Abstract
We sequenced the complete plastid and mitochondrial genomes of the unicellular marine phytoplankton Triparma laevis, belonging to the order Parmales (Heterokonta). The cells of Parmales are surrounded by silicified cell walls, similar to Bacillariophyta (diatoms). T. laevis was recognized as a sister group of Bacillariophyta using a molecular phylogenetic analysis based on SSU rDNA and rbcL sequences. Bacillariophyta are the most successful group of phytoplankton in the modern ocean, but the origin and early evolution of them have not been clearly established. Detailed molecular analyses of T. laevis may increase our understanding of the evolutionary relationships among Parmales and Bacillariophyta. The gene contents of the plastid and mitochondrial genomes are similar between T. laevis and Bacillariophyta. The gene order of the plastid genome is also similar to Bacillariophyta, whereas the gene order of the mitochondrial genome is not conserved in Bacillariophyta, but the structure is more compact than Bacillariophyta. Phylogenetic analyses, using plastid-encoded concatenated amino acid datasets and mitochondria-encoded concatenated amino acid datasets suggest that T. laevis is a sister group of Bacillariophyta. These results suggest that the characteristics of the organellar genomes of T. laevis are similar and conserve ancestral characteristics more than Bacillariophyta.
Similar content being viewed by others
References
Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104–2105
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Booth BC, Marchant HJ (1987) Parmales, a new order of marine chrysophytes, with descriptions of three new genera and seven new species. J Phycol 23:245–260
Booth BC, Lewin J, Norris RE (1980) Siliceous nanoplankton. 1. Newly discovered cysts from the Gulf of Alaska. Mar Biol 58:205–209
Cavalier-Smith T (1998) A revised six-kingdom system of life. Biol Rev Camb Philos Soc 73:203–266
Daugbjerg N, Guillou L (2001) Phylogenetic analyses of Bolidophyceae (Heterokontophyta) using rbcL gene sequences support their sister group relationship to diatoms. Phycologia 40:153–161
Delwiche CF, Palmer JD (1996) Rampant horizontal transfer and duplication of rubisco genes in eubacteria and plastids. Mol Biol Evol 13:873–882
Drouin G, Daoud H, Xia J (2008) Relative rates of synonymous substitutions in the mitochondrial, chloroplast and nuclear genomes of seed plants. Mol Phylogenet Evol 49:827–831
Felsenstein J (1978) Cases in which parsimony or compatibility methods will be positively misleading. Syst Zool 27:401–410
Field CB, Behrenfeld MJ, Randerson JT, Falkowski P (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281:237–240
Fox TD (1979) Five TGA “stop” codons occur within the translated sequence of the yeast mitochondrial gene for cytochrome c oxidase subunit II. Proc Natl Acad Sci USA 76:6534–6538
Glöckner G, Rosenthal A, Valentin K (2000) The structure and gene repertoire of an ancient red algal plastid genome. J Mol Evol 51:382–390
Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms I. Cyclotella nana Hustedt and Detonula confervacea (cleve) Gran. Can J Microbiol 8:229–239
Guillou L, Chrétiennot-Dinet M-J, Medlin LK, Claustre H, Loiseaux-de Göer S, Vaulot D (1999) Bolidomonas: a new genus with two species belonging to a new algal class, the Bolidophyceae (Heterokonta). J Phycol 35:368–381
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321
Ichinomiya M, Kuwata A (2015) Seasonal variation in abundance and species composition of the Parmales community in the Oyashio region, western North Pacific. Aquat Microb Ecol 75:207–223
Ichinomiya M, Yoshikawa S, Kamiya M, Ohki K, Takaichi S, Kuwata A (2011) Isolation and characterization of Palmales (Heterokonta/Heterokontophyta/Stramenopiles) from the Oyashio region, western North Pacific. J Phycol 47:144–151
Kim E, Archibald JM (2009) Diversity and evolution of plastids and their genomes. The chloroplast—interactions with the environment. In: Aronsson H, Sandelius AS (eds) Plant cell monographs, vol 13. Springer, Berlin, pp 1–39
Komuro C, Narita H, Imai K, Nojiri Y, Jordan RW (2005) Microplankton assemblages at Station KNOT in the subarctic western Pacific, 1999–2000. Deep Sea Res Part II: Top Stud Oceanogr 52:2206–2217
Konno S, Jordan RW (2007) An amended terminology for the Parmales (Chrysophyceae). Phycologia 46:612–616
Kosman CA, Thomsen HA, Østergaard JB (1993) Parmales (Chrysophyceae) from Mexican, Californian, Baltic, Arctic and Antarctic waters with the description of a new subspecies and several new forms. Phycologia 32:116–128
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948
Le SQ, Gascuel O (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25:1307–1320
Lommer M, Roy AS, Schilhabel M, Schreiber S, Rosenstiel P, LaRoche J (2010) Recent transfer of an iron-regulated gene from the plastid to the nuclear genome in an oceanic diatom adapted to chronic iron limitation. BMC Genom 11:718
Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964
Mann DG (1999) The species concept in diatoms. Phycologia 38:437–495
