sign in sign up
<<
Home , Michael Melkonian, Protistology

EVOLUTIONARY The as Cell

Proceedings of the 5th Meeting of the International Society for Evolutionary Protistology, Banyuls-sur-Mer, France, June 1983

Edited by

LYNN MARC ULIS Boston University

MARIE-ODILE SOYER-COBILLARD Laboratoire Arago

JOHN CORLISS University of Maryland

Reprinted from Origins ofLife , Volume 13, Nos. 3-4

D. Reidel Publishing Company

Dordrecht I Boston ISBN- I 3 978-94-009-6400-6 c-ISBN- I 3 978-94-009-6398-6 DOl 10 1007/978-94-009-6398-6 All Righ ts Reserved © 1984 by D. Reidel Publishing Company, Dordrecht, Holland Softcover reprint of the hardcover 15t edition 1984 No part of the material protected by this copyright notice may be reproduced or utilized in any form or by any means, electronic or mechanical including photocopying, recording or by any information storage and retrieval system, without written permission from the copyright owner TABLE OF CONTENTS

List of Participants vii Foreword ix M. LITTLE, R. F. LUDUENA, L. C. MOREJOHN, C. ASNES, and E. HOFFMAN I The Tubulins of , , Fungi and - Implications for Metazoan Evolu• tion 169 A. ADOUTTE, M. CLAISSE, and J. CANCE I Tubulin : An Electrophoretic and Immunological Analysis 177 U.-P. ROOS I From Proto- to Mitosis - An Alternative Hypothesis on the Origin and Evolution of the Mitotic Spindle 183 C. GALLERON I The Fifth Base: A Natural Feature of DNA 195 M. HERZOG, S. VON BOLETZKY, and M.-O. SOYER I Ultrastructural and Biochemical Nuclear Aspects of Classification: Independent Evolution of the Dino- as a Sister Group of the Actual ? 205 E. B. SMALL I An Essay on the Evolution of Ciliophoran Oral Cytoarchitecture Bases on Descent·from Within a Karyorelictean Ancestry 217 S. E. LENK, E. B. SMALL, and J. GUNDERSON I Preliminary Observations of Feeding in the Psammobiotic Tracheloraphis 229 D. L. LIPSCOMB I Methods of Systematic Analysis: The Relative Superiority of Phylogenetic Systematics 235 V. MACHELON, 1. GIfNERMONT, and Y. DATTEE I A Biometrical Analysis of Morpho- logical Variation Within a Section of Genus Eupiotes (Ciliata, Hypotrichida), with Special Reference to the E. vannus Complex of Sibling Species 249 P. A. KIVIC and P. L. WALNE I An Evaluation of a Possible Phylogenetic Relationship between the Euglenophyta and 269 R. K. ZAHN I A Green Alga with Minimal Eukaryotic Features: Nanochlorum Eucaryotum 289 G. BRUGEROLLE and J.-P. MIGNOT / The Cell Characters of Two Helioflagellates Related to the Centrohelidian Lineage: Dimorpha and Tetradimorpha 305 C. FEBVRE-CHEVALIER and J. FEBVRE / Axonemal Microtubule Pattern of Cienkowskya Mereschkovskyi and a Revision of Heliozoan Taxonomy 315 J. THEODORIDES I The Phylogeny of the Gregarinia (Sporozoa) 339 I. DESPORTES I The Paramyxea Levine 1979: An Original Example of Evolution Towards Multicellularity 343

