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FERTIG Diplomarbeit 2 12 10 Beate Übelleitner Morphological and genetic analysis of moss-dwelling tardigrades Masterarbeit zur Erlangung des akademischen Grades einer Magistra an der Naturwissenschaftlichen Fakultät der Karl-Franzens-Universität Graz Associate Professor Dr. Steven Weiss Institut für Zoologie 2010 1 Thanks, to Steven Weiss and Kathrin Winkler for their supervision and help and Theodora Kopun, Adriana Atanassova and Maria Unterberger for their time. I would also like to thank my family and friends for their support. 2 Deutsche Zusammenfassung/German Summary Tardigraden sind mikroskopisch kleine Invertebraten, die marine und terrestrische Ökosysteme, sowie Süßwasser-Ökosysteme bewohnen und auf einen Wasserfilm um ihren Körper angewiesen sind um zu leben. Das Phylum Tardigrada besteht aus zwei Klassen: Heterotardigrada und Eutardigrada. Von verschiedenen Habitaten in der Steiermark wurden Moosproben genommen und nach Tardigraden untersucht. Aus einigen Proben wurden Dauerpräparate hergestellt, andere wurden für die genetische Analyse verwendet, wobei die mtDNA COI Region analysiert wurde. Insgesamt wurden 104 Tardigraden, 92 Eutardigraden und 12 Heterotardigraden, anhand von morphologischen Merkmalen bestimmt. Fast alle Präparate ( N = 103) wurden auf Gattungsniveau zugeordnet, 59 Individuen konnten einer von sechs Arten zugeordnet werden. Zusätzlich konnten vier weitere Arten mit Hilfe von mtDNA Sequenzen (COI Gen) bestimmt werden. Die erlangten Sequenzen wurden mit 55 Sequenzen aus der GenBank vervollständigt und einer phylogenetischen Analyse unterzogen, welche die Monophylie von Heterotardigraden und Eutardigraden zeigte. Einzelne Sequenzen von vermeintlichen Echiniscus blumi , Macrobiotus richersi und Richtersius coronifer erschienen in entfernten Positionen innerhalb des Stammbaumes. Die P-distances einzelner Exemplare dieser Taxa umfassten Werte von unter einem halben Prozent bis über 22%. Solch große Distanzen wären atypisch für intraspezifische Diversität. Aus unserer phylogenetischen Rekonstruktion aus verfügbaren GenBank Sequenzen geht hervor, dass die systematische und taxonomische Zuordnung von Tardigraden einer umfangreichen Überarbeitung bedarf. 3 Abstract Tardigrades, or water bears, are considered a phylum subdivided in two classes: Heterotardigrada and Eutardigrada. These microscopic invertebrates depend on water to maintain an active life and they inhabit marine, freshwater and terrestrial ecosystems. Moss samples were collected from various habitats in Styria and searched for tardigrades. Permanent slides were made of some samples whereby others were used for genetic analysis of the cytochrome subunit I (COI) mtDNA gene. A total of 104 tardigrades, 92 Eutardigrada and 12 Heterotardigrada, were identified on the basis of morphological characteristics. Nearly all preparations ( N = 103) could be assigned to the genus level, whereby 59 individuals were assigned to one of six species. An additional four species were determined with the aid of an mtDNA sequence (COI gene). The obtained sequences were aligned with 55 sequences downloaded from GenBank. A phylogenetic analysis based upon Bayesian inference showed the monophyly of both Heterotardigrades and Eutardigrades. Individual sequences of putative Echiniscus blumi , Macrobiotus richtersi and Richtersius coronifer appear in distant positions of the tree. The pairwise distances (p-distances) among individual specimens assigned to these taxa display a wide range of distances from less than a half of percent to over 22%. Such high distances would be highly atypical for intraspecfic diversity, therefore it is clear that based on our own phylogenetic reconstruction of available GenBank sequences the current systematic and taxonomic assignment of tardigrades requires substantial revision. 4 TABLE OF CONTENTS 1 INTRODUCTION .............................................................................................................. 7 1.1 Systematic and morphology of Tardigrades ................................................................ 7 1.2 The distribution of Tardigrades ................................................................................. 10 1.3 Cryptobiosis ............................................................................................................... 12 1.3.1 Anhydrobiosis .................................................................................................... 12 1.3.2 Cryobiosis ........................................................................................................... 13 1.3.3 Encystment ......................................................................................................... 13 1.4 Identification of tardigrades ....................................................................................... 