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Dinoflagellate Genome Evolution MI65CH19-Hackett ARI 27 July 2011 8:43 Dinoflagellate Genome Evolution Jennifer H. Wisecaver and Jeremiah D. Hackett Ecology and Evolutionary Biology Department, University of Arizona, Tucson, Arizona 85721; email: [email protected] Annu. Rev. Microbiol. 2011. 65:369–87 Keywords First published online as a Review in Advance on endosymbiosis, trans-splicing, gene transfer, alveolate, gene expression June 14, 2011 The Annual Review of Microbiology is online at Abstract micro.annualreviews.org The dinoflagellates are an ecologically important group of microbial eu- by University of Arizona Library on 11/07/11. For personal use only. This article’s doi: karyotes that have evolved many novel genomic characteristics. They 10.1146/annurev-micro-090110-102841 possess some of the largest nuclear genomes among eukaryotes arranged Copyright c 2011 by Annual Reviews. Annu. Rev. Microbiol. 2011.65:369-387. Downloaded from www.annualreviews.org ⃝ on permanently condensed liquid-crystalline chromosomes. Recent ad- All rights reserved vances have revealed the presence of genes arranged in tandem arrays, 0066-4227/11/1013-0369$20.00 trans-splicing of messenger RNAs, and a reduced role for transcrip- tional regulation compared to other eukaryotes. In contrast, the mito- chondrial and plastid genomes have the smallest gene content among functional eukaryotic organelles. Dinoflagellate biology and genome evolution have been dramatically influenced by lateral transfer of in- dividual genes and large-scale transfer of genes through endosymbio- sis. Next-generation sequencing technologies have only recently made genome-scale analyses of these organisms possible, and these new meth- ods are helping researchers better understand the biology and evolution of this enigmatic group of eukaryotes. 369 MI65CH19-Hackett ARI 27 July 2011 8:43 a complete genome sequence. Next-generation Contents sequencing technologies have finally placed a complete genome sequence of a dinoflagellate INTRODUCTION.................. 370 within reach and are already helping to eluci- DINOFLAGELLATE date the biology and evolution of these enig- PHYLOGENETICS . 370 matic organisms. NUCLEARBIOLOGY............... 372 Nuclear Genome Organization and Evolution . 372 DINOFLAGELLATE ORGANELLAR GENOMES. 376 PHYLOGENETICS The Mitochondrial Genome. 376 Dinoflagellates, apicomplexans, and ciliates are Dinoflagellate Plastids the dominant phyla of the well-supported su- and Their Genomes. 377 perphylum Alveolata, named for the flattened EVOLUTION OF vesicles (cortical alveoli) that form a contin- DINOFLAGELLATE GENE uous layer just under the plasma membrane CONTENT...................... 378 (21). The ciliates are predominantly unicellu- Endosymbiotic Gene Transfer in the lar heterotrophs that exhibit nuclear dimor- Evolution of Dinoflagellate phism and show deviations from the universal Genomes . 379 genetic code (87, 90, 113). Apicomplexans are Lateral Gene Transfer mostly intracellular parasites (54) and contain from Bacteria . 380 a nonphotosynthetic plastid (the apicoplast) in- CONCLUDING REMARKS . 380 volved in production of fatty acids, isoprene, heme, and iron-sulfur clusters (119). Phyloge- netic analyses are inconclusive but suggest alve- INTRODUCTION olates are related to stramenopiles (e.g., diatoms Dinoflagellates are ecologically and economi- and kelp) and rhizarians (e.g., forams and ra- cally important organisms in aquatic environ- diolarians) (18, 19). Within the alveolates, di- ments. They display tremendous morphologi- noflagellates are sister to the apicomplexans cal diversity and have one of the most extensive (29). Alveolate species that do not fall within fossil records among microbial eukaryotes due these three phyla are important for inferring to the formation of robust cysts by a large num- ancestral conditions. For example, the oyster ber of species (33). In marine environments they pathogen Perkinsus marinus is sister to dinoflag- are important primary producers, both as free- ellates and retains many typical eukaryotic char- by University of Arizona Library on 11/07/11. For personal use only. living phytoplankton and as symbionts of reef- acteristics (91), whereas the free-living marine forming corals. Many species are heterotrophic phototroph Chromera velia is sister to the para- Annu. Rev. Microbiol. 