Of the remaining lineages, the ‘Plantae’ ‘Chromalveolata’: (3, 44). These supergroups (see Figure 1) is gaining the most support from multigene putative trees (83) and features associated with the monophyletic group contain the protistan roots of all multi- descended from a cellular eukaryotes and are currently de- photosynthetic organelle (plastid) in these protist common fined as ‘Opisthokonta’ (e.g., animals, fungi, taxa (e.g., 63, 78, 99). This group is very ancestor that choanoflagellates), ‘Amoebozoa’ (e.g., lobose likely to be monophyletic, a key feature that captured a red alga amoebae, slime molds), ‘Archaeplastida’ or plays an important role in understanding plas- and maintained it as tid evolution. The ‘Rhizaria’ includes pho- a secondary ‘Plantae’ [red, green (including land plants), endosymbiont and glaucophyte algae], ‘Chromalveolata’ tosynthetic amoebae (chlorarachniophytes (e.g., diatoms, ciliates, giant kelps), ‘Rhizaria’ and Paulinella chromatophora) and receives Chromalveolata Plantae Alveolates Red, Glaucophyte Stramenopiles Green algae Haptophytes Cryptophytes Figure 1 Schematic view of the eukaryotic tree of life showing the putative six supergroups. The broken lines Amoebozoa Rhizaria by UNIVERSITE DE LIEGE on 04/10/10. For personal use only. denote uncertainty Entamoebae Radiolaria of branch positions Amoebae Cercozoa in the tree. For Slime molds Annu. Rev. Genet. 2007.41:147-168. Downloaded from arjournals.annualreviews.org example, the ‘Rhizaria’ are likely monophyletic but may branch within chromalveolates and the ‘Excavata’ may comprise at Animals least two distinct Choanozoa Euglenids lineages. The Fungi Parabasalids presence of Microsporidia Diplomonads plastid-containing Jakobids taxa in the Opisthokonta supergroups is Excavata shown with the cartoon of an alga. 148 Reyes-Prieto‘Chromalveolates’Weber Bhattacharya are one of the six · · putative Eukaryotic supergroups. Reyes-Prieto et al. (2007) Annu Rev Genet 41:147-168 Review TRENDS in Genetics Vol.18 No.11 November 2002 581 and ultrastructural features suggest a relationship between some or all chlorophyll a+c-containing Heterokonts Stramenopiles organisms (Fig. 2). Of the four lineages with Haptophytes chlorophyll-a+c-pigmented plastids, heterokonts and haptophytes are most similar from an ultrastructural Fucoxanthin and derivatives One autoflourescent flagellum and biochemical perspective, sharing fucoxanthin and Chrysolaminaran fucoxanthin-like carotenoids, a single autofluorescent ʻChromistsʼflagellum, and chrysolaminaran stored in cytoplasmic Tub. mito. cristae Four plastid vacuoles, characteristics that once led to their Three thylakoids membranes classification together [39]. s /stack Plastid OM e fused with m Although these data are suggestive, this picture is e n ER o not without wrinkles. Most significantly, a common ig Chl c t s Chl a a origin of these plastids implies that both plastid and m Red algal plastid r host lineages should be demonstrably related, but la u ub early molecular data appeared to contradict such a Peridinin T Nucleomorph Plastid OM not fused Flat mito. cristae relationship. The sequences of haptophyte, heterokont with ER Phycobilins and cryptomonad plastid SSU rRNA and Rubisco have Three plastid membranes Two thylakoids/stack been examined extensively, and typically do not form a Starch single group in phylogenetic analyses [21,34,40]. From Alveolates Dinoflagellates CryptomonadsCryptophytes the host lineage, phylogenies of nuclear SSU rRNA have also failed to show such a relationship [41], and this has been interpreted as additional support TRENDS in Genetics for several independent endosymbioses involving red algae. Recently, however, an analysis of five ChlorophyllFig. 