l. Michel Herzog 12. John Dodge 23. David Patterson 34. Michelle Laval-Peuto 45. M. C. Tellez 57. Susan Lenk 2. Paul Prevot 13. Christine Metivier 24. Claude Grevet 35. Jean Genermont 46. Monique Cachon 58. Morris Alexander 3. Colette Galleron 14. Marie Albert 25. Peter Westbroek 36. Deniis Searcy 47. Thos Cavalier-Smith 59. Melvyn Little 4. F. J. R. Taylor 15. Guy Brugerolle 26. Drs Peter Roos 37. Guy Orrison 48. Richard Luduefia 60. Diana Lipscomb 5. Marie-Odile Soyer 16. Pilar Garcia 27. Colette Demar 38. Josette Rouviere-Yaniv 49. Faye Murrin 61. David Lloyd 6. Annie Boillot 17. Isabella Desportes 28. Veronique Machelon 39. Jean Cachon 50. Giinther Bahnweg 62. 7. Yvonne Bhaud 18. M.Dynner 29. Patricia Walne 40. 1. Bren tHea th 51. 63. Jerome Motta 8. Peter Rizzo 19. Martin Estrada 30. John Corliss 41. Betsy Dexter-Dyer 52. S. T. Moss 64. Dennis Goode 9. Peter Kivic 20. qlivind Moestrup 31. Alvin Poppenheimer 42. Robert Allen 53. John Heisler 65. Christian Bandele 10. David Sigee 21. I.-P. Mignot 32. Andre Lwoff 43. Gisele Bardele 54. Andre Adoutte 66. Vincent Demoulin 11. Anton Bopman 22. Marcella Lefotron 33. Alain Bilbaut 44. Mrs. Motta 55. Gil Rosano 67. Eugene Small 56. Lisa MaeKerracher 68. Jean Febvre LIST OF PARTICIPANTS

I.S.E.P.1983

Adoutte Andre, Centre de genetique moleculaire, C.N.R.S., 91190 Gif-sur-Yvette (France) Albert Marie, Laboratoire Arago, 66650 Banyuls-sur-Mer (France) Allen Robert D., Department of Biological Science, Dartmouth College, Hanover, NH, 03755 (U.S.A.) Bahnweg Gunther, Institut fiir Mikrobiologie der Universitiit Giittingen, Grisebachstrasse 8, 34 Giittingen (F.R.G.) Bardele C F., Institut fiir Biologie III, Lehrstuhl Zoologie, Auf der Morgenstelle 74, Tiibingen (F.R.G.) Bhaud Yvonne, Labomtoire Arago, 66650 Banyuls-sur-Mer (France) Bilbaut A., Laboratoire d'Histologie et Biologie tissulaire, Cniversite Claude Bernard - Lyon I, 43 Boulevard du II novembre, 69621 Villeurbanne (France) Billy (de) Fran90ise, Laboratoire Arago, 66650 Banyuls-sur-Mer (France) Boillot Annie, Laboratoire Zoologique, La Darse, 06300 Villefranche-sur-Mer (France) Boletzky Sigurd (von), Laboratoire Arago, 66650 Banyuls-sur-Mer (France) Borman Anton H., Biochemisch Laboratorium, Rijksuniversiteit Leiden, Wassenaarseweg 64 2333 AL Leiden (Holland) Brugerolle Guy, Laboratoire de Zoologie, Complexe scientifique des Cezeaux, B.P. 45, Les Cezeaux, 63170 Aubiere (France) Cachon Jean, Laboratoire de Protistologie marine, Station de Biologie marine, 06230 Villefranche-sur-Mer (France) Cachon Monique, Laboratoire de Protistologie marine, Station de Biologie marine, 06230 Villefranche-sur- Mer (France) Cavalier-Smith T., University of London Kings College, 26 Drury Lane, London WC2B 5RL (U.K.) Corliss John 0., Department of , University of Maryland, College Park, MD 20742 (U.S.A.) Demar Colette, Laboratoire de Zoologie, 46 rue d'Ulm, 75230 Paris Cede x 05 (France) Demoulin V., Departement de Botanique, Universite de Liege, Sart Tilman, 4000 Liege (Belgium) Dcsportes Isabelle, Laboratoire d 'evolution des Ftres organises, 105 Boulevard Raspail, 75006 Paris (France) Dodge J. D., Department of , Royal Holloway College, Huntersdale Callow Hill, Virginia Water, Surrey GU 25 4LN (CX.) Febvre Colette, Laboratoire de Protistologie marine, Station de Biologie marine, 06230 Villefranche-sur• Mer (France) Febvre Jean, Laboratoire de Protistologie marine, Station de Biologie marine, 06230 Villefranche-sur-Mer (France) Fernandez-Leborans G., Laboratorio de Biologia general, Facultad de Biologia, Universitad Complutense, Ciudad Universitaria, Madrid 3 (Spain) Gadea Enrique, Departamento de Zoologia, Facultad de Biologia, Universitad de Barcelona, Gran Via 585, Barcelona 7 (Spain) Galbon Colette, 64 rue Dutot, 75015 Paris (France) Genermont Jean, Laboratoire de Zoologie, Universite Paris Sud, 91405 Orsay (France) Gil Rosario, CS.I.C, Institut Immunologia y Biologia Microbiana, Velazquez 144. Madrid 6 (Spain) Goode D., Department of Zoology, University of Maryland, College Park, MD 20742 (U.S.A.) Gracia-Royo M. P., Departamento de Zoologia, Universitad de Barcelona, Gran via 585, Barcelona 7 (Spain) . Grain J., Groupe de Zoologie et Protistoiogie, Universite de Clermont, Complexe Scientifique des Cezeaux, B.P. 45, 63170 Aubiere (France) Greuet C, Laboratoire de Biologie animalc et Cytologie, Faculte des Sciences, 06034 Nice Cedex (France) Grosovsky Betsey, Department, Boston University, 2 Cummington Street, Boston, MA02215 (U.S.A.) . Heath I. B., Department of Biology, York University, 4700 Keele Street, Downsview, Ontario M3J IP3 (Canada)

