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Ciliate Biodiversity and Phylogenetic Reconstruction Assessed by Multiple Molecular Markers Micah Dunthorn University of Massachusetts Amherst, [email protected]

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University of Massachusetts Amherst ScholarWorks@UMass Amherst Open Access Dissertations 9-2009 Ciliate Biodiversity and Phylogenetic Reconstruction Assessed by Multiple Molecular Markers Micah Dunthorn University of Massachusetts Amherst, [email protected] Follow this and additional works at: https://scholarworks.umass.edu/open_access_dissertations Part of the Life Sciences Commons Recommended Citation Dunthorn, Micah, "Ciliate Biodiversity and Phylogenetic Reconstruction Assessed by Multiple Molecular Markers" (2009). Open Access Dissertations. 95. https://doi.org/10.7275/fyvd-rr19 https://scholarworks.umass.edu/open_access_dissertations/95 This Open Access Dissertation is brought to you for free and open access by ScholarWorks@UMass Amherst. It has been accepted for inclusion in Open Access Dissertations by an authorized administrator of ScholarWorks@UMass Amherst. For more information, please contact [email protected]. CILIATE BIODIVERSITY AND PHYLOGENETIC RECONSTRUCTION ASSESSED BY MULTIPLE MOLECULAR MARKERS A Dissertation Presented by MICAH DUNTHORN Submitted to the Graduate School of the University of Massachusetts Amherst in partial fulfillment of the requirements for the degree of Doctor of Philosophy September 2009 Organismic and Evolutionary Biology © Copyright by Micah Dunthorn 2009 All Rights Reserved CILIATE BIODIVERSITY AND PHYLOGENETIC RECONSTRUCTION ASSESSED BY MULTIPLE MOLECULAR MARKERS A Dissertation Presented By MICAH DUNTHORN Approved as to style and content by: _______________________________________ Laura A. Katz, chair _______________________________________ Robert L. Dorit, member _______________________________________ George B. McManus, member _______________________________________ Benjamin B. Normark, member _______________________________________ Joseph S. Elkinton, Graduate Program Director Program in Organismic & Evolutionary Biology To Frank Buchholz 13 February 1952—15 July 1991 ACKNOWLEDGEMENTS Much thanks goes to my dissertation committee. Laura A. Katz, my advisor, provided her support throughout this dissertation. I thank Laura for allowing me to work in her lab and for teaching me many molecular methods. Rob Dorit was able to point out the bigger picture and context. George McManus was great to talk about ciliate evolution and the intricacies of ciliate taxonomy. And Ben Normark was always there to push me towards our current theoretical gaps. Much thanks also goes to Professor Dr. Wilhelm Foissner, who isolated and identified most of the ciliates that were used in this dissertation, and is a co-author on many of the chapters. I am not sure how he was able to put up with me while I visited his laboratory. Chapter 2 was a collaboration with Thorsten Stoeck, Marion Eppinger, M. V. Julian Schwarz, Michael Schweikert, and Jens Boenigk. Denis Lynn collaborated on the PhyloCode classification in Chapter 7. Phil Cantino, the editor for the Companion Volume to which the PhyloCode definitions will be published, was extremely helpful and patient in his edits. This dissertation would also not be possible without the many folks in the Katz lab. I will miss Mary Doherty’s jokes and her insights into ciliate biogeography. The following directly or indirectly also made an impact: Becky Zufall, Sofia Annis, Erica Barbero, Jennifer DeBarardinis, Jessica Grant, Meaghan Hall, Hannah Jaris, Allie Kovner, Dan Lahr, Christina Lyman, Bob Merritt, Laura Parfrey, Maiko Tamura, Yonas Tekle, Sam Torquato, and Laura Vann. Help also came from members of the Organismic and Evolutionary Biology program: Penny Jaques, Norman Johnson, David Lahti, and v Lynn Margulis. Caffeine and delicious vegan