Evolution of the diatoms: V. Morphological and cytological support for the major clades and a taxonomic revision

Abstract Phylogenetic reconstructions of the diatoms have been inferred with the 18S and 16S ribosomal RNA genes. Previous studies have shown that the group is divided into two major clades, with support coming initially from the arrangement of the Golgi bodies inside the cells in extant taxa. Features of extinct taxa that also support these clades can be found in the earliest fossil record of the diatoms and include the presence or absence of a central structure in the valve wall and the type of peripheral linking mechanisms between cells. Here we demonstrate that the general pattern of the auxospore expansion and the structure of their walls, the structure of the pyrenoid and the ultrastructure of the spermatozoid further support the molecular clades. Given the combined molecular and morphological support, we propose two new subdivisions (Coscinodiscophytina and Bacillariophytina), emend the classes Coscinodiscophyceae and Bacillariophyceae and propose a new class, the Mediophyceae for the bipolar centrics and the Thalassiosirales.

[1]  R. W. Drum.  Electron microscopy of paired Golgi structures in the diatom Pinnularia nobilis. , 1966, Journal of ultrastructure research.

[2]  I. Manton.  Observations on the fine structure of the male gamete of the marine centric diatom Lithodesmium undulatum , 1966 .

[3]  K. Kowallik,et al.  Observations on the fine structure and development of the spindle at mitosis and meiosis in a marine centric diatom (Lithodesmium undulatum) , 1969, Journal of microscopy.

[4]  K. Kowallik,et al.  Observations on the fine structure and development of the spindle at mitosis and meiosis in a marine centric diatom (Lithodesmium undulatum). II. The early meiotic stages in male gametogenesis. , 1969, Journal of cell science.

[5]  K. Kowallik,et al.  Observations on the fine structure and development of the spindle at mitosis and meiosis in a marine centric diatom (Lithodesmium undulatum). 3. The later stages of meiosis I in male gametogenesis. , 1970, Journal of cell science.

[6]  R. Crawford.  The auxospore wall of the marine diatom Melosira nummuloides (Dillw.) C. Ag. and related species , 1974 .

[7]  E. E. Cupp.  Marine Plankton Diatoms of the West Coast of North America , 1977 .

[8]  G. L. Floyd,et al.  Ultrastructure of the centric diatom, Cyclotella meneghiniana: vegetative cell and auxospore development* , 1979 .

[9]  M. Borowitzka,et al.  Morphogenesis and Biochemistry of Diatom Cell Walls , 1981 .

[10]  F. E. Round.  Some aspects of the origin of diatoms and their subsequent evolution. , 1981, Bio Systems.

[11]  R. Crawford.  The diatom genus Aulacoseira Thwaites: its structure and taxonomy , 1981 .

[12]  F. E. Round.  Auxospore Structure, Initial Valves and the Development of Populations of Stephanodiscus in Farmoor Reservoir , 1982 .

[13]  D. Mann.  STRUCTURE, LIFE HISTORY AND SYSTEMATICS OF RHOICOSPHENIA (BACILLARIOPHYTA). II. AUXOSPORE FORMATION AND PERIZONIUM STRUCTURE OF RH. CURVATA 1 , 1982 .

[14]  F. E. Round,et al.  The lines of evolution of the Bacillariophyta - II. The centric series , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[15]  D. Mann.  Auxospore formation and development in Neidium (Bacillariophyta) , 1984 .

[16]  J. Felsenstein.  CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP , 1985, Evolution; international journal of organic evolution.

[17]  Grethe Rytter Hasle.  The Fossil Diatom Thalassiosira oranica, n. sp. , 1985 .

[18]  J. Pickett-Heaps,et al.  CELLULAR MOVEMENT IN THE CENTRIC DIATOM ODONTELLA SINENIS 1 , 1986 .

[19]  R. Crawford,et al.  Histochemical and ultrastructural evidence for the function of the labiate process in the movement of centric diatoms , 1986 .

[20]  A. Schmid.  Morphogenetic Forces in Diatom Cell Wall Formation , 1987 .

[21]  D. Mann.  SEXUAL REPRODUCTION IN CYMATOPLEURA , 1987 .

[22]  David M. Williams,et al.  REVISION OF THE GENUS FRAGILARIA , 1987 .

