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The Root of the Dictyostelid Tree

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The Root of the Dictyostelid Tree GROUP 4 GROUP 4 GROUP 3 GROUP 3 GROUP 2 GROUP 2 GROUP 1 GROUP 1 GROUP 4 GROUP 4 GROUP 3 GROUP 3 GROUP 2: P + D GROUP 1 GROUP 2: A GROUP 2 ?GROUP 1 Cover illustration by Stina Weststrand. Abstract The root represents the oldest point in a phylogeny, and determining it gives evolution a time arrow. The first molecular treatment of the social amoebae (Dictyostelia) was carried out with small subunit ribosomal DNA (SSU rDNA) data in 2006, and from this four major dictyostelid groups were defined. However, the relationships among them, i.e. the root of the tree, could not be confidently determined. In this study, a ‘new’ protein data set – eukaryotic release factor 3 (eRF3) – was developed for deep dictyostelid phylogeny. This included the work with designing degenerate PCR primers, developing PCR strategies and assembling currently available dictyostelid data sets. Phylogenetic reconstructions show substantial support for an alternative topology placing the root in between the major groups 1 + 2 and 3 + 4. This outcome indicates that the current rooting (SSU rDNA data), which places group 1 as the most basal divergence, should be viewed with caution. In addition, the analyses reveal the root of the dictyostelid group 4, and Dictyostelium purpureum can now with strong support be seen as the deepest divergence in this major group. This result is, among other things, important for determining the age of Dictyostelia. Keywords: Dictyostelia, phylogeny, root, eRF3, RPB1, SSU rDNA, α-tubulin Populärvetenskaplig sammanfattning Att förstå hur organismer är släkt med varandra är en viktig del av biologiska studier. Genom att skapa evolutionära släktträd, fylogenier, kan man få en god förståelse för hur till exempel olika egenskaper kan ha uppstått och hur de har utvecklas till det vi ser idag. En organismgrupp där fylogenetiska studier spelar en viktig roll är de sociala amöborna, Dictyostelia. Sociala amöbor är eukaryota mikrober med en fascinerande livsstrategi. De lever i jorden och under fördelaktiga förhållanden är de encelliga, livnär sig på bakterier och förökar sig genom celldelning. I brist på föda intar dictyosteliderna en ny fas – flercellighet. Med hjälp av självutsöndrade kemiska signaler klumpar amöbor ihop sig och bildar fruktkroppar som innehåller sporer. Via dessa sporer kan dictyosteliderna sedan spridas till nya områden där förhållandena förhoppningsvis är bättre. Genom att befinna sig i gränslandet mellan en- och flercellighet utgör de sociala amöborna ett viktigt studieobjekt för att förstå hur komplexitet har uppstått och hur mekanismer såsom cell-cellkommunikation och celldifferentiering fungerar. Alla evolutionära frågor behöver dock ställas med fylogenetisk information som grund, och kunskapen om de evolutionära släktskapen hos dictyosteliderna är långtifrån fullständig. Mitt arbete syftar till att ”rota” de sociala amöbornas släktträd. Detta innebär att jag har undersökt vad som är upp och vad som är ner i trädet, det vill säga vilka arter av dictyosteliderna som kan anses som de ”evolutionärt äldsta”. Att rota evolutionära träd är ett av de största problemen kopplade till fylogenetiska studier. Framför allt kräver det att man har tillgång till en stor mängd molekylär data. I mitt arbete har jag lagt samman information från fyra olika gener. En av dessa gener har aldrig tidigare använts för fylogenetiska studier hos de sociala amöborna, och under större delen av projektet har jag arbetat med att ta fram data för denna gen. Arbetet med att samla in data från en ”ny” gen består av flera olika steg. Jag började med att söka i databaser för att hitta en gen som lämpade sig för ändamålet. Efter det designade