snacks were made possible by Melissa Krueger at the Elbow Room Café. Partial funding for this dissertation and for presenting at conferences came from: International Travel Award for Young Scholars, Society for the Study of Evolution; Holz-Connor Travel Grant, International Society of Protozoologists; Mini-PEET Award, Society of Systematic Biologists; Graduate Research Award, Society of Systematic Biologists; Travel Grant, 56th Annual Meeting, Society of Protozoologists; Graduate Fellowship, Massachusetts Space Grant Consortium. Funding was also provided by Laura A. Katz through her U.S. National Science Foundation grant #636498. I would also like to thank my mother and father—Lani and Tom—for their patience and help throughout my time in graduate school. Finally, I want to thank my son—(captain) Aureliano—for thinking that working in the lab consists of watching movies in my office, since that is what he did the so many times I dragged him to the lab so I can perform just more PCR and cloning on a Saturday afternoon. vi ABSTRACT CILIATE BIODIVERSITY AND PHYLOGENETIC RECONSTRUCTION ASSESSED BY MULTIPLE MOLECULAR MARKERS SEPTEMBER 2009 MICAH DUNTHORN, B.A., GEORGE MASON UNIVERSITY M.A., UNIVERSITY OF MISSOURI ST. LOUIS PH.D., UNIVERSITY OF MASSACHUSETTS AMHERST Directed by: Laura A. Katz Ciliates provide a powerful system within microbial eukaryotes in which molecular genealogies can be compared to detailed morphological taxonomies. Two groups with such detailed taxonomies are the Colpodea and the Halteriidae. There are about 200 described Colpodea species that are found primarily in terrestrial habitats. In Chapters 1 and 2, taxon sampling is increased to include exemplars from all major subclades using nuclear small subunit rDNA (nSSU-rDNA) sequencing. Much of the morphological taxonomy is supported, but extensive non-monophyly is found throughout. The conflict between some nodes of the nSSU-rDNA genealogy and morphology-based taxonomy suggests the need for additional molecular marker. In Chapter 3, character sampling is increased using mitochondrial small subunit rDNA (mtSSU-rDNA) sequencing. The nSSU-rDNA and mtSSU-rDNA topologies for the Colpodea are largely congruent for well-supported nodes, suggesting that nSSU-rDNA work in other ciliate clades will be supported by mtSSU-rDNA as well. Chapter 4 compares the underlying genetic variation within two closely related species in the vii Halteriidae with increased taxon and molecular sampling using nSSU-rDNA and internally-transcribed spacer (ITS) region sequencing. The morphospecies Halteria grandinella shows extensive genetic variation that is consistent with either a large effective population size or the existence of multiple cryptic species. This pattern contrasts with the minimal of genetic variation in the morphospecies Meseres corlissi. Chapter 5 discusses the congruence and incongruence among morphological and molecular data in ciliates. Most of the incongruence occurs where there is little statistical support for the molecules, or where molecular data is consistent with alternative morphological hypotheses. Chapter 6 reviews the data for sex, or lack thereof, in the Colpodea, a potentially ancient asexual group where sex was regained in a derived species. In Chapter 7, four ciliate clades are redefined using the PhyloCode. viii CONTENTS Page ACKNOWLEDGEMENTS……………………………………………………………… v ABSTRACT…………………………………………………………………………..…vii LIST OF TABLES………………………………………………………………………xiv LIST OF FIGURES……………………………………………………………………...xv CHAPTERS 1. MOLECULAR PHYLOGENETIC ANALYSIS OF CLASS COLPODEA (PHYLUM CILIOPHORA) USING BROAD TAXON SAMPLING………………….……………..1 1.1. Abstract……………………………………………………………………….2 1.2. Introduction……………………….…………………………………………..3 1.3. Materials and methods…………………….……………………….................7 1.3.1. Taxon sampling and collection……………………………..