Origins of 13 (1984), vii. viii LIST OF PARTICIPANTS

Heisler J. J., Department of Zoology, University of Maryland, College Park, MD 20742 (U .S.A.) Herzog Michel, Laboratoire Arago, 66650 Banyuls-sur-Mer (France) Kivic P., Botany Department, University of Tennessee, Knoxville, TN 37916 (U.S.A.) Lefort-Tran Marcelle, CNRS, Cytophysiologie de la Photosynthese, 91190 Gif-sur-Yvette (France) Lenk Susan E., Department of Zoology, University of Maryland, College Park, MD 20742 (U .S.A.) Li Jing Yan, Kunming Institute of Zoology, Academia Sinica, Kunming, Yunnan Province (China) Lipscomb D. L., The George Washington University, Department of Biological Sciences, Washington, DC 20052 (U.S.A) Little Melvyn, German Cancer Research Center, Institute of Cell and Tumor Biology, 1m Neuenheimer Feld 280, Heidelberg (F.R.G.) Lloyd David, University College, Newport Road, CardiffCF2 ITA (U.K.) Luduefia R. F., Department of Biochemistry, University of Texas Health Science Center, San Antonio, TX 78284 (U.S.A.) Lwoff Andre, 69 avenue de Suffren, 75007 Paris (France) Machelon V., Laboratoire de Zoologie, Universite Paris Sud, 91405 Orsay (France) MacKerracher Lisa, York University, Department of Biology, 4700 Keele St., Downsview, Ontario M3J IP3 (Canada) Margulis Lynn, Biology Department, Boston University, 2 Cummington Street, Boston, MA 02215 (U.S.A.) Melkonian Michael, Botanisches Institut, Schlossgarten 3, 4400 Munster (F.R.G.) Metivier Christine, Laboratoire Arago, 66650 Banyuls-sur-Mer (France) Mignot Jean-Pierre, Laboratoire de Zoologie, Complexe scientifique des Cezeaux, B.P. 45, 63170 Aubiere (France) Moestrup Ojvind, Kobenhavns Universitet, Institut fUr Sporeplanter, Ofarimagsgade 2 D, 1353 Kobenhavn (Denmark) Moss Stephen, Biological Sciences, Portsmouth Polytechnic, King Henry Building, King Henry Street, Portsmouth P012DY (U.K.) Motta J., Department of Botany, University of Maryland, College Park, MD 20742 (U .S.A.) Murrin Faye, York University, Faculty of Science, 4700 Keele Street, Downsview, Ontario M35 IP3 (Canada) Ourisson Guy, Universite Louis Pasteur, Institut de Chimie, 1 rue Blaise Pascal 67008 Strasbourg Cedex (France) Papenheimer Alvin, Harvard University, Biological Laboratory, 16 Divinity Avenue, Cambridge, MA02138 (U.S.A.) Patterson D. J., Department of Zoology, University of Bristol, Woodland Road, Bristol BS8 1UG (U.K.) Peuto Michele, Laboratoire de Protistologie marine, Universite de Nice, Parc Valrose, 06034 Nice Cedex (France) Prevot Paul, Laboratoire Arago, 66650 Banyuls-sur-Mer (France) Puytorac P., Biologie comparee des Protistes, Universite de Clermont-Ferrand Les Cezeaux, B.P.45, 63170 Aubiere (France) Rizzo Peter, Biology Department, Texas A. & M. University, College Station, TX 77843 (U.S.A.) Roos V. P., Department de Cytologie, Universite de Zurich, Zurich (Switzerland) Rouviere-Yaniv, Institut Pasteur, 25 rue du Dr. Roux, 75724 Paris Cedex 15 (France) Searcy D. G., Zoology Department, University of Massachusetts, Amherst, MA 01003 (U.S.A.) Sigee David, Department of Botany and Zoology, University of Manchester, Manchester (U.K.) Small