Plastid Genome-Based Phylogeny Pinpointed the Origin of the Green-Colored Plastid in the Dinoflagellate Lepidodinium chlorophorum

Unlike many other photosynthetic dinoflagellates, whose plastids contain a characteristic carotenoid peridinin, members of the genus Lepidodinium are the only known dinoflagellate species possessing green alga-derived plastids. However, the precise origin of Lepidodinium plastids has hitherto remained uncertain. In this study, we completely sequenced the plastid genome of Lepidodinium chlorophorum NIES-1868. Our phylogenetic analyses of 52 plastid-encoded proteins unite L. chlorophorum exclusively with a pedinophyte, Pedinomonas minor, indicating that the green-colored plastids in Lepidodinium spp. were derived from an endosymbiotic pedinophyte or a green alga closely related to pedinophytes. Our genome comparison incorporating the origin of the Lepidodinium plastids strongly suggests that the endosymbiont plastid genome acquired by the ancestral Lepidodinium species has lost genes encoding proteins involved in metabolism and biosynthesis, protein/metabolite transport, and plastid division during the endosymbiosis. We further discuss the commonalities and idiosyncrasies in genome evolution between the L. chlorophorum plastid and other plastids acquired through endosymbiosis of eukaryotic photoautotrophs.

[1]  C. Lemieux,et al.  Six newly sequenced chloroplast genomes from prasinophyte green algae provide insights into the relationships among prasinophyte lineages and the diversity of streamlined genome architecture in picoplanktonic species , 2014, BMC Genomics.

[2]  C. Howe,et al.  Genome-Wide Transcript Profiling Reveals the Coevolution of Plastid Gene Sequences and Transcript Processing Pathways in the Fucoxanthin Dinoflagellate Karlodinium veneficum , 2014, Molecular biology and evolution.

[3]  Matthew W. Brown,et al.  Nucleomorph and plastid genome sequences of the chlorarachniophyte Lotharella oceanica: convergent reductive evolution and frequent recombination in nucleomorph-bearing algae , 2014, BMC Genomics.

[4]  R. Waller,et al.  A tertiary plastid gains RNA editing in its new host. , 2013, Molecular biology and evolution.

[5]  C. Howe,et al.  Functional remodeling of RNA processing in replacement chloroplasts by pathways retained from their predecessors , 2012, Proceedings of the National Academy of Sciences.

[6]  Y. Inagaki,et al.  Prasinoxanthin is absent in the green-colored dinoflagellate Lepidodinium chlorophorum strain NIES-1868: pigment composition and 18S rRNA phylogeny , 2012, Journal of Plant Research.

[7]  V. Hampl,et al.  The Plastid Genome of Eutreptiella Provides a Window into the Process of Secondary Endosymbiosis of Plastid in Euglenids , 2012, PloS one.

[8]  C. Delwiche,et al.  Phylogeny and Molecular Evolution of the Green Algae , 2012 .

[9]  J. V. Van Etten,et al.  The GC-Rich Mitochondrial and Plastid Genomes of the Green Alga Coccomyxa Give Insight into the Evolution of Organelle DNA Nucleotide Landscape , 2011, PLoS ONE.

[10]  Sohta A. Ishikawa,et al.  A deviant genetic code in the green alga-derived plastid in the dinoflagellate Lepidodinium chlorophorum. , 2011, Molecular phylogenetics and evolution.

[11]  A. Nederbragt,et al.  Genome Evolution of a Tertiary Dinoflagellate Plastid , 2011, PloS one.

[12]  Y. Inagaki,et al.  Green-colored plastids in the dinoflagellate genus Lepidodinium are of core chlorophyte origin. , 2011, Protist.

[13]  W. Pirovano,et al.  Scaffolding pre-assembled contigs using SSPACE , 2011, Bioinform..

[14]  Y. Inagaki,et al.  A phylogenetic mosaic plastid proteome and unusual plastid-targeting signals in the green-colored dinoflagellate Lepidodinium chlorophorum , 2010, BMC Evolutionary Biology.

[15]  A. Horák,et al.  A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids , 2010, Proceedings of the National Academy of Sciences.

[16]  P. Keeling,et al.  The Complete Plastid Genomes of the Two ‘Dinotoms’ Durinskia baltica and Kryptoperidinium foliaceum , 2010, PloS one.

[17]  P. Keeling.  The endosymbiotic origin, diversification and fate of plastids , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[18]  C. Lemieux,et al.  The chloroplast genomes of the green algae Pedinomonas minor, Parachlorella kessleri, and Oocystis solitaria reveal a shared ancestry between the Pedinomonadales and Chlorellales. , 2009, Molecular biology and evolution.

[19]  Nicolas Lartillot,et al.  PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating , 2009, Bioinform..

[20]  M. Kawachi,et al.  Mitochondrial group II introns in the raphidophycean flagellate Chattonella spp. suggest a diatom-to-Chattonella lateral group II intron transfer. , 2009, Protist.

[21]  C. O'kelly,et al.  The chloroplast genomes of the green algae Pyramimonas, Monomastix, and Pycnococcus shed new light on the evolutionary history of prasinophytes and the origin of the secondary chloroplasts of euglenids. , 2009, Molecular biology and evolution.

[22]  J. Archibald.  The Puzzle of Plastid Evolution , 2009, Current Biology.

