H. E. A. Schenk et al. (Eds.) Eukaryotism and Springer Berlin Heidelberg New York Barcelona Budapest Hong Kong London Milafi Paris Santa Clara Singapore Tokyo H. E. A. Schenk· R. G. Herrmann· K. W. Jeon N. E. MUller· W. Schwemmler {Eds.} Eukaryotism and Symbiosis Intertaxonic Combination versus Symbiotic Adaptation

With 145 Figures

, Springer Prof. Dr. Hainfried E. A. Schenk Dip!. Biochem. Norbert E. Miiller University of Tiibingen University of Tiibingen Botanical Institute Botanical Institute Auf der Morgenstelle Auf der Morgenstelle 72076 Tiibingen, Germany 72076 Tiibingen, Germany

Prof. Dr. Reinhold G. Herrmann Prof. Dr. Werner Schwemmler University of Munich Free University Berlin Botanical Institute Institute of Physiology Menzinger Str. 67 Krahmerstr. 6 80638 Miinchen, Germany 12207 Berlin, Germany

Prof. Dr. Kwang W. Jeon University of Tennessee at Knoxville Dept. of Biochemistry Knoxville, Tennessee 37996 USA

In collaboration with the International Society of Endocytobiology

Endocytobiology VI, updated edition of the Proceedings of the Sixth International Collo• quium on Endocytobiology and Symbiosis, TUbingen, September 6-10, 1995

Sponsors: Landesgirokasse, Stiftung Natur und Umwelt, Stuttgart Prof Dr. Reinhold G. Herrmann, Manchen Prof Dr. Klaus Wolf. Aachen Vereinigung der Freunde der Universitiit Tabingen (Universitiitsbund e. \1.) ISBN-13: 978-3-642-64598-3 e-ISBN-13: 978-3-642-60885-8 DOl: 10.1007/978-3-642-60885-8 Die Deutsche Bibliothek - CIP-Einheitsaufnahme Eukaryotism and symbiosis: intertaxonic combination versus symbiotic adaption; [proceedings of the Sixth International Colloquium on Endocytobiology and Symbiosis, Tiibingen Septem• ber 6-lO, 1995) I H. E. A. Schenk ... [In collab. with the International Society of Endocytobiol• ogy). - Berlin; Heidelberg; New York; Barcelona; Budapest; Hong Kong; London; Milan; Paris; Santa Clara; Singapore; Tokyo: Springer, 1997

This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned, specifically the rights of , reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilm or in any other way, and storage in data banks. Duplication of this publication or parts thereof is permitted only under the provisions of the German Copyright Law of September 9, 1965, in its current version, and permission for use must always be obtained from Springer-Verlag. Violations are liable for prosecution under the German Copyright Law. © Springer-Verlag Berlin· Heidelberg 1997 Softcover reprint of the hardcover 1st edition 1997 The use of general descriptive names, registered names, trademarks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. Cover Design: Design & Production GmbH, Heidelberg SPIN 10567054 3113137-5 4 3 2 I 0 - Printed on acid-free paper Preface