E., Deprtment of Zoology, University of Maryland, College Park, MD 20742 (U.s.A.) Soyer-Gobillard Marie-Odile, Laboratoire Arago, 66650 Banyuls-sur-Mer (France) Surek Barbara, Botanisches Institut, Schlossgarten 3,4400 Munster (F.R.G.) Taylor F. J. R., The University of British Columbia, 6270 University Boulevard, Vancouver, BC V6T 1W5 (Canada) Tellez M. C., Institut d'Oceanographie, Paseo Nacional, Barcelona (Spain) Theodorides Jean, Laboratoire d'Evolution des Etres organises, 105 Bd.Raspail, 7500 Paris (France) Walne P. L., Department of Botany, University of Tennessee, Knoxville, TN 37916 (U.S.A.) Westbroek Peter, Department of Biochemistry, Leiden University, Wassenaarseweg 64,2333 AL Leiden (Holland) FOREWORD

INTERNATIONAL SOCIETY FOR EVOLUTIONARY PROTISTOLOGY (ISEP)

5th International Meeting

Banyuls-sur-Mer, France, June 4-6, 1983

For the first time since its inception, at Boston University in June 1975 1, the Society for Evolutionary Protistology met in Europe. Under the direction of Marie-Odile Soyer• Gobillard and hosting some 70 people representing a dozen nations (Belgium, Canada, Denmark, England, France, W. Germany, The Netherlands, Poland, Scotland, Spain, Switzerland, U.S.A.) the meeting was held at Banyuls-sur-Mer in Catalunya. The 1983 ISEP met at the famed Laboratoire Arago on the Mediterranean Sea, most partici• pants were housed in the Laboratory's newly refurbished Grand Hotel. The previous meetings had emphasized single themes, e.g., (First) Boston, 1975 Evolution of Mitosis in Eukaryotic : (Second) Downsview Ontario, 1977 Criteria for Phylogeny in Protists. In spite of the fact that the third meeting, planned for Leeds, England in June of 1979, was never held some of the papers scheduled to be presented there were published in BioSystems, Volume 12, Numbers 1 and 2. The fourth meeting at Port Deposit, Maryland, 1981 called Conference on Cellular Evolution focused on the Evolution of Micro tubules, Mitosis, Microfilaments and other Fibrillar Systems. The proceedings of this meeting were published in BioSystems, Volume 14, Numbers 3 and 4. This fifth meeting was planned around multiple themes: Experimental methods in studying evolution, uniformity and diversity in protistan structure, relationships between protistan phyla, relationship between nucleoid and cytoplasm in archaebacteria and nucleus and cytoplasm in eukaryotic cells, dinoflagellate chromosome organization and the origin of muticellu• larity. The papers from this 5th meeting are here (Origins of Life vol. 13, p. 169-352 as the journal and the book) with the exception of contributions by Li-Jing Yang, D. Sigee, J. Dodge, P. Rizzo and Morris that deal with . Those four promptly submitted papers appeared in BioSystems vol. 17, 1984. The invited speaker at the meeting, Professor Guy Ourisson of the University ofStrasbourg, introduced the protistologists to the power of organic geochemistry. He discussed studies of secondary in aiding the interpretation of phylogenies as well as the use of organic geochemical analysis in the, interpretation of the fossil history of photosynthetic