Mann DG, Vanormelingen P (2013) An inordinate fondness? The number, distributions, and origins of diatom species. J Eukaryot Microbiol 60:414–420
Nelson DM, Tréguer P, Brzezinski MA, Leynaert A, Quéguiner B (1995) Production and dissolution of biogenic silica in the ocean: revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Global Biogeochem Cycles 9:359–372
Nishida S (1986) Nanoplankton flora in the Southern Ocean, with special reference to siliceous varieties. Mem Nat Inst Polar Res Spec Issue 40:56–68
Noguchi H, Taniguchi T, Itoh T (2008) MetaGeneAnnotator: detecting species-specific patterns of ribosomal binding site for precise gene prediction in anonymous prokaryotic and phage genomes. DNA Res 15:387–396
Oudot-Le Secq MP, Green BR (2011) Complex repeat structures and novel features in the mitochondrial genomes of the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana. Gene 476:20–26
Oudot-Le Secq MP, Loiseaux-de Goër S, Stam WT, Olsen JL (2006) Complete mitochondrial genomes of the three brown algae (Heterokonta: Phaeophyceae) Dictyota dichotoma, Fucus vesiculosus and Desmarestia viridis. Curr Genet 49:47–58
Oudot-Le Secq MP, Grimwood J, Shapiro H, Armbrust EV, Bowler C, Green BR (2007) Chloroplast genomes of the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana: comparison with other plastid genomes of the red lineage. Mol Genet Genomics 277:427–439
Prihoda J, Tanaka A, de Paula WB, Allen JF, Tirichine L, Bowler C (2012) Chloroplast-mitochondria cross-talk in diatoms. J Exp Bot 63:1543–1557
Qiu H, Yang EC, Bhattacharya D, Yoon HS (2012) Ancient gene paralogy may mislead inference of plastid phylogeny. Mol Biol Evol 29:3333–3343
Rice DW, Palmer JD (2006) An exceptional horizontal gene transfer in plastids: gene replacement by a distant bacterial paralog and evidence that haptophyte and cryptophyte plastids are sisters. BMC Biol 4:31
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Ruck EC, Nakov T, Jansen RK, Theriot EC, Alverson AJ (2014) Serial gene losses and foreign DNA underlie size and sequence variation in the plastid genomes of diatoms. Genome Biol Evol 6:644–654
Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B (2000) Artemis: sequence visualization and annotation. Bioinformatics 16:944–945
Sagan L (1967) On the origin of mitosing cells. J Theor Biol 14:255–274
Sasaki NV, Sato N (2010) CyanoClust: comparative genome resources of cyanobacteria and plastids. Database 2010:bap025
Sato N (2000) SISEQ: manipulation of multiple sequence and large database files for common platforms. Bioinformatics 16:180–181
Sato N (2009) Gclust: trans-kingdom classification of proteins using automatic individual threshold setting. Bioinformatics 25:599–605
Silver MW, Mitchell JG, Ringo DL (1980) Siliceous nanoplankton. II. Newly discovered cysts and abundant choanoflagellates from the Weddell Sea, Antarctica. Mar Biol 58:211–217
Smith DR, Hua J, Lee RW, Keeling PJ (2012) Relative rates of evolution among the three genetic compartments of the red alga Porphyra differ from those of green plants and do not correlate with genome architecture. Mol Phylogenet Evol 65:339–344
Smith DR, Arrigo KR, Alderkamp AC, Allen AE (2014) Massive difference in synonymous substitution rates among mitochondrial, plastid, and nuclear genes of Phaeocystis algae. Mol Phylogenet Evol 71:36–40
Starkenburg SR, Kwon KJ, Jha RK, McKay C, Jacobs M, Chertkov O, Twary S, Rocap G, Cattolico RA (2014) A pangenomic analysis of the Nannochloropsis organellar genomes reveals novel genetic variations in key metabolic genes. BMC Genom 15:212
Tajima N, Sato S, Maruyama F, Kurokawa K, Ohta H, Tabata S, Sekine K, Moriyama T, Sato N (2014) Analysis of the complete plastid genome of the unicellular red alga Porphyridium purpureum. J Plant Res 127:389–397
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Whelan S, Goldman N (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18:691–699
Williams KP, Sobral BW, Dickerman AW (2007) A robust species tree for the alphaproteobacteria. J Bacteriol 189:4578–4586
Yang EC, Boo GH, Kim HJ, Cho SM, Boo SM, Andersen RA, Yoon HS (2012) Supermatrix data highlight the phylogenetic relationships of photosynthetic stramenopiles. Protist 163:217–231
Acknowledgments
This work was supported in part by a Grant-in-Aid for the Global COE Program, “From the Earth to Earths” and Scientific Research (No. 26291085) from the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan and the Canon Foundation (A. K. and N. S.).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. Kupiec.
This work is part of a dissertation submitted to the University of Tokyo in partial fulfillment of the requirements for the PhD degree.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Tajima, N., Saitoh, K., Sato, S. et al. Sequencing and analysis of the complete organellar genomes of Parmales, a closely related group to Bacillariophyta (diatoms). Curr Genet 62, 887–896 (2016). https://doi.org/10.1007/s00294-016-0598-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00294-016-0598-y