[23]  D. Mann.  SEXUAL REPRODUCTION AND SYSTEMATICS OF NAVICULA PROTRACTA , 1988 .

[24]  K. Mullis,et al.  Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. , 1988, Science.

[25]  J. Pickett-Heaps,et al.  PERIZONIUM AND INITIAL VALVE FORMATION IN THE DIATOM NAVICULA CUSPIDATA (BACILLARIOPHYCEAE) 1 , 1989 .

[26]  D. Mann,et al.  Meiosis, nuclear cyclosis, and auxospore formation in Navicula sensu stricto (Bacillariophyta) , 1989 .

[27]  J. Doyle,et al.  Isolation of plant DNA from fresh tissue , 1990 .

[28]  P. Hargraves.  Studies on marine plankton diatoms. V, Morphology and distribution on Leptocylindrus minimus Gran , 1990 .

[29]  L. Medlin,et al.  MORPHOLOGICAL AND GENETIC VARIATION WITHIN THE DIATOM SKELETONEMA COSTATUM (BACILLARIOPHYTA): EVIDENCE FOR A NEW SPECIES, SKELETONEMA PSEUDOCOSTATUM 1 , 1991 .

[30]  T. Christensen,et al.  The Diatoms. Biology and Morphology of the Genera , 1991 .

[31]  J. Huelsenbeck,et al.  Signal, noise, and reliability in molecular phylogenetic analyses. , 1992, The Journal of heredity.

[32]  D. Bhattacharya,et al.  ALGAE CONTAINING CHLOROPHYLLS a + c ARE PARAPHYLETIC: MOLECULAR EVOLUTIONARY ANALYSIS OF THE CHROMOPHYTA , 1992, Evolution; international journal of organic evolution.

[33]  David M. Williams,et al.  The evolution of the diatoms (Bacillariophyta) I. Origin of the group and assessment of the monophyly of its major divisions , 1993 .

[34]  J. Bull,et al.  An Empirical Test of Bootstrapping as a Method for Assessing Confidence in Phylogenetic Analysis , 1993 .

[35]  J. Neefs.  Compilation of small subunit ribosomal RNA sequences , 1993 .

[36]  R. Andersen,et al.  ULTRASTRUCTURE AND 18S RRNA GENE SEQUENCE FOR PELAGOMONAS CALCEOLATA GEN. ET SP. NOV. AND THE DESCRIPTION OF A NEW ALGAL CLASS, THE PELAGOPHYCEAE CLASSIS NOV. 1 , 1993 .

[37]  P. Sims.  BENETORUS, GLADIOPSIS AND RELATED GENERA FROM THE CRETACEOUS , 1994 .

[38]  A. Schmid.  SLIT-SCALES IN THE AUXOSPORE SCALE CASE OF COSCINODISCUS GRANII: THE RUDIMENTS OF RIMOPORTULAE? , 1994 .

[39]  Anna-Maria M. Schmid.  Aspects of morphogenesis and function of diatom cell walls with implications for taxonomy , 1994 .

[40]  Detlef D. Leipe,et al.  The stramenopiles from a molecular perspective 16S-like rRNA sequences from Labyrinthuloides minuta and Cafeteria roenbergensis , 1994 .

[41]  M. Mizuno.  SEXUAL REPRODUCTION AND AUXOSPORE FORMATION IN ACHNANTHES JAVANICA F. SUBCONSTRICTA , 1994 .

[42]  D. Mann,et al.  Sexual reproduction and systematics of Placoneis (Bacillariophyta) , 1995 .

[43]  F. Gasse,et al.  A preliminary phylogeny of diatoms based on 28S ribosomal RNA sequence data , 1995 .

[44]  L. Medlin,et al.  Evolution of the diatoms (Bacillariophyta). II. Nuclear-encoded small-subunit rRNA sequence comparisons confirm a paraphyletic origin for the centric diatoms. , 1996, Molecular biology and evolution.

[45]  L. Medlin,et al.  Evolution of the diatoms (Bacillariophyta) III. Molecular evidence for the origin of the Thalassiosirales , 1996 .

[46]  S. Giovannoni,et al.  Phylogenetic diversity of marine coastal picoplankton 16S rRNA genes cloned from the continental shelf off Cape Hatteras, North Carolina , 1997 .