1 See BioSystems, Volume 7, Numbers 3 and 4, Symposium on The Evolution of Mitosis in Eukaryotic Microorganisms.

Origins of Life I3 (1984), ix. x FOREWORD

microbes and plants. Nobel Laureate, Andre Lwoff whose book of ciliate morphoge• nesis2 and techniques of ciliate cortical staining (Chatton-Lwoff technique) has provided protistological inspiration since the 1940's, was in attendance and introduced Professor Ourisson. As emphasized by John Corliss of the University of Maryland, the protists ( lato, by which he means the protoctists, eukaryotic exclusive of members of the Kingdoms Animalia, Plantae and Fungi) comprise a far larger and diverse group of organisms than most realize. Corliss estimates that there are more than 110,000 species of protists comprising perhaps 40 major lineages or phyla. These organisms include the 'water molds' or so-called 'motile fungi' such as Saprolegnia and other oomycotes that are serving as excellent material to provide the basis for understanding of mitotic movement and sexuality. This was amply demonstrated by Professor 1. B. Heath and his group (F. Murrin and L. MacKerracher). A general theory of the evolution of mitotic movements was presented by U.-P. Roos from Zurich. The polyphyly of multicellularity was demonstrated by the work of Isabelle Desportes (Paris), in work on the bizarre life cycle of the Paramarteilia (myxospo• ridians, parasite of Polychaetes) in which cells develop inside other cells of the same organism. The use of microtubular ultrastructural patterns to assess relatedness has become apparent to everyone. Both the taxonomy of heliozoans (Colette and Jean Febvre, Villefranche-sur-Mer) and the taxonomy of (Eugene Small, College Park, Maryland) are being extensively revised. The concept of kinetid (cinetid), the unit pattern of cell cortex which is comprised of the basal structure of microtubules and microfibrils surrounding the kinetosome, is becoming crucial in the explication of the phylogeny of members of the protoctists, independent of the presence ofplastids. The importance of the heterotrophic portion of the cell was elegantly pointed out by P. Kivic and P. Walne (Tennessee) in a paper that showed members of the and Kinetoplastids (the group to which Trypanosoma belongs) to be far more related than euglenoids and, for example, the chlorophyte green . The importance of protists in the elucidation of fundamental cell problems was demonstrated by several speakers. The presence of striated fibers involved in cell calcium regulation and movement was shown by M. Melkonian (Munster) in his work on the prasinophyte Tetraselmis (= Platymonas). Biomineralization, for example, the intracellular production of calcium carbonate tests, is optimally studied in the (coccolithophorids), as shown by P. Westbroek from Leiden. A fascinating hypothesis that relates light perception and directed behavior in dinoflagellates was presented by J. Dodge (Surrey) in a paper that involves a strand of microtubules (originating at the base of the longitudinal undulipodium). This strand of microtubules passes over the eyespot (in two rather different species of dinoflagellates each with different eyespot organization). Dodge