………7 1.3.2. Identification………………………………………………………..7 1.3.3. DNA extraction, amplification, cloning and sequencing…………...7 1.3.4. Genealogical analyses………………………………………………9 1.4. Results……………………………………………………………………….10 1.4.1. Pairwise distances within collections……………………………...10 1.4.2. Deletion within one SSU rDNA copy in Bryometopus pseudochilodon…………………………………………………..11 1.4.3. Intron in Cyrtolophosis mucicola…………………………………12 1.4.4. SSU rDNA genealogy of the Colpodea…………………………...12 1.5. Discussion…………………………………………………………………...16 1.5.1. Comparisons between morphology and molecules………………..16 1.5.1.1. The class…………………………………………………16 1.5.1.2. The orders……………………………………………….16 1.5.1.3. The genus Colpoda……………………………………...20 1.5.2. Open questions with some species designations………………..…21 1.5.3. Evidence for sex…………………………………………………...22 1.5.4. Group I intron in Cyrtolophosis mucicola………………………...23 1.5.5. Reconciling morphology and molecules in the Colpodea………...24 1.6. References………………………………………………………………...…25 ix 2. PHYLOGENETIC PLACEMENT OF THE CYRTOLOPHOSIDIDAE STOKES, 1888 (CILIOPHORA; COLPODEA) AND NEOTYPIFICATION OF ARISTEROSTOMA MARINUM KAHL, 1931…………………………………………...40 2.1. Abstract……...………………………………………………………………41 2.2. Introduction………………………………………………………………….42 2.3. Methods……………………………………………………………………...43 2.3.1. Taxon sampling……………………………………………………43 2.3.2. Light and electron microscopy…………………………………….44 2.3.3. Terminology……………………………………………………….45 2.3.4. Autecology……………………………………………………...…45 2.3.5. Amplification and sequencing ……………………………………47 2.3.6. Genealogical analyses……………………………………………..48 2.3.7. Constrained analysis……………………………………………....49 2.3.8. Rate class analysis…………………………………………………49 2.4. Results……………………………………………………………………….49 2.4.1. Description of the neotype of Aristerostoma marinum Kahl, 1931………………………………………………………..49 2.4.2. Electron microscopy………………………………………………51 2.4.3. Autecology………………………………………………………..52 2.4.4. Pairwise SSU rDNA sequence differences within the Cyrtolophosididae………………………………………………..52 2.4.5. Genealogical analysis……………………………………………...53
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  • Mixotrophic Protists Among Marine Ciliates and Dinoflagellates: Distribution, Physiology and Ecology

    Mixotrophic Protists Among Marine Ciliates and Dinoflagellates: Distribution, Physiology and Ecology

    FACULTY OF SCIENCE UNIVERSITY OF COPENHAGEN PhD thesis Woraporn Tarangkoon Mixotrophic Protists among Marine Ciliates and Dinoflagellates: Distribution, Physiology and Ecology Academic advisor: Associate Professor Per Juel Hansen Submitted: 29/04/10 Contents List of publications 3 Preface 4 Summary 6 Sammenfating (Danish summary) 8 สรุป (Thai summary) 10 The sections and objectives of the thesis 12 Introduction 14 1) Mixotrophy among marine planktonic protists 14 1.1) The role of light, food concentration and nutrients for 17 the growth of marine mixotrophic planktonic protists 1.2) Importance of marine mixotrophic protists in the 20 planktonic food web 2) Marine symbiont-bearing dinoflagellates 24 2.1) Occurrence of symbionts in the order Dinophysiales 24 2.2) The spatial distribution of symbiont-bearing dinoflagellates in 27 marine waters 2.3) The role of symbionts and phagotrophy in dinoflagellates with symbionts 28 3) Symbiosis and mixotrophy in the marine ciliate genus Mesodinium 30 3.1) Occurrence of symbiosis in Mesodinium spp. 30 3.2) The distribution of marine Mesodinium spp. 30 3.3) The role of symbionts and phagotrophy in marine Mesodinium rubrum 33 and Mesodinium pulex Conclusion and future perspectives 36 References 38 Paper I Paper II Paper III Appendix-Paper IV Appendix-I Lists of publications The thesis consists of the following papers, referred to in the synthesis by their roman numerals. Co-author statements are attached to the thesis (Appendix-I). Paper I Tarangkoon W, Hansen G Hansen PJ (2010) Spatial distribution of symbiont-bearing dinoflagellates in the Indian Ocean in relation to oceanographic regimes. Aquat Microb Ecol 58:197-213.