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Systematics of Protosteloid Amoebae Lora Lindley Shadwick University of Arkansas

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Systematics of Protosteloid Amoebae Lora Lindley Shadwick University of Arkansas University of Arkansas, Fayetteville ScholarWorks@UARK Theses and Dissertations 12-2011 Systematics of Protosteloid Amoebae Lora Lindley Shadwick University of Arkansas Follow this and additional works at: http://scholarworks.uark.edu/etd Part of the Comparative and Evolutionary Physiology Commons, and the Organismal Biological Physiology Commons Recommended Citation Shadwick, Lora Lindley, "Systematics of Protosteloid Amoebae" (2011). Theses and Dissertations. 221. http://scholarworks.uark.edu/etd/221 This Dissertation is brought to you for free and open access by ScholarWorks@UARK. It has been accepted for inclusion in Theses and Dissertations by an authorized administrator of ScholarWorks@UARK. For more information, please contact [email protected]. SYSTEMATICS OF PROTOSTELOID AMOEBAE SYSTEMATICS OF PROTOSTELOID AMOEBAE A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Cell and Molecular Biology By Lora Lindley Shadwick Northeastern State University Bachelor of Science in Biology, 2003 December 2011 University of Arkansas ABSTRACT Because of their simple fruiting bodies consisting of one to a few spores atop a finely tapering stalk, protosteloid amoebae, previously called protostelids, were thought of as primitive members of the Eumycetozoa sensu Olive 1975. The studies presented here have precipitated a change in the way protosteloid amoebae are perceived in two ways: (1) by expanding their known habitat range and (2) by forcing us to think of them as amoebae that occasionally form fruiting bodies rather than as primitive fungus-like organisms. Prior to this work protosteloid amoebae were thought of as terrestrial organisms. Collection of substrates from aquatic habitats has shown that protosteloid and myxogastrian amoebae are easy to find in aquatic environments. Also, prior to this work the Eumycetozoa sensu Olive 1975, was a supposedly monophyletic taxon that included protosteloid amoebae as basal to Myxogastria and Dictyostelia. Three studies presented here erode this idea. These studies include a brief review of the diversity in nucleolar ultrastructure present among eumycetozoans in which new transmission electron micrographs of the protosteloid amoeba Echinosteliopsis oligospora are presented. Further, phylogenetic analyses of protosteloid amoebae based on the gene sequences of the small subunit of the ribosomal RNA (SSU rDNA) show that protosteloid amoebae are polyphyletic within the eukaryote supergroup, Amoebozoa, and that some are deeply embedded within well characterized lineages of nonfruiting amoebae, i.e., vannellids and acanthamoebids. As a result, we now call these simple, fruiting amoebae 'protosteloid amoebae' as opposed to 'protostelids' since the latter implies (incorrectly) that these organisms comprise a natural phylogenetic group. These molecular phylogenetic analyses suggest that isolate LHI05 represents a new protosteloid species that branches among the Acanthamoebidae, an amoebozoan taxon in which fruiting amoebae have never previously been described. Thus a new genus and species, Luapeleamoeba hula g. ad interim sp. ad interim, are proposed to accommodate protosteloid isolate LHI05. Suggestions for additional taxonomic revision are presented as are suggestions for future research particularly with respect to molecular phylogenetic, phylogenomic, and evolutionary/developmental biological approaches. Finally, this work has prompted critical thinking about the origins and evolution of simple fruiting bodies and complex life cycles among amoebozoans, and these basic biological questions are discussed. This dissertation is approved for recommendation to the Graduate Council Dissertation Directors: _______________________________________ Dr. Frederick W. Spiegel _______________________________________ Dr. Jeffrey D. Silberman Dissertation Committee: _______________________________________ Dr. Steven L. Stephenson _______________________________________ Dr. Ines Pinto _______________________________________ Dr. Allen L. Szalanski DISSERTATION DUPLICATION RELEASE I hereby authorize the University of Arkansas Libraries to duplicate this dissertation when needed for research and/or scholarship. Agreed __________________________________________ Lora Lindley Shadwick Refused __________________________________________ Lora Lindley Shadwick ACKNOWLEDGEMENTS I would like to thank my advisors Fred Spiegel and Jeff Silberman for exposing me to new ways of looking at the world and for encouraging me to continuously challenge old ways of thinking and long-held beliefs. I would like to thank Edward Haskins, George Ndiritu, Matt Brown, Maria Aguilar, and John