2 Problems of Morphogenesis in Ciliates: The Kinetosomes in Development, and Evolution, 1950. New York: Wiley Publishers. FOREWORD xi

suspects that the microtubules have a direct role in the transmission of directional stimuli that bring about the phototropic response. The uniqueness of the genetic organization of dinoflagellates was emphasized by several investigators (M. Herzog, M. O. Soyer-GobiIlard, Banyuls-sur-Mer: Peter Rizzo, College Station; David Sigee, Manchester: and C. Galleron of Paris). Apparently the high quantity of hydroxy methyl uracil which replaces so much thymine in dinoflagellates appears in the DNA by means of a post-replicative mechanism. The peculiar characteristics of the dinoflagellates' nuclei strongly suggest that this group is monophyletic and has evolved independently of the other eukaryotes. The tubulin proteins, especially beta-tubulin, comprising undulipodia are re• markably conserved in the great range of eukaryotes studied. On the other hand M. Little (Heidelberg), R. Luduefia (San Antonio) and their colleagues have shown that variations in alpha-tubulin provide fine tools for reconstructing the phylogeny of eukaryotic microbes and their relationships to animals and plants. Nonanimal alpha• tubulins, as determined by peptide digest studies, of the cytoplasm of a (rose) are nearly identical to the alpha-tubulins of the and ciliates tested, and are very similar to cytoplasmic alpha-tubulins of the plasmodial Physarum and the heliozoan Echinosphaerium. These are in marked contrast to alpha-tubulins which closely resemble each other. These investigators including Andre Adoutte (Gif• sur-Yvette) hope to use tubulin sequence data and immunocytochemistry to solve the thorny problem of which protists were ancestral to animals and plants. Another approach to this classical problem came from C. Bardele (Tiibingen) who showed that the details of the undulipodial necklace (membrane patterns, as revealed by freeze etching on the inside of cilia and sperm tails) show a close relatedness in all animals studied but are far more varying in protists. Perhaps by finding the pattern most like that ofthe metazoa, the extant lineage most closely related to the ancestral animals will eventually be identified. Many ISEP members who participated in this meeting are also contributing to the Handbook ofProtoctists. This handbook, edited by Lynn Margulis, John Corliss and David Chapman, is scheduled to be published in early 1985 by Jones and Bartlett Publishers. It will be one volume with chapters on each phylum in Protoctista. P. Westbroek, P. Walne and P. Kivic, E. Cox, M. Melkonian, E.Small and D. Lynn, and D. Barr are some of these authors. Due to the hard work of I. Brent Heath, the fledgling ISEP has achieved legal status as an international nonprofit scientific organization, registered in Canada. According to the by-laws a regular member of ISEP "shall be persons having an interest in the origin, evolution and phylogeny of eukaryotic organisms who have made an appli• cation to and have been accepted by the Secretary". The presidency of the Society has now passed from Christian Bardele to Professor Heath. The Secretary is Dr. Diana Lipscomb. It was decided after much discussion that the next biennial meeting will be held again in North America, at Ottawa June 10-14 1985, under the direction of Dr. Donald Barr. At that time Dr. Dennis Goode (University of Maryland), who was elected President Elect ofISEP at Banyuls, will begin his presidency. xii FOREWORD

The Banyuls meeting was beautifully organized, aid was forthcoming from several sources. Sources of money were: Centre National de la Recherche Scientifique (Secteur sciences de la vie), C.N.R.S. - PIRO (Programme interdisciplinaire pour la recherche oceanographique), Universite Pierre et Marie Curie, Paris VI, Association Naturalia et Biologia (Paris). The food was remarkable and many participants greatly enjoyed their visit to Tautauvel, the small Catalunyan town. It was here, in the cave of Arago, that a fine fossil skull and other bones and teeth of Homo erectus, about 400,000 years old, have been found. These represent the oldest evidence for early man in Europe demonstrating the extreme desirability as living space ofthis magnificent, ancient part of the world. I thank I. B. Heath, B. Dexter Dyer, Donna Mehos, and Marie-Odile Soyer• Gobillard for aid in preparing this report.

LYNN MARGULIS