The rapidly growing interest in the fascinating field of Endocytobiology, the science of both organismic leading to symbiotic adaptations at the cellular level and the integrative potential of cells (intertaxonic combination) originating in new taxonic entities, induced the establishment of a triennial cycle of meetings, the International Colloquium on Endocytobiology and SymbioSis, and the founding of the International Society of Endocytobiology (lSE) in 1983. Since 1980, the colloquium has been held in different places around the world, with an expanding range of topics especially in recent years, indicative of the growth, vitality and momentum of the field. This volume (with important reviews, updated until Spring 1997) <;ontains the proceedings of the Sixth International Colloquium held at the University of Tiibingen on September 6-10, 1995, under the auspices of the International Society ofEndocytobiology. Interdependence among is a law of . The degree of interdepend• ence may vary substantially, and it may range from entirely innocuous events or purely nutritional aspects to obligatorily symbiotic (mutualistic or parasitic) forms. Many interact through surfaces or via some damaged tissues, but a significant fraction has evolved highly sophisticated mechanisms including those which allow for cellular endocytosis. Well-known examples are found in mycorrhizal fungi or among soil , , which in their symbiotic state behave as a quasi-organelle, and tumefaciens which manipulates its by direct gene transfer to provide nitrogenous and carbon compounds that only the bacterium can metabolize. Only very few of such interactions have made an enduring contribution to the development of , i.e. they led to new taxonic entities, most prominent among them being the eukaryotic cell(s). Mitochondria, kinetosomes, hydrogenosomes, and plastids, all organelles of fundamental impor• tance in the living world, are proposed to have come from endocytobionts. Within this frame of diversity, the focussed topics for the Colloquium into two principal aspects (given by the subheadings) rather than giving an overview on the immense multiplicity of symbiotic associations and phenomena, that were subject of the earlier colloquia (see the previous proceedings: Endocytobiology I to V). The two topics were adaptation phenomena associated with extra- and intracellular sym• bioses, and the far-less understood proc,esses and events at the physiological, structural and genomic levels, that lead to unequal intertaxonic combinations of cells from different taxons. Advances in techniques of molecular and cell biology during the past decade have generated unprecedented opportunities for exploring new horizons in under• standing the Life on our planet and its . The molecular phylogenetic analysis to determine how complex organisms have developed, maintained ge• netic integrity over time, and interacted in biological associations is one of the VI most amazing and fascinating chapters in modern biology. However, our knowl• edge of the underlying fundamental processes is still limited, and related data are scattered among various disciplines, often with little relationship to each other. The Tiibingen conference accounted for the interdisciplinary aspects and brought together researchers in various fields of biology, medicine, biochemistry, and biophysics. There it became obvious that an up-to-date account of the state of knowledge in the field was urgently needed, especially since there had been no recent treatment of individual aspects per se, or in combination. This book has been designed to fill a portion of the gap, primarily for the benefit of research workers (e.g., molecular evolutionists), university teachers and advanced students who wish to gain first-hand knowledge on the scope and direction. Written by prominent scientists, these 45 articles cover various topics in both fields. They present an overview of current accomplishments and potential future directions, argue against outdated notions from the traditional biology of the eukaryotic cell, and convey many of the remarkable, recently discovered aspects of the biology of complex cells, organisms, and of their interactions. The organizers and editors thank all chairpersons for giving program proposals, especially P. Wrede, W.-H. Kunau and H.-D. Gortz. They thank the ISE members and other participants who came from Australia, Austria, France, Germany, Great Britain, Hungary, Italy, Japan, The Netherlands, Russia, Spain, Sweden, and USA, and worked out their presentations into stimulating reviews, quite frequently up• dating them until the last minute. They express their special gratitude to the spon• sors of the Colloquium, the University of Tiibingen, the Universitatsbund e.V., who provided support in fmancial, technical as well as other matters, and, regard• ing this book, to the Landesgirokasse Stuttgart, the Association of Friends of the Tiibingen University, Prof. Dr. R.G. Herrmann, Munich, and Prof. Dr. K. Wolf, Aachen, who provided the printing cost. Without such fmancial support this book could not have been produced. The organizers are most grateful to the Dean of the Faculty of Biology, Prof. Hans-Ulrich Seitz, who kindly opened the conference, and also to our colleagues at the Institute of Botany, especially Prof. Hager and Prof. Hampp for their support. An unforgettable event was the awarding of the Miescher-Ishida-Prize to Prof. Masahiro Sugiura for his outstanding work on plastid by the Presi• dent of the Society, Prof. K.W. Jeon. The ceremony included warm words of Dr. Hans Kossel to the prizewinner and a musical frame arranged by a young musical baroque trio ofNoriko and Kazuhiro Fujiwara and Ilka Meyer-Schenk with pieces by Jacques Hoteterre. We are grateful to many assistants and secretaries, workmen and graduate stu• dents at the Institute, particularly Albin Nickol, Birgit Blank and Fred Kippert. Finally the editors thank the Springer Verlag Company for their support produc• ing this volume, and last not least Birgit Blank for her indefatigable effort in set• ting up the content of this volume camera ready.