2. Venn diagram cof-containing the pigment composition and algae significant sharebiochemical and a cell-biological number ofcon catenated plastid genes showed strong support for featuresbiochemical of organisms that have andsecondary ultrastructural plastids of red-algal origin. Abbreviations: features. a monophyletic group consisting of haptophytes, Chl, chlorophyll; ER, endoplasmic reticulum; mito., mitochondrial; OM, outer membrane; heterokonts and cryptomonads (D. Bhattacharya, Tub., tubular. Note that (1) fucoxanthin carotenoids are quite diverse in haptophytes and heterokonts, (2) starch is stored in the cytosol of dinoflagellates, but in the periplastidadapted from space Archibald of cryptomonads. and Keeling (2002) pTiGer s18:577-584. commun.), tipping the scales decidedly in favor of a single origin for the plastids of these organisms. chlorarachniophyte plastids are the product of a At the same time as the relationships among single secondary endosymbiosis [9,27], there is cryptomonads, heterokonts and haptophytes were currently no evidence supporting this. The host cells being debated, another line of inquiry developed that lack significant structural similarity [16] and has altered our view of eukaryotic evolution phylogenies based on nuclear and plastid genes show considerably. It has long been known that apicomplexa no support for a specific relationship between and dinoflagellates are close relatives (together with euglenid and chlorarachniophyte hosts or plastids ciliates, making up the alveolates) [42]. Accordingly, [24,28–30], altogether suggesting that these lineages when a cryptic plastid was discovered in apicomplexa represent two independent endosymbiotic events [43,44], it immediately sparked a heated debate about involving different hosts and different green algae. whether apicomplexan and dinoflagellate plastids share a common origin, a debate heightened by Red endosymbionts uncertainty about whether the apicomplexan plastid In contrast to green endosymbionts, the situation was derived from a red or green alga [45–47]. Until with red endosymbionts remains quite complicated, very recently, however, no dinoflagellate plastid in part because of the greater diversity they represent. sequences were available to test this hypothesis. A range of data, especially molecular phylogenies Several dinoflagellate plastid genes have now been based on plastid and cryptomonad nucleomorph characterized and, unexpectedly, found to reside on genes, and conserved features of plastid genome small single-gene minicircles, unlike all other known organization, have now conclusively shown that the plastid DNAs [48]. Phylogenetic analyses of these plastids of heterokonts, haptophytes, cryptomonads, genes not only confirmed a red-algal origin for the dinoflagellates and apicomplexan parasites are all dinoflagellate plastid [48,49] but also suggested a derived from red algae [3,21,31–37]. Apicomplexan specific relationship between the plastids of plastids are non-photosynthetic and accordingly have dinoflagellates and apicomplexa [36]. These data are, no pigments, but all other red-algal secondary plastids however, plagued by the fact that both the contain a unique combination of chlorophylls a and c, dinoflagellate and apicomplexan plastid genes are whereas cryptomonads also contain phycobilins. extraordinarily divergent and AT rich. Such divergent, Among eukaryotes, chlorophyll c is unique to these biased sequences tend to cluster together in algae [although chlorophyll-c-like pigments have been phylogenetic trees regardless of their true found in a few other isolated cases (e.g. Ref. [38])], evolutionary history, making it impossible to rule out suggesting that all organisms with this chlorophyll a methodological artifact [36]. Nevertheless, the might be directly related. Indeed, several biochemical simplest interpretation is that apicomplexan and http://tig.trends.com ANRV329-GE41-08 ARI 21 June 2007 22:19 Karenia brevis a Cryptophytes b Emiliania huxleyi chl.c Isochrysis galbana Haptophytes ʻChromistsʼ Prymnesium parvum Thalassiosira pseudonana Stramenopiles Phaeodactylum tricornutum Heterocapsa triquetra Ancestral Alexandrium tamarense Chromalveolate Amphidinium carterae Galdieria sulphuraria Alveolates Cyanidioschyzon merolae Red algae Eudicot Arabidopsis thaliana Oryza sativa Green algae Euglenids Chlamydomonas reinhardtii The Chromalveolate hypothesis positsBigelowiella
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