13 2 MATERIAL AND METHODS ....................................................................................... 15 2.1 Sampling .................................................................................................................... 15 2.1.1 Moss identification ............................................................................................. 17 2.1.2 Preparation of permanent slides ......................................................................... 17 2.1.3 Taking photos of the permanent slides for further determination ...................... 17 2.1.4 Identification ...................................................................................................... 18 2.2 DNA extraction .......................................................................................................... 19 2.2.1 PCR - Polymerase chain reaction ....................................................................... 19 2.2.2 Gel electrophoresis ............................................................................................. 20 2.2.3 PCR product purification ................................................................................... 20 2.2.4 DNA Sequencing ............................................................................................... 20 2.2.5 Data Analysis ..................................................................................................... 21 2.2.6 MrBayes ............................................................................................................. 21 3 RESULTS ......................................................................................................................... 22 3.1 Morphological identification ..................................................................................... 22 3.2 Molecular identification ............................................................................................ 39 5 4 DISCUSSION .................................................................................................................. 45 5 REFERENCES ................................................................................................................. 49 6 APPENDIX ...................................................................................................................... 55 6 Introduction 1 INTRODUCTION 1.1 Systematic and morphology of Tardigrades Tardigrades, or water bears, are microscopic invertebrates closely related to arthropods and onychophorans (Garey et al., 1996; Giribet et al., 1996; Mallatt et al., 2004). In 1773, the German parish priest J.A.E. Goeze was the first to write about the "kleiner WasserBär" (little water bear). The name tardigrade has been used since the 18th century; it means slow walker (tardi = slow, grade = walker) and describes the animals lumbering gait. At the end of the 19th century only 25 tardigrada species were known (Greven, 1980). Over the last few decades the number of newly described tardigrades has increased to more than 940 (Guidetti and Bertolani, 2005). Today there are two classes, four orders, 21 families and 104 genera known (Guidetti et. al, 2009). The phylum tardigrada comprises two main classes: Heterotardigrada and Eutardigrada. Heterotardigrada are subdivided in two orders: Arthotardigrada and Echiniscoidea, while Eutardigrada are subdivided in Apochela and Parachela (Guidetti and Bertolani, 2005). The armored tardigrades, or Heterotardigrades, have morphological characteristics such as cephalic appendages, cuticular extensions, claws and the pattern of dorsal cuticular plates, whereas the main characteristics of the naked tardigrades (Eutardigrade) are claws, the buccopharyngeal apparatus and a cuticle structure, which can be smooth, granulated or bearing tubercles. The phrase "naked" refers to the absence of cuticular dorsal plates, which are present in Heterotardigrada (Romano, 2003). Different species of tardigrades from the two classes are shown in Figure 1. 7 Introduction Figure 1: Different tardigrades. a) Tanarctus velatus (Heterotardigrada, about 120 µm), b) Stygarctus abornatus (Heterotardigrada, about 95 µm), c) Echiniscus trisetosus (Heterotardigrada, about 375 µm), d) Hypsibius oberhaeuseri (Eutardigrada, about 500 µm), e) Milnesium tardigradum (Eutardigrada, about 600 µm). The measurements represent the average length of the particular species. a,b after McKirdy et al. 1976; c,d,e after Marcus 1936. 8 Introduction Tardigrades range in size from less than 100 µm to 500 µm and they depend on water to permit gas exchange and locomotion to maintain an active life (Kinchin, 1994). Their bilaterally symmetrical body has four pairs of lobopodous legs and is separated into five segments: a first cephalic segment
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