The Editors Introductory Remarks

During the past decade there has been a radical conceptual change in viewing at the living matter, owing to new biochemical techniques that have allowed a spec• tacular progress in the study of evolution at the molecular level. The concept of "molecular phylogeny", presently one of the most fertile fields in biology, has not only established unequivocally that all life forms fall into one of three lines of descent, , Eubacteria (both ) and - relevant in the context - Eukarya, it has also allowed the formulation of a new concept of eukaryotism. It is now indisputable that the eukaryotic cell with its compartmentalized (e.g. nucleus/cytosol, mitochondria, ), which alone possessed a potential to develop into advanced forms of life, is the result of processes that have changed (endo )cytobioses to the stage of this cell. It is also true that both its generation and its evolution have proceeded in a very complex manner. It can involve as many as five or six originally autonomous cells of different taxonomic origin (intertaxonic combination). Today, the cell may be considered as a "genomic laboratory" with an enormous potential of restructuring genetic material. This concept will ulti• mately lead to a natural, coherent and universal of life as well as to an under• standing of (symbiotic, pathogenic and ecological) organismic interactions at the molecular genetic and/or physiological levels. The new topics include, for in• stance, exogenosomal organellar evolution in contrast to evolutionary adaptation of partners in symbiotic associations, aspects of gene transfer, RNA editing, organel• lar protein import, and even a related nomenclature. The diversity of cases and the rapidly expanding knowledge, which inherently include changes in interpretation, render it difficult to formulate a comprehensive and unequivocal terminology that describes events and genetic make-up of eu• karyotic cells and of processes related to their generation. This uncertainty can be observed in the use of distinct terms in the field of intertaxonic combination: for instance, it is a question of what 'the is: a symbiont or a cell organelle. What is a eukaryotic cell? Is it a host with (like chloroplasts or mitochondria) or a host with endocytobiotic cell organelles or a cellular entity with distinct organelles some of which originate from earlier endocytobionts? These questions do not seem to be trivial as may be simply demonstrated with the terms cyanome and cyanelle. According to the original definition by Pascher, Glaucocysto• phyta (earlier called cyanomes) surely are not symbiotic consortia in comparison with real cyanomes, as the endocytobiotie consortia of with Nostoc, or Rhizosolenia with intracellularis are. It should also be obvious that a term like "symbiosis" can only be used for living systems and not for chemical (mole• cular) "complexes" at the level of inanimate matter. Clearly, there is a need for a generally agreed terminology that describes the outlined complex biology appro• priately. The editors endeavored to standardize the text to some extent, taking care that introduced changes did not distort the intended meaning. The Glossary also provides some defmitions which may contribute to resolve controversial points.

The Editors VIII

Glossary biont (Hawksworth 1988): biological system with the ability of genetically independent reproduction (genetically autonomous biological system). cell organelle: cell compartment with distinct functions (normally surrounded by at least one envelope membrane) composed additionally by proteins of which at least some are encoded on nuclear DNA. Phylogenetically 2 forms are distinguished: ~- and endogenosomes. complex plastid: an exogenosome of phyletic secondary or tertiary order. cyanelle: genetically autonomous, symbiotic living cyanobacterium (like a zoochlorella, Pascher 1929: "Cyanelle bezeichnet eben eine endosymbiontisch lebende Blaualge gegeniiber der freilebenden. Cyanelle solI so wenig ein systematischer Begriff sein wie Zoochlorelle und Zooxanthelle"). The term should not be used any more for photosynthetic glaucocystophytan chromatophores which are exogenosomes on the status ofplastids (cyanoplasts). cyanome (Pascher 1929): symbiotic consortium, consisting of host and cyanelle. cyanoplast (Schenk 1990): eukaryotic, photo (hydro)trophic cell organelle, with regard to di• stinct cyanobacterial characteristics obviously originating from a former cyanelle by lITe. cytobiont: a biont associated either endo- or epi-cytobio(n)tic with the host cell. dibiont: a symbiotic consortium of two bionts, e.g. adibiontic (Hawksworth 1988). endocytobiont: a facultative or obligate intracellular biont. endogenosome (phylogenetic term, Schenk 1992): usually a membrane-bounded cell organelle with an endogenous (autogenous) origin. : following Smith and Douglas (1987) a biont which "occurs within host cells" (endocytobiont) "or" (only in multicellular hosts also) "outside them (extracellular)". exogenosome (phylogenetic term, Schenk 1992a): per definitionem a cell organelle (con• taining DNA or not), descending from a former cytobiont, which finally and irreversibly has come under the genomic control of the former host cell by IITC (contrast: "endogenosome", an organelle as autogenous product of a pro- or eukaryotic cell). intertaxonic combination (lTC, Sitte 1991): intracellular processes (including gene trans• fer) changing a symbiotic consortium towards a new taxon by irreversible combination (mixing) of the original symbiotic (Sitte 1991). The observed gene transfer is unequal (IITC), proceeding mainly from the cytobiont towards the former host nucleus (" endocytobiologica1 rule", Sitte 1991). IITC changes a dibiont towards a monobiont system. Serial Endosymbiosis Theory (SET, Taylor 1974): ITC is not only a unique event (Endo• symbiosis Theory, EST, Margulis 1970), but happened several times in series towards complex exogenosomes (complex plastids). symbiosis: " ... Zusarnmenleben ungleichnarniger Organismen ... " (de Bary 1879), "a per• manent or long-lasting (Smith and Douglas 1987) association of differently named bionts". This broad definition includes both parasitic and mutualistic heterologous associations. (Roth, Jeon and Stacey 1988): cell compartment composed by one or more cells of the endocytobiont (symbiont) and by the symbiosome (outer envelope) membrane, also called perisymbiontic (e.g. perialgal, peribacteroid) membrane. In case of one symbi• ont per symbiosome its plasmalemma represents the inner envelope of the symbiosome. can be newly formed, artificially or naturally, dependent on the ontogenetic stage of the partners, or can be transmitted from one to the next generations. Contents