[47]  Masakazu Haga.  MORPHOLOGY OF VEGETATIVE AND RESTING SPORE VALVES OF STEPHANOPYXIS NIPPONICA , 1997 .

[48]  L. Medlin,et al.  Phylogenetic relationships of the 'golden algae' (haptophytes, heterokont chromophytes) and their plastids , 1997 .

[49]  G. Gerdts,et al.  Phylogenetic analysis of selected toxic and non-toxic bacterial strains isolated from the toxic dinoflagellate Alexandrium tamarense , 1997 .

[50]  D. Harwood,et al.  NEW PROCESS, GENUS AND FAMILY OF LOWER CRETACEOUS DIATOMS FROM AUSTRALIA , 1997 .

[51]  M. Mizuno.  SEXUAL REPRODUCTION AND AUXOSPORE FORMATION OF THE MARINE MONORAPHID DIATOM COCCONEIS PELLUCIDA , 1998 .

[52]  David Posada,et al.  MODELTEST: testing the model of DNA substitution , 1998, Bioinform..

[53]  N. Kröger,et al.  Diatom cell wall proteins and the cell biology of silica biomineralization. , 1998, Protist.

[54]  N. Kröger,et al.  Polycationic peptides from diatom biosilica that direct silica nanosphere formation. , 1999, Science.

[55]  David G. Mann,et al.  The species concept in diatoms , 1999 .

[56]  B. Hall,et al.  Long-branch attraction and the rDNA model of early eukaryotic evolution. , 1999, Molecular biology and evolution.

[57]  Carole C. Perry,et al.  Biosilicification: the role of the organic matrix in structure control , 2000, JBIC Journal of Biological Inorganic Chemistry.

[58]  L. Medlin,et al.  A review of the evolution of the diatoms - a total approach using molecules, morphology and geology , 2000 .

[59]  David M. Williams,et al.  Systematics of naviculoid diatoms: the interrelationships of some taxa with a stauros , 2000 .

[60]  I. Kaczmarska.  Fine structure of the gamete, auxospore and initial cell in the pennate diatom Pseudo-nitzschia multiseries (Bacillariophyta) , 2000 .

[61]  T. Ohama,et al.  Phylogenetic analysis of diatom coxI genes and implications of a fluctuating GC content on mitochondrial genetic code evolution , 2000, Current Genetics.

[62]  B. Edvardsen,et al.  Phylogenetic reconstructions of the Haptophyta inferred from 18S ribosomal DNA sequences and available morphological data , 2000 .

[63]  Oceans Canada,et al.  A review of auxospore structure, ontogeny and diatom phylogeny , 2001 .

[64]  D. Bhattacharya,et al.  Ribosomal DNA phylogeny of the Bangiophycidae (Rhodophyta) and the origin of secondary plastids. , 2001, American journal of botany.

[65]  Jonathan P. Bollback,et al.  Bayesian Inference of Phylogeny and Its Impact on Evolutionary Biology , 2001, Science.

[66]  W. Kooistra,et al.  Molecular systematics, historical ecology, and phylogeography of Halimeda (Bryopsidales). , 2002, Molecular phylogenetics and evolution.

[67]  L. Medlin.  WHY SILICA OR BETTER YET WHY NOT SILICA? SPECULATIONS AS TO WHY THE DIATOMS UTILISE SILICA AS THEIR CELL WALL MATERIAL , 2002 .

[68]  U. Sorhannus,et al.  RpoA: A Useful Gene for Phylogenetic Analysis in Diatoms , 2003, The Journal of eukaryotic microbiology.

[69]  Victor Smetacek,et al.  Architecture and material properties of diatom shells provide effective mechanical protection , 2003, Nature.

[70]  D. Maddison,et al.  MacClade 4: analysis of phy-logeny and character evolution , 2003 .

[71]  A. Schmid.  The special Golgi-ER-mitochondrium unit in the diatom genusCoscinodiscus , 2004, Plant Systematics and Evolution.

[72]  D. Mann.  Patterns of sexual reproduction in diatoms , 1993, Hydrobiologia.

[73]  P. Lockhart,et al.  Substitutional bias confounds inference of cyanelle origins from sequence data , 1992, Journal of Molecular Evolution.

[74]  A. Schmid.  Aspects of morphogenesis and function of diatom cell walls with implications for taxonomy , 1994, Protoplasma.