Abstract
We report the complete mitochondrial sequences of three brown algae (Dictyota dichotoma, Fucus vesiculosus and Desmarestia viridis) belonging to three phaeophycean lineages. They have circular mapping organization and contain almost the same set of mitochondrial genes, despite their size differences (31,617, 36,392 and 39,049 bp, respectively). These include the genes for three rRNAs (23S, 16S and 5S), 25–26 tRNAs, 35 known mitochondrial proteins and 3–4 ORFs. This gene set complements two previously studied brown algal mtDNAs, Pylaiella littoralis and Laminaria digitata. Exceptions to the very similar overall organization include the displacement of orfs, tRNA genes and four protein-coding genes found at different locations in the D. dichotoma mitochondrial genome. We present a phylogenetic analysis based on ten concatenated genes (7,479 nucleotides) and 29 taxa. Stramenopiles were always monophyletic with heterotrophic species at the base. Results support both multiple primary and multiple secondary acquisitions of plastids.
Similar content being viewed by others
Abbreviations
- Mt:
-
Mitochondrial
References
Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, PutnamNH, Zhou, Allen AE, Apt KE, Bechner M, Brzezinski MA, Chaal BK, Chiovitti A, Davis AK, Demarest MS, Detter JC, Glavina T, Goodstein D, Hadi MZ, U. Hellsten M. Hildebrand, Jenkins BD, Jurka J, Kapitonov VV, Kroger N, Lau WW, Lane TW, Larimer FW, Lippmeier JC, Lucas S, Medina M, Montsant A, Obornik M, Parker MS, Palenik B, Pazour GJ, Richardson PM, Rynearson TA, Saito MA, Schwartz DC, Thamatrakoln K, Valentin K, Vardi A, Wilkerson FP, Rokhsar DS (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79–86
Blackwell WH, Powell MJ (2000) A review of group filiation of Stramenopiles, additional approaches to the question. Evol Theor 12:49–88
Boore JL, Brown WM (1998) Big trees from little genomes: mitochondrial gene order as a phylogenetic tool. Curr Opin Genet Dev 8:668–674
Burger G, Citterich MH, Nelson MA, Werner S, Macino G (1985) RNA processing in Neurospora crassa mitochondria: transfer RNAs punctuate a large precursor transcript. EMBO J 4:197–204
Burger G, Forget L, Zhu Y, Gray MW, Lang BF (2003) Unique mitochondrial genome architecture in unicellular relatives of animals. Proc Natl Acad Sci USA 100:892–897
Burger G, Plante I, Lonergan KM, Gray MW (1995) The mitochondrial DNA of the amoeboid protozoon, Acanthamoeba castellanii: complete sequence, gene content and genome organization. J Mol Biol 245:522–537
Cavalier-Smith T (1998) A revised six-kingdom system of life. Biol Rev 73:203–266
Clayton DA (1984) Transcription of the mammalian mitochondrial genome. Ann Rev Biochem 53:573–594
Costa M, Fontaine J-M, Loiseaux-de Goër S, Michel F (1997) A group II self-splicing intron from the brown alga Pylaiella littoralis is active at unusually low magnesium concentrations and forms populations of molecules with a uniform conformation. J Mol Biol 274:353–364
Daugbjerg N, Andersen RA (1997) A molecular phylogeny of the heterokont algae based on analyses of chloroplast-encoded rbcL sequence data. J Phycol 33:1031–1041
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 (1997) The origin of plastids and their spread via secondary symbiosis. In: Bhattacharya D (ed) Origins of algae and their plastids. Springer Verlag, pp 53–86
Draisma SGA, Prud’ homme van Reine WF, Stam WT, Olsen JL (2001) A reassessment of phylogenetic relationships within the Phaeophyceae based on rubisco large subunit and ribosomal DNA sequences. J Phycol 37:586–603
Elzanowski AA, Ostell J (2000) The genetic codes. NCBI web site. http://www.ncbi.nlm.nih.gov/Taxonomy/Utils/wprintgc.cgi
Fast NM, Keeling PJ (2001) Alpha and beta subunits of pyruvate dehydrogenase E1 from the microsporidian Nosema locustae: mitochondrion-derived carbon metabolism in microsporidia. Mol Biochem Parasit 117:201–209
Goertzen LR, Theriot EC (2003) Effect of taxon sampling, character weighting, and combined data on the interpretation of relationships among the heterokont algae. J Phycol 39:423–439
Guillou L, Chrétiennot-Dinet M-J, Medlin LK, Claustre H, Loiseaux-de Goër 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
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acid Symp Ser 41:95–98
Leipe DD, Tong SM, Goggin CL, Slemenda SB, Pieniazek NJ, sogin ML (1996) 16S-like rDNA sequences from Developayella elegans, Labyrinthuloides haliotidis, and Proteromonas lacertae confirm that the stramenopiles are a primarily heterotrophic group. Eur J Protistol 32:449–458
Leipe DD, Wainright PO, Gunderson JH, Porter D, Patterson DJ, Vlois F, Himmerich S, Sogin ML (1994) The stramenopiles from a molecular perspective: 16S-like rRNA sequences from Labyrinthuloides minuta and Cafeteria roenbergensis. Phycologia 33:369–377
Mabuchi K, Miya M, Satoh TP, Westneat MW, Nishida M (2004) Gene rearrangements and evolution of tRNA pseudogenes in the mitochondrial genome of the parrotfish (Teleostei: Perciformes: Scaridae). J Mol Evol 59:287–297