Part I Intertaxonic Combination and the Origin and Differentiation of the Cell

1.1 Phylogeny of Exogenosomes

Origin and Evolution of Chloroplasts: Current Status and Future Perspectives 3 K.KOWALLIK What's Eu? The Role of EukaryotelEukaryote Endosymbioses in Plastid Origins 24 G.!. MCFADDEN The Complete Sequence of the Cyanelle Genome of Cyanophora paradoxa: The Genetic Complexity of a Primitive Plant 40 W. LOFFELHARDT, V. STIREWALT, C.B. MICHALOWSKI, H.I. BOHNERT, D. BRYANT Plastid-like Organelles in Anaerobic Mastigotes and Parasitic Apicomplexans 49 1.H.P. HACKSTEIN, H. SCHUBERT, 1. ROSENBERG, U. MACKENSTEDT, M.VAN DEN BERG, S. BRUL, 1. DERKSEN, H.C.P. MATTHIJS Complete Mitochondrial DNA Sequence of Budding Hansenula wingei Indicates Its Intermediary Characteristics Between Those of and Filamentous Fungi 57 T SEKITO, K.OKAMOTO, H. KITANO, K. YOSHIDA Biogenesis of Hydrogenosomes in Psalteriomonas lanterna: No Evidence for an Exogenosomal Ancestry 63 1.H.P. HACKSTEIN, 1. ROSENBERG, C.A.M. BROERS, H.C.P. MATTHIJS, C.K. STUMM, G.D. VOGELS x

1.2 Intertaxonic Combination and Gene Transfer (Interspecific, Intracellular)

Eukaryotism, Towards a New Interpretation 73 R.G. HERRMANN Obituary: Hans Kossel (1934-1995) 119 P. SITTE Transcript Editing in Chloroplasts of Higher 123 R. BOCK, F. ALBERTAZZI, R. FREYER, M. FUCHS, S. RUF, P. ZELTZ, R.M. MAIER The Mobile Introns in Yeast Mitochondria: A Short Review and New Data 138 B. SCHAFER, K. WOLF Gene Transfer from Zygomycete Parasitella parasitica to Its Hosts: An Evolutionary Link Between Sex and ? 145 J. WOSTEMEYER, A. WOSTEMEYER, A. BURMESTER, K. CZEMPINSKI Trans-Kingdom Conjugation as a Model for Gene Transfer from Endosymbionts to Nucleus During the Origin of Organelles 153 K. YOSHIDA, K. KAMIn, A. MAHMOOD, T. SEKITO, H. ISHITOMI Chronobiology and Endocytobiology: Where Do They Meet? 165 F.KIPPERT

1.3 Protein Import into Cell Organelles• Exogenosomes and Endogenosomes

Evolution of Protein Sorting Signals 191 G. VON HEIJNE Protein Import into Peroxisomes 195 R. ERDMANN, W.-H. KUNAU Membrane Transport of Proteins: A Multitude of Pathways at the Thylakoid Membrane 206 R.B. KLOSGEN, J. BERGHOFER, 1. KARNAUCHOV Analysis of Mitochondrial and Chloroplast Targeting Signals by Neural Network Systems 214 G. SCHNEIDER, J. SCHUCHHARDT, A. MALIK, J. GLIENKE, B. JAGLA, D. BEHRENS, S. MULLER, G. MULLER, P. WREDE XI

1.4 Metabolic Control and Ontogenetic Regulations Between Exogenosomes and Nucleus

Impact of Plastid Differentiation on of Nuclear and Mitochondrial Genes 233 W.R. HESS, B. LINKE, T. BORNER Glucose-6-Phosphate Dehydrogenase Isoenzyrnes from Cyanophora paradoxa: Examination of Their Metabolic Integration Within the Meta- Endocytobiotic System 243 T. FESTER, H.E.A. SCHENK The Phycobiliproteins Within the Cyanoplasts of Cyanophora paradoxa Store Carbon, Nitrogen, and Sulfur for the Whole Cell 252 N.E. MULLER, O. HAULER, H.E.A. SCHENK

