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Polyphasic Approach to the Taxonomy of Selected Cyanobacteria Rndr. Jan Mareš

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Polyphasic Approach to the Taxonomy of Selected Cyanobacteria Rndr. Jan Mareš School of Doctoral Studies in Biological Sciences University of South Bohemia in České Bud ějovice Faculty of Science Polyphasic approach to the taxonomy of selected cyanobacteria Ph.D. Thesis RNDr. Jan Mareš Supervisor: Doc. RNDr. Jan Kaštovský, Ph.D. Faculty of Science, University of South Bohemia in České Bud ějovice, Czech Republic České Bud ějovice, 2015 This thesis should be cited as: Mareš J (2015) Polyphasic approach to the taxonomy of selected cyanobacteria. Ph.D. Thesis. University of South Bohemia, Faculty of Science, School of Doctoral Studies in Biological Sciences, České Bud ějovice, Czech Republic, 109 pp. ANNOTATION The modern taxonomic revision of cyanobacteria is a work in progress, with both theoretical and practical challenges to be addressed. This thesis investigated selected terrestrial cyanobacterial taxa using a polyphasic approach, based on molecular phylogenetic analysis and accompanied by phenotypic characterization and nomenclatural treatment. Diverse methodological approaches were used including optical and transmission electron microscopy, molecular analysis (DNA sequencing) of cyanobacterial strains, single cells and filaments, and phylogenetic analysis of multiple genomic loci. This study provided systematic revisions of individual cyanobacterial genera and the entire phylum, and suggestions for future study projects. DECLARATION [IN CZECH] Prohlašuji, že svoji diserta ční práci jsem vypracoval samostatn ě pouze s použitím pramen ů a literatury uvedených v seznamu citované literatury. Prohlašuji, že v souladu s § 47b zákona č. 111/1998 Sb. v platném zn ění souhlasím se zve řejn ěním své diserta ční práce, a to v úprav ě vzniklé vypušt ěním vyzna čených částí archivovaných P řírodov ědeckou fakultou elektronickou cestou ve ve řejn ě p řístupné části databáze STAG provozované Jiho českou univerzitou v Českých Bud ějovicích na jejích internetových stránkách, a to se zachováním mého autorského práva k odevzdanému textu této kvalifika ční práce. Souhlasím dále s tím, aby toutéž elektronickou cestou byly v souladu s uvedeným ustanovením zákona č. 111/1998 Sb. zve řejn ěny posudky školitele a oponent ů práce i záznam o pr ůběhu a výsledku obhajoby kvalifika ční práce. Rovn ěž souhlasím s porovnáním textu mé kvalifika ční práce s databází kvalifika čních prací Theses.cz provozovanou Národním registrem vysokoškolských kvalifika čních prací a systémem na odhalování plagiát ů. České Bud ějovice, 16. 2. 2015 ............................................ Jan Mareš This thesis originated from a partnership of Faculty of Science, University of South Bohemia, and Institute of Botany, Czech Academy of Sciences, supporting doctoral studies in the Botany study programme. FINANCIAL SUPPORT The research present in this thesis was financially supported by Czech Science Foundation grant No. P506/12/1818, MŠMT/AMVIS project LH12100, Grant Agency of the University of South Bohemia project GAJU 135/2010/P, Center for Algal Biotechnology T řebo ň – ALGATECH (CZ. 1.05/21.00/03.0110), FRS-FNRS of Belgium, by a short-term research fellowship for foreign doctoral students at the University of Liège, Belgium, and by the long- term research development project of the Institute of Botany CAS (RVO 67985939). ACKNOWLEDGEMENTS It is a great pleasure for me to express my gratitude to all who helped me enjoying and finishing my studies. I am especially grateful to my mentors in cyanobacterial taxonomy – Ji ří Komárek, Jan „Hanys“ Kaštovský, and Jeff Johansen – for their proffessional advice and much more. I sincerely appreciate the contribution of all my colleagues and friends, especially Pavel Hrouzek, Tomáš Hauer, Markéta Bohunická, and Ota Strunecký, and all my kind co- authors (Yannick Lara, Ifka Dadáková, Annick Wilmotte, Stefano Ventura, Aharon Oren, Pierre Compère, Radek Ka ňa, and Bohuš Uher). My greatest thanks belong to my family and to all whom I love. LIST OF PAPERS AND AUTHOR´S CONTRIBUTIONS I. Mareš J. , Hrouzek P., Ka ňa R., Ventura S., Strunecký O. & Komárek J. (2013). The primitive thylakoid-less cyanobacterium Gloeobacter is a common rock-dwelling organism. PloS ONE 8: e66323. (IF=3.53) Jan Mareš performed isolation and cultivation of strains, analyses of morphology and ultrastructure, molecular analyses, participated in phylogenetic analyses, and was responsible for preparation of the manuscript. II. Mareš J. , Komárek J., Compère P. & Oren A. (2013). Validation of the generic name Gloeobacter Rippka et al. 1974, Cyanophyceae. Cryptogamie Algologie 34: 255-262. (IF=0.67) Jan Mareš conducted the taxonomic investigation and participated in preparation of the manuscript. III. Mareš J. , Komárek J., Compère