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Cryptic Diversity of Cyanobacteria CRYPTIC DIVERSITY OF CYANOBACTERIA DOCTORAL THESIS FOR A DOCTORAL DEGREE Department of Botany Faculty of Science, Palacký University Olomouc Author MGR. EVA JAHODÁŘOVÁ Supervisor DOC. RNDR. PETR HAŠLER, PH.D. Olomouc 2019 © Eva Jahodářová, Palacký University Olomouc, 2019 You can't even begin to understand biology, you can't understand life, unless you understand what it's all there for, how it arose-and that means evolution. Richard Dawkins ACKNOWLEDGMENTS I owe many thanks to colleagues, advisors, friends, and family: PETR HAŠLER, PETR DVOŘÁK and ALOISIE POULÍČKOVÁ for accepting me into Algological laboratory and taking care of me during my study. I would also like to express my greeting for the opportunity to undertake my doctoral studies with their advice, feedback, inspiration, support, guidance, and total assistance. MATĚJ BOČEK, MARKÉTA LETÁKOVÁ, LUCIE KOBRLOVÁ, MICHAL HRONEŠ, JANA RŮŽIČKOVÁ, MICHAELA ŠVÉCAROVÁ, IVETA HRADILOVÁ, and other members of the botanical and zoological department for their help, advice and support. Foundation NADÁNÍ JOSEFA, MARIE A ZDEŇKY HLÁVKOVÝCH for its financial support during my internship in the Natural History Museum, London. My dear family and my boyfriend MICHAL MOTYKA for everything! DECLARATION I declare that this Ph.D. thesis has been written solely by myself. All the sources quoted in this work are listed in the Reference section. All published results included in this thesis have been approved with the help of mentioned co-authors. In Olomouc 15.5.2019 Mgr. Eva Jahodářová ABSTRACT Cyanobacteria emerged on Earth approximately 3.5 billion years ago. They are the major contributor to global biogeochemical cycles and are ancestors of today's chloroplast of higher plants. Cyanobacteria thrive across many habitats. However, due to their enormous diversity, taxonomy remains in chaos and most taxa are uncharacterised. In this thesis, I have investigated the morphological and molecular features of three new cyanobacterial genera from tropical areas (Pinocchia, Onodrimia, and Elainella). Moreover, I aimed to identify gaps in cyanobacterial systematics and cooperated on a book chapter focused on cyanobacterial diversity. Recent investigations revealed that Leptolyngbya and Pseudanabaena are extensively polyphyletic cyanobacterial taxa. Both species-rich genera have very simple morphology, create thin filaments and occur mostly in aquatic and terrestrial habitats. However, due to polyphyly, Leptolyngbya was divided into several genera such as Oculatella and Nodosilinea. Pseudanabaena still waits for its revision. I identified two unknown genera similar to Leptolyngbya and Pseudanabaena. They were named Onodrimia and Pinocchia. Both of them are simple filamentous cyanobacteria with tropical origin. The phylogenetic study of 16S rRNA clearly distinguished Pinocchia and Onodrimia as monophyletic clades distant from Pseudanabaena and Leptolygbya sensu stricto. I endeavoured to find the unique apomorphic character which would strictly define newly described genera. Pinocchia is a cryptic genus but some trichomes possess prolongated, pointed and sometimes conical apical cell. For confirmation of this morphological apomorphy, I applied nutrient experiment. The results did not show any significant difference between standard and experimental cultures. On the other hand, Onodrimia possess a peculiar type of reproduction (it reproduces by tree-like hormogonia tufts). This character could be considered as apomorphy. Another new tropical cyanobacterium Elainella is morphologically very similar to Pseudophormidium. Pseudophormidium is poorly studied lineage, with unclear morphology. For confirmation of this new genus, I used 16S rRNA phylogeny, morphological data and also whole genome assessment. The total length of the draft genome was 8 702 141 bp. Elainella genome contains genes for atmospheric nitrogen fixation and also 10 potentially biosynthetic genes clusters, but only 2 were assigned as already known genes with the ability to produced cytotoxic metabolites. A dated phylogeny of 69 orthologous genes revealed the origin of Elainella and its sister's clade Leptolyngbya sp. JSC-1. They diverged probably 2.24–2.47 BYA. Gene for the small subunit of the prokaryotic ribosome (16S rRNA) is a widely used marker for bacterial phylogeny. There are hundreds of thousands of sequences of this gene in molecular databases. But it is widely known that morphological characters do not perfectly correspond with molecular phylogeny. Therefore, I wanted to describe this evident paradox of increasing data yet poor phylogenetic resolutions by PTP (Poisson Tree Process) algorithm. I aligned 10037 sequences of 16S rRNA and I used PTP delimitation to a defined quantity of species in GenBank