1.5 Molecular evolution

Hypercycles in Biological Systems 263 M.GEBINOGA Evolutionary Optimization of Enzymes and Metabolic Systems 277 R. HEINRICH The Endocytobiological Concept of Evolution: A Unified Model 289 W. SCHWEMMLER Giglio-Tos and Pierantoni: A General Theory of Symbiosis that Still Works 300 F.M.SCUDO

Part II Symbiotic Systems Adaptation, Signal Transduction, Taxonomy and Evolution

2.1 Molecular Approach to Taxonomy of Endocytobionts

Progress in the Studies of Endosymbiotic from Larger Foraminifera 329 J.1. LEE, J. MORALES, 1. CHAI, C. WRAY, R. ROTTGER Phylogeny Reconstruction Based on Molecular Property Patterns 345 W. SCHMIDT XII

2.2 Endocytobionts in and Invertebrates

Symbiosis and Macromolecules 359 K.W.JEON Acidification in Digestive Vacuoles Is an Early Event Required for Holospora Infection of Paramecium Nucleus 367 M. FUJI SHIMA, M. KAWAI Monoclonal Antibody Specific for Activated Form of Holospora obtusa, a Macronucleus-Specific Bacterium of Paramecium caudatum 371 M. KAWAI, M. FUJISHIMA Interactions of Host Paramecia with Infectious Holospora Endocytobionts 375 E. BAIER, H.-D. GORTZ Appearance of Viable Bacteria in Acanthamoeba royreba After Amoebic Exposure to Megarad Doses of Gamma Radiation 379 A.A. VASS, R.P. MACKOWSKI, R.L. TYNDALL Endosymbiosis of Sogatodes orizicola (Muir: Insecta) with Yeast-like Symbionts 389 E. KREIL, H. TAUCHERT, G. HOHEISEL, S. RICHTER A Chaperonin-Like Protein in the Principal Endocytobiotes of the Weevil Sitophilus 395 H. CHARLES, A. HEDDI, P. NARD ON

2.3 Symbiotic Plant Microbe/ Interactions

Host Signals Dictating Growth Direction, Morphogenesis and Differentiation in Arbuscular Mycorrhizal Symbionts 405 M. GIOVANNETTI Role of Fungal Wall Components in Interactions Between Endomycorrhizal Symbionts 412 A. GOLLOTTE, C. CORDIER, M.e. LEMOINE, V. GIANINAZZI-PEARSON Control of Elicitor-Induced Reactions in Spruce Cells by Auxin and by Enzymatic Elicitor Degradation 429 P. SALZER, R. MENSEN, G. HEBE, K. GASCHLER, A. HAGER A Novel IS Element is Present in Repeated Copies Among the Nodulation Genes of Rhizobium 'hedysari' 441 F. MENEGHETTI, S. ALBERGHINI, E. TOLA, A. GIACOMINI, F.J. OLLERO, A. SQUARTINI, M.P. NUTI XIII

Effect of Drought Stress on Carbohydrate in Nodules of Lupinus angustifolius 449 M.L. COMlNO, M.R DE FELIPE, M. FERNANDEZ-PASCUAL, L.MARTIN Creation of Artificial Symbiosis Between and Higher Plants 457 E. PREININGER, P. KORANYI, I. GYURJAN

2.4 Intra- and Extracellular Interactions Between Phycobionts and Mycobionts

News on Geosiphon pyriforme, an Endocytobiotic Consortium of a Fungus with a Cyanobacterium 469 M. KLUGE, H. GEHRIG, D. MOLLENHAUER, R. MOLLENHAUER, E. SCHNEPF, A. SCHUSSLER Isoforms of Arginase in the Evernia prunastri and Xanthoria parietina: Physiological Roles and Their Implication in the Controlled Parasitism of the Mycobiont 477 M.e. MOLINA, C. VICENTE, M.M. PEDROSA, M.E. LEGAZ Comparison Between Recent-Isolated and Cultured Populations of Phycobionts from Xanthoria parietina (L.) 484 M.C. MOLINA, E. STOCKER-WORGOTTER, R. ZORER, R. TORK., C. VICENTE Presence and Identification of Polyamines and Their Conjugation to Phenolics in Some Epiphytic Lichens 491 J.L. MATEOS, M.E. LEGAZ

2.5 Vertebrate Evolution and Medical Significans

Intestinal Methanogens and Vertebrate Evolution: Symbiotic Archea are Key Organisms in the Differentiation of the Digestive Tract 501 J.H.P. HACKSTEIN, P. LANGER Pleomorphic Bacterial Intracytoplasmic Bodies: Basic Biology and Medical Significance 507 G.J. DOMINGUE

List of Authors and Participants 519 Photograph of Many of the Participants (by W. Schwemmler) 521 Subject Index 523