Martin WF, Müller M (1998) The hydrogen hypothesis for the first eukaryote. Nature 392:37–41
Massana R, Guillou L, Diez B, Pedros-Alio C (2002) Unveiling the organisms behind novel eukaryotic ribosomal DNA sequences from the ocean. Appl Environ Microbiol 68:4554–4558
Medlin LK, Kooistra WHCF, Potter D, Saunders GW, Andersen RA (1997) Phylogenetic relationships of the “golden algae” (haptophytes, heterokont chromophytes) and their plastids. Pl Syst Evol Suppl 11:187–219
Oudot-Le Secq M-P, Fontaine J-M, Rousvoal S, Kloareg B, Loiseaux-de Goër S (2001) The complete sequence of a brown algal mitochondrial genome, the Ectocarpale Pylaiella littoralis (L.) Kjellm. J Mol Evol 53:80–88
Oudot-Le Secq M-P, Kloareg B, Loiseaux-de Goër S (2002) The mitochondrial genome of the brown alga Laminaria digitata: a comparative analysis. Eur J Phycol 37:163–172
Patterson DJ (1999) The Diversity of Eukaryotes. Am Nat 154:S96–S124
Pearson G, Serrão EA, Cancela ML (2001) Suppression subtractive hybridization for studying gene expression during aerial exposure and desiccation in fucoid algae. Eur J Phycol 36:359–366
Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818
Potter D, Saunders GW, Andersen RA (1997) Phylogenetic relationships of the Raphidophyceae and Xanthophyceae as inferred from nucleotide sequences of the 18S ribosomal RNA gene. Am J Bot 84:966–972
Rokas A, Holland PW (2000) Rare genomic changes as a tool for phylogenetics. Trends Ecol Evol 15:454–459
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Rousseau F, Burrowes R, Peters AF, Kuhlenkamp R, de Reviers B (2001) A comprehensive phylogeny of the Phaeophyceae based on nrDNA sequences resolves the earliest divergences. CR Acad Sci III-Vie 324:305–319
Rousseau F, de Reviers B (1999) Phylogenetic relationships within the Fucales (Phaeophyceae) based on combined partial SSU + LSU rDNA sequence data. Eur J Phycol 34:53–64
Rousvoal S, Oudot M-P, Fontaine J-M, Kloareg B, Loiseaux-de Goër S (1998) Witnessing the evolution of transcription in mitochondria: the mitochondrial genome of the primitive brown alga Pylaiella littoralis (L.) Kjellm. encodes a T7-like RNA polymerase. J Mol Biol 277:1047–1057
Sanchez Puerta MV, Bachvaroff TR, Delwiche CF (2004) The complete mitochondrial genome sequence of the haptophyte Emiliania huxleyi and its relation to heterokonts. DNA Res 11:1–10
Sankoff D, Bryant D, Deneault M, Lang BF, Burger G (2000) Early eukaryote evolution based on mitochondrial gene order breakpoints. J Comput Biol 7:521–535
Saunders GW, Potter D, Paskind MP, Andersen RA (1995) Cladistic analyses of combined traditional and molecular data sets reveal an algal lineage. Proc Natl Acad Sci USA 92:244–248
Schneider A, Maréchal-Drouard L (2000) Mitochondrial tRNA import: are there distinct mechanisms? Trends Cell Biol 10:509–513
Swofford DL (2003) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts
Sorhannus U (2001) A “total evidence” analysis of the phylogenetic relationships among the photosynthetic stramenopiles. Cladistics 17:227–241
Sprinzl M, Horn C, Brown M, Ioudovitch A, Steinberg S (1998) Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res 26:148–153
Van de Peer Y, Baldauf SL, Doolittle WF, Meyer A (2000) An updated and comprehensive rRNA phylogeny of (crown) eukaryotes based on rate-calibrated evolutionary distances. J Mol Evol 51:565–576
Van de Peer Y, Van der Auwera G, De Wachter R (1996) The evolution of stramenopiles and alveolates as derived by “substitution rate calibration” of small ribosomal subunit RNA. J Mol Evol 42:201–210
Vellai T, Takacs K, Vida G (1998) A new aspect to the origin and evolution of eukaryotes. J Mol Evol 46:499–507
Wuyts J, Van de Peer Y, Winkelmans T, De Wachter R (2002) The European database on small subunit ribosomal RNA. Nucleic Acids Res 30:183–185
Yoon HS, Hackett JD, Ciniglia C, Pinto G, Bhattacharya D (2004) A molecular timeline for the origin of photosynthetic eukaryotes. Mol Biol Evol 21:809–818
Zagryadskaya EI, Kotlova N, Steinberg S (2004) Key elements in maintenance of the tRNA L-shape. J Mol Biol 340:435–444
Acknowledgements
We thank S.A. Boele-Bos and J. Veldsink, for technical assistance, as well as G. Hoarau and M. Chevolot for helpful discussions. We also would like to thank two anonymous reviewers for useful comments to improve the manuscript. M.-P. O.-L.S. was supported by a Marie Curie Individual Fellowship (programme “Quality of Life and Management of Living Resources” QLK3-CT-2000-52053).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Ralph Bock
Nucleotide sequence data reported are available in the GenBank databases under the accession numbers AY494079, AY500368 and AY500367.
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Secq, MP.OL., Goër, S.Ld., Stam, W.T. et al. Complete mitochondrial genomes of the three brown algae (Heterokonta: Phaeophyceae) Dictyota dichotoma, Fucus vesiculosus and Desmarestia viridis . Curr Genet 49, 47–58 (2006). https://doi.org/10.1007/s00294-005-0031-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00294-005-0031-4