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Nivicolousmyxomycetes EXPLORING THE DIVERSITY OF N I V I C O L O U S M Y X O M Y C E T E S: An analysis of the genetic diversity, species distribution and community composition I N A U G U R A L D I S S E R T A T I O N Zur Erlangung des akademischen Grades eines Doctor rerum naturalium (Dr. rer. nat.) an der Mathematisch-Naturwissenschaftlichen Fakultät der Universität Greifswald vorgelegt von: Mathilde Borg Dahl Greifswald, 30. Januar 2018 Dekan: Prof. Dr. Werner Weitschies 1. Gutachter: Prof. Dr. Martin Schnittler 2. Gutachter: Ass. Prof. Regin Rønn 3. Gutachter: Prof. Carsten Suhr Jacobsen Tag der Promotion: 1. Oktober 2018 PREFACE This cumulative dissertation is a product of my just under three years enrolment in the graduate school RESPONSE (GRK 2010) under the supervision of Prof. Dr. Martin Schnittler. In these years I have conducted fieldwork (including seven trips to the German Alps and a journey to the Rocky Mountains) to collect nivicolous myxomycetes and soil. I have done numerous (~700) DNA extractions and obtained sequences of the collected specimens (Greifswald, DE) as well as an Illumina library (3x 48 samples) of myxamoebae, fungi and bacteria (Copenhagen, DK). In addition I have participated in international conferences in the Czech Republic (Ecology of Soil Microorganisms, 2015), Germany (3rd Thünen Symposium on Soil Metagenomics, 2016) and Canada (The ISME conference, 2016). All of the information presented henceforth was obtained from my original independent work with collaborations with experts from around the world. I was fortunate to work with Prof. Søren J. Sørensen (University of Copenhagen, Denmark) and his lab who specialize in molecular techniques and Illumina sequencing. I also had the pleasure of visiting the laboratory of Prof. Steven K. Schmidt (University of Boulder, Colorado, USA), whose working group specializes in under-snow microbial communities. Finally my study benefitted from the collaboration with Prof. Yuri K. Novozhilov (Komarov Botanical Institute, St. Petersburg, Russia) an expert among myxomycetes taxonomist. After the abstract in Chapter 1 and a general introduction in Chapter 2, four manuscripts (on three of which I am first author) are presented in Chapter 3. Chapter 3.1 aims at establishing species delimitation of dark-spored myxomycetes by the use of a genetic marker (SSU; small subunit ribosomal RNA) and the complications in doing so are discussed. Chapter 3.2 reviews the state-of-the-art barcoding methods for myxomycetes and their potential as well as challenges and limitations are discussed. Chapter 3.3 presents an ecological study of the distribution of dark-spored myxamoebae along a natural altitudinal gradient; demonstrating fine scale niche differentiation as well as taxa specific interactions with bacteria. Finally, Chapter 3.4 presents a comparative study between the distribution of soil myxamoebae and a quantitative fructification collection from a natural altitudinal gradient in the German Alps, as well as a year to year comparison in fructification success in relation to climatic conditions. Chapter 4 summarizes the important findings of this dissertation and highlights its significant contributions to the current knowledge on 1) barcoding and 2) niche differentiation among myxamoebae in natural habitats of dark-spored myxomycetes. i LIST OF PUBLICATIONS INCLUDED IN THIS DISSERTATION ACCEPTED IN PEER REVIEWED JOURNALS Borg Dahl M, Brejnrod A, Unterseher M, Hoppe T, Feng Y, Novozhilov YK, Sørensen SJ and Schnittler M (2017) Genetic barcoding of dark-spored myxomycetes (Amoebozoa) – identification, evaluation and application of an identification threshold for species differentiation in NGS studies. Molecular Ecology Resources 1–13. doi: 10.1111/1755- 0998.12725. Schnittler M, Shchepin O, Dagamac N, Borg Dahl M and Novozhilov YK (2017). Barcoding myxomycetes with molecular markers: challenges and opportunities. Nova Hedwigia 104:23– 341. doi: 10.1127/nova_hedwigia/2017/0397. MANUSCRIPTS SUBMITTED FOR PEER REVIEW Borg Dahl M, Brejnrod A, Russel J, Sørensen SJ and Schnittler M (2017) Fine scale niche differentiation among amoebal communities of dark-spored myxomycetes determined by landscape structures as well as biotic factors. Environmental Microbiology (Submitted 30.12.2017). Borg Dahl M, Shchepin O, Schunk C, Menzel A, Novozhilov YK and Schnittler M (2017) Distribution patterns between fruit bodies and soil amoebae of nivicolous myxomycetes. Ecology (Submitted 26.01.2018). ii CONTENT Preface .................................................................................................................................................. i Manuscripts submitted for peer review ............................................................................................. ii Contents ............................................................................................................................................... iii 1 Abstract .......................................................................................................................................... 1 1.1 Deutsch ................................................................................................................................................................ 1 1.2 English ................................................................................................................................................................... 2 2 General introduction ..................................................................................................................... 5 2.1 Background .......................................................................................................................................................... 6 2.2 Field work ........................................................................................................................................................... 9 2.3 Conceptual framework of RESPONSE ....................................................................................................... 12 2.4 Objectives of the thesis .................................................................................................................................. 13 2.5 Literature ............................................................................................................................................................ 14 3 Publications .................................................................................................................................... 19 3.1 Genetic barcoding of dark-spored myxomycetes (Amoebozoa) – identification, evaluation and application of an identification threshold for species differentiation in NGS studies ................................ 20 3.2 Barcoding myxomycetes with molecular markers: challenges and opportunities ............................ 43 3.3 Fine scale niche differentiation among amoebal communities of dark-spored myxomycetes determined by landscape structures as well as biotic factors .......................................................................... 67 3.4 Distribution patterns between fruit bodies and soil amoebae of nivicolous myxomycetes .......... 91 4 Conclusions and perspectives ....................................................................................................... 108 4.1 Main findings ...................................................................................................................................................... 108 4.2 Challenges and limitations .............................................................................................................................. 109 4.3 Citations .............................................................................................................................................................. 109 5 Affidavits......................................................................................................................................... 110 5.1 Selbstständigkeitserklärung / Declaration .................................................................................................. 110 5.2 Erklärung bei Gemeinschaftsarbeiten (Eigenanteil)/ Declaration for thesis works with joint publication (own contribution) ................................................................................................................................ 111 5.3 Erklärung zur Abgabe einer elektronischen Kopie der Dissertation Declaration on the submission of an electronic copy of the PhD thesis ................................................................................................................ 113 6 Acknowledgement ......................................................................................................................... 114 iii 1 ABSTRACT 1.1 DEUTSCH Myxomyceten sind Protisten, die der Großgruppe der Amöben (Amoebozoa) zugerechnet werden. Nach dem traditionellen, inzwischen durch molekulare Phylogenien überholten, System werden sie in fünf Ordnungen gegliedert: Liceales, Trichiales, Physarales, Stemonitales und Echinosteliales. Molekulare Phylogenien zeigen jedoch zwei basale Gruppen: Physarales und Stemonitales (die sogenannten dunkelsportigen Myxomyceten) als eine und die anderen genannten Ordnungen (die hellsporigen Myxomyceten) als zweite. Außer den Echinosteliales ist jedoch keine der Ordnungen monophyletisch; sie müssen neu gefasst werden. Die dunkelsporigen Myxomyceten umfassen die Mehrzahl der beschriebenen Morphospezies. Aufgrund der hohen genetischen
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