P. & Oren A. (2013). (2194) Proposal to conserve the name Gloeobacter violaceus against Aphanothece caldariorum , Gloeothece coerulea , and Gloeothece linearis (Cyanophyceae). Taxon 62:1055. (IF=3.05) Jan Mareš conducted the taxonomic and nomenclatural investigation and participated in preparation of the manuscript. IV. Mareš J. , Hauer T., Komárek J. & Compère P. (2013). (2195) Proposal to conserve the name Gloeothece (Cyanophyceae) with a conserved type. Taxon 62:1056. (IF=3.05) Jan Mareš conducted the taxonomic and nomenclatural investigation and participated in preparation of the manuscript. V. Mareš J. , Lara Y., Dadáková I., Hauer T., Uher B., Wilmotte A. & Kaštovský J. (2015). Phylogenetic analysis of cultivation-resistant terrestrial cyanobacteria with massive sheaths (Stigonema spp. and Petalonema alatum , Nostocales, Cyanobacteria) using single-cell and filament sequencing of environmental samples. Journal of Phycology 51: published online. DOI: 10.1111/jpy.12273 (IF=2.53) Jan Mareš organized the study, participated in experimental design, isolation of the material, molecular and phylogenetic analyses, and prepared the manuscript for publication. VI. Komárek J., Kaštovský J., Mareš J. & Johansen J. R. (2014). Taxonomic classification of cyanoprokaryotes (cyanobacterial genera) 2014, using a polyphasic approach. Preslia 86:295- 335. (IF=2.78) Jan Mareš performed phylogenetic analyses, created all figures, and participated in writing the manuscript. CONTENTS CHAPTER I. GENERAL INTRODUCTION ........................................................................... 1 CHAPTER II. .......................................................................................................................... 20 The primitive thylakoid-less cyanobacterium Gloeobacter is a common rock-dwelling organism CHAPTER III. ......................................................................................................................... 34 Validation of the generic name Gloeobacter Rippka et al. 1974, Cyanophyceae (2194) Proposal to conserve the name Gloeobacter violaceus against Aphanothece caldariorum , Gloeothece coerulea , and Gloeothece linearis (Cyanophyceae) (2195) Proposal to conserve the name Gloeothece (Cyanophyceae) with a conserved type CHAPTER IV. ........................................................................................................................ 49 Phylogenetic analysis of cultivation-resistant terrestrial cyanobacteria with massive sheaths ( Stigonema spp. and Petalonema alatum , Nostocales, Cyanobacteria) using single-cell and filament sequencing of environmental samples CHAPTER V. .......................................................................................................................... 62 Taxonomic classification of cyanoprokaryotes (cyanobacterial genera) 2014, using a polyphasic approach CHAPTER VI. SUMMARY OF THE RESULTS ................................................................. 106 CHAPTER I. GENERAL INTRODUCTION Cyanobacteria represent the most abundant and most important phylum of photosynthetic prokaryotes on Earth. They inhabit almost all imaginable aquatic and terrestrial habitats, in which they frequently perform crucial ecological services (Whitton 2012). The significance of cyanobacteria in the global biosphere largely follows from their extremely long evolutionary history (Cavalier-Smith 2006). Their continuous presence and biological activity on Earth has probably lasted since approximately 3 billion years BP. In the course of this long period, they have been involved in the origins of the oxygen-rich atmosphere during the „Great Oxidation Event“ (Planavsky et al. 2014, Schopf 2014, Schirrmeister 2013), and in formation of a great portion of biogenous calcium carbonates (stromatolites, travertines) (Altermann et al. 2006, Riding 2000). The extensive evolutionary radiation and ecological success of cyanobacteria has been driven by an impressive set of metabolic skills. These include photosynthesis via chlorophyll a with both photosystems typical for plants (Bjorn and Govindjee 2009), fixation of the atmospheric nitrogen (Thompson and Zehr 2013, Flores and Herrero 2010, Berman- Frank et al. 2003), and production of a tremendous variety of secondary metabolites (Dittmann et al. 2013, Leflaive and Ten-Hage 2007). Cyanobacteria as free-living microorganisms hold substantial importance in a wide spectrum of aquatic communities such as ocean picoplankton (Flombaum et al. 2013), plankton of lakes and reservoirs (Komárek and Mareš 2012, Komárek 2003, Lyra et al. 2001), and benthos or periphyton of shallow waters and marshlands (Vargas and Novelo 2007, Rejmánková et al. 2004). The planktonic types are frequently capable of forming excessive accummulations of biomass in eutrophic water bodies (O´Neil et al. 2012, Yamamoto et al. 2009, Jozwiak et al. 2008),
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