Shadwick for lively and stimulating scientific discussions. I would like to thank Drs. Cynthia Sagers and Kathryn Curtin who provided not only scientific discussion but also encouragement, babysitting, and help with moving. I would like to thank my parents, whose love and support helped me get to graduate school in the first place and also my mother-in-law and father-in-law who provided support and encouragement during the final writing stages. Finally, I must thank my husband John Shadwick for the continuous, day-by-day love and support—the kind that keeps you going when you no longer feel like it. DEDICATION This is dedicated to all those who see the intrinsic beauty and importance of ALL organisms, especially those people who marvel at the tiny world that can be seen only through the lens of a microscope, and to my sons John Miles and Samuel Marshall. TABLE OF CONTENTS I. Chapter 1: Introduction 1 A. General background 1 B. Taxonomy 1 C. Life cycles 5 1. Definitions 5 2. Obligate amoebae 11 3. Flagellates 12 D. Evolutionary history 18 1. Molecular phylogenetics 18 E. Overview 19 F. Literature cited 24 II. Chapter 2: Protostelids and myxomycetes isolated from aquatic habitats 29 A. Introduction 29 B. Materials and methods 31 1. Substrates 31 2. Collection sites 31 3. Protostelid primary isolation plates 31 4. Myxomycete moist chambers 32 C. Results 32 D. Discussion 37 E. Acknowledgements 37 F. Literature cited 37 III. Chapter 3: Variations in nucleolar morphology in eumycetozoans 43 A. Introduction 44 B. Materials and methods 46 1. Cultures 46 2. Light microscopy 46 3. Transmission electron microscopy 47 C. Results 47 D. Discussion 48 1. Single, central nucleolus 49 2. Multiple peripheral nucleoli 49 3. Multiple peripheral vs. peripheral lobed Nucleoli 49 4. Central, diffuse nucleoli 50 5. Taxonomic Implications 50 E. Acknowledgements 51 F. Literature cited 51 IV. Chapter 4: Eumycetozoa = amoebozoa?: SSUrDNA phylogeny of protosteloid slime molds and Its significance for the amoebozoan supergroup 58 A. Introduction 59 B. Results 62 1. Hypothesis testing 65 C. Discussion 66 1. The protosteliid clade – Group I 67 2. The schizoplasmodiid clade – Group II 68 3. The soliformoviid clade – Group III 69 4. The cavosteliid clade – Group IV 69 5. The protosporangiid clade – Group Va 70 6. Groups VI & VII 70 7. Eumycetozoa question 72 D. Materials and Methods 74 1. Cultures 74 2. DNA extraction 75 3. PCR and DNA sequencing 76 4. Phylogenetic analyses 77 5. Hypotheses testing 79 E. Acknowledgements 80 F. Financial disclosure 80 G. References 80 H. Competing interests 87 I. Abbreviations 87 J. Supporting information disk V. Chapter 5: A New Amoeba with Ballistosporous Protosteloid Fruiting:Luapeleamoeba hula g. ad interim sp. ad interim 101 A. Introduction 103 B. Materials and methods 103 1. Collections 103 2. Primary isolation plates 104 3. Mono-eukaryotic culture 104 4. Strains examined 104 5. Light microscopy 104 6. Fixation 104 C. Results 105 D. Discussion 108 1. Generic diagnosis 111 a. Etymology 111 b. Type species 112 2. Species Diagnosis 112 a. Etymology 113 b. Type locality 113 c. Prevalence 113 d. Ecology/Habitat 113 e. Specimens examined 113 f. Deposition of type specimens 113 E. Acknowledgements 113 F. Literature cited 114 VI. Chapter 6: Overall Conclusion 119 A. Recapitulation of conclusions 119 B. Change in perception: from protostelids to protosteloid amoebae 120 C. Current state of research 120 1. Chapter 2 120 2. Chapter 3 122 3. Chapter 4 122 D. Future work 131 1. Taxonomic revisions 131 2. Expanding molecular phylogenies 139 E. Biological questions 143 1. Fruiting bodies 144 2. Flagellates 148 3. Complex life cycles 153 F. Concluding remarks 163 G. Literature cited 164 H. Appendix disk LIST OF PUBLISHED PAPERS Lindley LA, Stephenson SL, Spiegel FW (2007) Protostelids and myxomycetes isolated from aquatic habitats. Mycologia 99(4): 504-509. Lindley LA, Edwards SM, Spiegel FW (2006) Variations in nucleolar morphology in eumycetozoans. Revista Mexicana de Micologia 23: 75-81. Shadwick LL, Spiegel FW, Shadwick JDL, Brown MW, Silberman JD (2009) Eumycetozoa = amoebozoa?: SSUrDNA phylogeny of protosteloid slime molds and its significance for the amoebozoan supergroup. PLoS ONE 4(8): e6754. doi:10.1371/journal.pone.0006754 CHAPTER 1 INTRODUCTION GENERAL BACKGROUND Protosteloid amoebae, formerly called protostelids, are amoebae that make small, simple fruiting bodies. A protosteloid fruiting body consists of an acellular stalk and a spore, though in some species there are up to eight spores per stalk. Protosteloid amoebae had been classified as a paraphyletic assemblage of slime molds in the class Eumycetozoa (Olive 1975). Olive considered protosteloid amoebae to be primitive eumycetozoans (Olive 1967, Olive 1970, Olive 1975, Olive and Stoianovitch 1976). In fact, it was the accidental discovery
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