[23]  O. Gascuel,et al.  An improved general amino acid replacement matrix. , 2008, Molecular biology and evolution.

[24]  T. Lybrand,et al.  Chloroplast genome sequencing analysis of Heterosigma akashiwo CCMP452 (West Atlantic) and NIES293 (West Pacific) strains , 2008, BMC Genomics.

[25]  Yuji Inagaki,et al.  Origins of plastids and glyceraldehyde-3-phosphate dehydrogenase genes in the green-colored dinoflagellate Lepidodinium chlorophorum. , 2008, Gene.

[26]  O. Hoegh‐Guldberg,et al.  A photosynthetic alveolate closely related to apicomplexan parasites , 2008, Nature.

[27]  S. Bowman,et al.  Plastid genome sequence of the cryptophyte alga Rhodomonas salina CCMP1319: lateral transfer of putative DNA replication machinery and a test of chromist plastid phylogeny. , 2007, Molecular biology and evolution.

[28]  C. Lemieux,et al.  The chloroplast genome sequence of the green alga Leptosira terrestris: multiple losses of the inverted repeat and extensive genome rearrangements within the Trebouxiophyceae , 2007, BMC Genomics.

[29]  Naiara Rodríguez-Ezpeleta,et al.  Detecting and overcoming systematic errors in genome-scale phylogenies. , 2007, Systematic biology.

[30]  H. Philippe,et al.  Suppression of long-branch attraction artefacts in the animal phylogeny using a site-heterogeneous model , 2007, BMC Evolutionary Biology.

[31]  J. Grimwood,et al.  Chloroplast genomes of the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana: comparison with other plastid genomes of the red lineage , 2007, Molecular Genetics and Genomics.

[32]  Alexandros Stamatakis,et al.  RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models , 2006, Bioinform..

[33]  K. Furuya,et al.  Photoautotrophic growth of Noctiluca scintillans with the endosymbiont Pedinomonas noctilucae , 2006 .

[34]  T. Cavalier-smith,et al.  Combined Heat Shock Protein 90 and Ribosomal RNA Sequence Phylogeny Supports Multiple Replacements of Dinoflagellate Plastids , 2006, The Journal of eukaryotic microbiology.

[35]  Naiara Rodríguez-Ezpeleta,et al.  Monophyly of Primary Photosynthetic Eukaryotes: Green Plants, Red Algae, and Glaucophytes , 2005, Current Biology.

[36]  A. Lambowitz,et al.  Mobile group II introns. , 2004, Annual review of genetics.

[37]  P. Keeling,et al.  Diversity and evolutionary history of plastids and their hosts. , 2004, American journal of botany.

[38]  R. Azanza,et al.  Green Noctiluca scintillans: a dinoflagellate with its own greenhouse , 2004 .

[39]  T. Cavalier-smith,et al.  Dinoflagellate Nuclear SSU rRNA Phylogeny Suggests Multiple Plastid Losses and Replacements , 2001, Journal of Molecular Evolution.

[40]  C. Delwiche,et al.  Phylogenetic analyses indicate that the 19'Hexanoyloxy-fucoxanthin-containing dinoflagellates have tertiary plastids of haptophyte origin. , 2000, Molecular biology and evolution.

[41]  E. Schnepf,et al.  Dinophyte chloroplasts and phylogeny - A review , 1999 .

[42]  S. Douglas,et al.  Plastid evolution: origins, diversity, trends. , 1998, Current opinion in genetics & development.

[43]  S. Eddy,et al.  tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. , 1997, Nucleic acids research.

[44]  M. Chihara,et al.  LEPIDODINIUM VIRIDE GEN. ET SP. NOV. (GYMNODINAIALES, DINOPHYTA), A GREEN DINOFLAGELLATE WITH A CHLOROPHYLL A‐ AND B‐CONTAINING ENDOSYMBIONT 1, 2 , 1990 .

[45]  S. W. Jeffrey,et al.  CHLOROPLAST PIGMENT PATTERNS IN DINOFLAGELLATES 1 , 1975 .

[46]  B. Sweeney.  LABORATORY STUDIES OF A GREEN NOCTILUCA FROM NEW GUINEA 1 , 2 , 1971 .

[47]  F. Raymond,et al.  which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Ray Meta: scalable de novo metagenome assembly and profiling , 2012 .

[48]  F. Leliaert,et al.  Diversity and Evolution of Algae: Primary Endosymbiosis , 2012 .

[49]  J. Archibald.  The Evolution of Algae by Secondary and Tertiary Endosymbiosis , 2012 .

[50]  P. Keeling.  Chromalveolates and the Evolution of Plastids by Secondary Endosymbiosis 1 , 2009, The Journal of eukaryotic microbiology.

[51]  J. Archibald,et al.  Diversity and Evolution of Plastids and Their Genomes , 2008 .

[52]  G. McFadden,et al.  The complete chloroplast genome of the chlorarachniophyte Bigelowiella natans: evidence for independent origins of chlorarachniophyte and euglenid secondary endosymbionts. , 2007, Molecular biology and evolution.

[53]  C. Delwiche,et al.  The complete plastid genome sequence of the haptophyte Emiliania huxleyi: a comparison to other plastid genomes. , 2005, DNA research : an international journal for rapid publication of reports on genes and genomes.

[54]  F. Tailor.  The biology of Dinoflagellates , 1987 .