database. PTP identified just 2741 PTP-defined species, but 51% PTP-defined species were assigned to uncultured samples. I also proposed possible suggestions which could improve this difficult situation. ABSTRAKT Sinice (Cyanobacteria) se na Zemi poprvé objevily asi před 3,5 miliardami let. Patří mezi hlavní organismy ovlivňující světové biogeochemické cykly a jsou prapředky chloroplastů dnešních vyšších rostlin. Sinice jsou schopny přežít v nejrůznějších prostředích. Díky jejich obrovské rozmanitosti zůstává velká většina taxonů systematicky nezařazena. V této práci jsem studovala morfologické i molekulární znaky tří nových rodů sinic z tropických oblastí (Pinocchia, Onodrimia a Elainella), také jsem se zaměřila na mezery v systematice sinic. Spolupracovala jsem na knižní kapitole pojednávající o diverzitě cyanobakterií. Recentní studie odhalily, že rody jako je Leptolyngbya nebo Pseudanabaena jsou výrazně polyfyletické. Oba druhově bohaté rody se značí jednoduchou morfologií, vytvářejí tenká vlákna a obývají jak vodní, tak i terestrické habitaty. Nicméně, na základě polyfyletického původu byla Leptolyngbya rozdělena do několika nových linií, jako je Oculatella nebo Nodosilinea. Pseudanabaena na svou revizi stále čeká. Podobně jsem i já popsala dva neznámé rody odvozené z rodů Leptolyngbya a Pseudanabaena. Pinocchia a Onodrimia jsou jednoduché vláknité cyanobakterie tropického původu. Fylogeneze založená na genu 16S rRNA jednoznačně odlišila monofyletické linie rodu Pinocchia a Onodrimia od Pseudanabaena a Leptolyngbya sensu stricto. Snažila jsem se najít morfologickou apomorfii, která by striktně definovala nově popsané rody. V případě rodu Pinocchia se jedná pravděpodobně o kryptický rod, avšak některé z trichomů měly výrazně prodlouženou, špičatou, někdy kuželovitou apikální buňku. Pro ověření, zda se skutečně jedná o apomorfii, jsem použila nutriční experiment. Nebyl však nalezen signifikantní rozdíl, který by odlišoval kontrolní a experimentální kulturu. Na druhou stranu, Onodrimia je charakteristická zvláštním typem reprodukce (produkuje hormogonia v takzvaných stromečkovitých formacích). Tento charakteristický znak lez považovat za apomorfii. Další nově popsaná tropická sinice Elainella je velice podobná sinici rodu Pseudophormidium. Pseudophormidium je málo prostudovaný taxon s nejasnou morfologií. Pro definici tohoto nového rodu jsem použila jak fylogenezi na základě 16S rRNA genu a morfologické informace, tak i celo-genomový přístup. Celková délka genomu byla 8 702 141 párů bází. V genomu rodu Elainella jsem identifikovala geny sloužící k fixaci vzdušného dusíku a deset potencionálně biosyntetických genových klastrů, pouze dva z nich zřejmě produkující cytotoxické metabolity. Z datované fylogeneze na základě 69 ortologních genů jsme se pokusila odhalit vznik rodu Elainella a kmene Leptolyngbya sp. JSC-1. Tento klád se pravděpodobně diversifikoval asi před 2,24– 2,47 miliardami let. Gen kódující malou podjednotku ribozomu (16S rRNA gen) je hojně užívaný marker pro fylogenezi bakterií. V databázích můžeme najít tisíce sekvencí tohoto genu. Na druhou stranu, je obecně známo, že morfologická charakteristika neodpovídá molekulární fylogenezi. Proto jsem chtěla tento zjevný paradox, neustále se zvětšujícího množství dat a nesprávného fylogenetického určení, prostudovat pomocí algoritmu PTP (Poisson Tree Process). Alignovala jsem 10 037 sekvencí genu 16S rRNA a pomocí PTP algoritmu jsem delimitovala počet druhů sinic v databázi GenBank. PTP identifikovalo pouze 2741 PTP- definovaných druhů, avšak 51 % PTP-druhů bylo nekultivovatelných. Také jsem se zaměřila na faktory, které by mohly tuto nelehkou situaci taxonomie sinic zlepšit (např. nově popsané taxony by měly být vždy charakterizovány autapomorfií, metagenomická data by měla být vyhodnocována pečlivěji, revize by měly být prováděny pouze s robustním a správným výběrem taxonů). CONTENTS 1. GENERAL INTRODUCTION 1 1.1. TAXONOMY 2 1.2. MOLECULAR MARKERS USED IN CYANOBACTERIAL TAXONOMY 4 1.3. BACTERIAL GENOME 5 1.4. HORIZONTAL GENE TRANSFER AND HOMOLOGOUS RECOMBINATION 6 1.5. PROBLEMATIC GENERA IN THIS STUDY 8 1.5.1. Pseudanabaena Lauterborn 1915 8 1.5.2. Leptolyngbya Anagsnotidis & Komárek 1988 8 1.5.3. Pseudophormidium (Forti) Anagnostidis & Komárek 1988 9 2. AIMS 11 2.1. SPECIFIC AIMS 11 3. MATERIAL AND METHODS 13 3.1. TAXONOMICAL PART 13 3.2. GENOMIC PART 14 3.3. GAPS IN CYANOBACTERIAL TAXONOMY 17 4. CONCLUSIONS 19 4.1. BOOK CHAPTER 19 4.1.1. DIVERSITY OF THE CYANOBACTERIA 19 4.2. INDIVIDUAL PAPERS 20 4.2.1. Polyphasic characterization of Pinocchia gen. and sp. nov. 20 4.2.2. Polyphasic characterization of Onodrimia gen. and sp. nov. 21 4.2.3. The complex genomic approach in a description of Elainella 22 4.2.4. Difference without distinction? Gaps in cyanobacterial systematics
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