2011.65:369-387. Downloaded from www.annualreviews.org ormixotrophicandareprolificgrazersofplank- sitic apicomplexans (70). Molecular clock analy- tonic organisms. Dinoflagellates also produce ses indicate the dinoflagellates and apicomplex- a wide variety of secondary metabolites in- ans diverged 800–900 million years ago (11, 37), cluding a diverse array of toxins that have a consistent with fossils attributed to dinoflagel- significant impact on marine ecosystems and lates appearing as early as the late Mesoprotero- fisheries. zoic (65). Whereas some aspects of eukaryotes’ (par- The dinoflagellates can be divided into three ticularly microbial lineages) genomes differ main groups based on molecular phylogenies: from canonical eukaryotic traits, the dinoflag- Oxyrrhinales, Syndiniales, and the core di- ellates are notable for the extreme nature and noflagellates comprising the majority of char- Plastid: organelles of sheer number of novel genome characteristics. acterized species (67) (Figure 1). A large un- eukaryotes involved in photosynthesis They are perhaps the most ancient and diverse culturable diversity of marine dinoflagellates, group of eukaryotes for which there is not yet termed Marine Alveolates Group I (MAGI), 370 Wisecaver Hackett · MI65CH19-Hackett ARI 27 July 2011 8:43 Important phylogenetic nodes Durinskia 1 Alveolates baltica 2 Dinofagellates 3 Syndiniales Galeidiniium 4 Core dinofagellates Kryptoperidinium Karenia 5 Gonyaulacoids D Peridinium brevis 6 Gymnodiniales-Peridiniales- Durinskia Prorocentrales (GPP complex) Peridiniopsis Karenia H Prorocentrum Plastid replacements in dinofagellates Karlodinium sp. Gymnodinium D Dinotom dinofagellates have diatom-derived plastids Prorocentrum Peridinium H Fucoxanthin dinofagellates have 6 Peridinium haptophyte-derived plastids Symbiodinium sp. G Lepidodinium, the green dinofagellate, Woloszynskia has a prasinophyte-derived plastid G Lepidodinium K Dinophysis species have temporary Akashiwo cryptophyte plastids (kleptoplasts) Symbiodinium Pfesteria sp. Protoceratium Ceratium Gonyaulax 5 Gambierdiscus Akashiwo sanguinea Dinokaryon Alexandrium peridinin Fragilidium 4 Crypthecodinium Blastodinium Ceratium longipes Heterocapsa Noctiluca Histone-like proteins K Dinophysis 2 Amphidinium Alexandrium catenella Amoebophrya 3 Trans-splicing Syndinium Oxyrrhis Form II RuBisCO Plastid polyurdylylation MAGI Dinophysis Perkinsus sp. Apicomplexa 1 Chromera Ciliates Oxyrrhis Stramenopiles marina by University of Arizona Library on 11/07/11. For personal use only. Rhizaria Figure 1 Annu. Rev. Microbiol. 2011.65:369-387. Downloaded from www.annualreviews.org A phylogenetic model of dinoflagellate evolutionary relationships based on molecular data. Branches uniting supported clades are indicated with numbers. Plastid replacements are indicated with letters. Arrows indicate the most likely branch for the origin of some distinctive characteristics of dinoflagellates. Micrographs were obtained from the micro∗scope Web site (http://starcentral.mbl.edu/ microscope/portal.php)andusedwithpermission.Imagecopyrights:Durinskia baltica (S. Murray, M. Hoppenrath, J. Larsen & D. Patterson); Karenia brevis, Prorocentrum sp., Ceratium longipes, Alexandrium catenella,andDinophysis sp. (R. Andersen & D. Patterson); Peridinium sp. (M. Bahr & D. Patterson); Symbiodinium sp. (D. Patterson & M. Farmer); Akashiwo sanguinea (H. Su Yoon); Oxyrrhis marina (R. Moore & M.V. Sanchez-Puerta). Abbreviation: MAGI, Marine Alveolates Group I. has been described by 18S rDNA environ- heterotrophic Oxyrrhinales contain just one mental surveys and appears to be composed of morphospecies, Oxyrrhis marina (61). These primarily parasitic species (60, 69, 105). Syn- heterotrophic taxa (MAGI, the Syndiniales, and diniales, such as Amoebophrya,arealsopredom- Oxyrrhis) occupy a basal position in the di- inantly parasitic species. The free-living and noflagellate tree (41, 95, 97, 124). However, www.annualreviews.org Dinoflagellate Genome Evolution 371 • MI65CH19-Hackett ARI 27 July 2011 8:43 phylogenetic analyses have not determined the Nuclear Genome Organization positions of these groups relative to each other, and Evolution leaving the deepest branches of the dinoflagel- Dinotoms: Most dinoflagellates have dinokaryotic nuclei, late tree unresolved. This is problematic when dinoflagllates with distinguished by permanently condensed chro- attempting to infer ancestral states of some of diatom endosymbionts mosomes that are attached to the nuclear enve- plastids, which are the more unusual dinoflagellate characteristics lope and lack nucleosomes (12). Amazingly, the minimally reduced and discussed below. chromosome structure appears to be the result retain the diatom Within the core dinoflagellates, the tra- nucleus and other of DNA liquid crystal formation in the nucleus ditional orders were based on morphologi- organelles (15, 32, 59) (Figure 2a). The nuclear DNA cal characters such as thecal plate tabulation Theca: armored is associated with basic nuclear proteins, or patterns or the absence of theca altogether plates composed of histone-like proteins (HLPs). These proteins (31). Molecular phylogenetics has shown that cellulose or other have a secondary structure similar to that
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