jag ”primrar” som skulle se till att den önskade genen ”klipptes ut” korrekt från genomet. Genbiten kopierades sedan upp i ett stort antal med hjälp av PCR (Polymerase Chain Reaction) och kloning med bakterier för att sedan skickas iväg för sekvensering. I fallet med sociala amöbor är det svårt att lyckas få data från den gen man tänkt sig. Primrarna går ofta inte att designa specifikt för dictyostelider och eftersom de lever i jorden är det vanligt att bakterie-DNA kommer med i proverna. Labarbetet innebar därför mycket testande fram och tillbaka, men resulterade trots detta i data från tio arter av sociala amöbor. Min insamlade data, tillsammans med data från de tre gener som redan fanns tillgänglig, tyder på att roten hos de sociala amöbornas släktträd kan vara en annan än den man hittills har förlitat sig på. Mitt arbete visar också att gruppen dictyostelider i stort är något yngre än vad man tidigare trott. Allt detta bidrar till en klarare bild av hur de sociala amöborna har evolverat och är ett steg på väg för att skapa en bättre förståelse för uppkomsten av bland annat flercellighet. Nomenclature 5PTase inositol 5-phosphatase aa amino acid BI Bayesian inference biPP posterior probability EF-2 elongation factor 2 eIF2 eukaryotic initiation factor 2 eIF5B eukaryotic initiation factor 5B eRF3 eukaryotic release factor 3 Hsp90 90 kDa heat shock protein INTS1 integrator complex subunit 1 ITS internal transcribed spacer LBA long branch attraction ML maximum likelihood mlBP bootstrap support value NT nucleotide RPB1 RNA polymerase II largest subunit SSU rDNA small subunit ribosomal DNA Contents 1 Introduction 8 1.1 Background . 8 1.2 Dictyostelids . 9 1.2.1 The dictyostelid life cycle . 9 1.2.2 Dictyostelid evolution . 11 1.2.3 Dictyostelid systematics . 11 1.3 Molecular phylogeny and its pitfalls . 13 1.3.1 Rooting . 13 1.3.2 Long branch attraction, mutational saturation and heterotachy . 13 1.3.3 The importance of increased sampling . 14 1.3.4 Finding genes appropriate for phylogenetic studies . 15 1.4 PCR amplification with degenerate primers . 15 1.5 Questions addressed . 16 1.6 Project aims . 17 2 Materials and Methods 18 2.1 Selecting target genes . 18 2.1.1 Phylogenetic evaluation of markers . 18 2.1.2 Degenerate primer design . 19 2.2 Taxonomic sampling . 20 2.2.1 Ingroup taxa . 20 2.2.2 Outgroup taxa . 21 2.3 Wet lab procedures . 21 2.3.1 Cell culture and DNA extraction . 21 2.3.2 PCR amplification with degenerate primers . 21 2.3.3 Cloning, PCR purification and sequencing . 23 2.4 Multiple sequence alignment . 24 2.5 Phylogenetic analyses . 24 2.5.1 Bayesian inference . 25 2.5.2 Maximum likelihood . 25 3 Results 27 3.1 Evaluation of possible phylogenetic markers . 27 3.2 PCR amplification with degenerate primers . 30 3.3 Constructing data sets . 31 3.4 Phylogenetic analyses . 32 3.4.1 The root of the dictyostelid tree . 33 3.4.2 The root of group 4 . 34 3.4.3 The root of group 2 . 34 4 Discussion 41 4.1 The root of the dictyostelid tree . 41 4.1.1 Benefits of eRF3 as a marker for deep dictyostelid phylogeny . 42 4.1.2 Problems with eRF3 and the other phylogenetic markers considered 42 4.1.3 Inostitol 5-phosphatase as a phylogenetic marker . 44 4.1.4 The ‘eRF3 root’ and evolutionary trends in Dictyostelia . 45 4.2 The root of group 4 . 45 4.3 Conclusions . 45 Acknowledgements 46 References 47 Appendices 51 A Primer maps 51 B eIF5B primers and unused eRF3 primers 53 C List of sequences used in the study 53 D Isolates not included in the analyses 56 E Supplemental trees 57 Introduction 1 Introduction 1.1 Background Understanding organismal relationships (phylogenetics) is the cornerstone of evolutionary study. Phylogenetic trees give guidance in how evolutionary questions should be asked and answered and also, they are important for how taxonomy should be treated. However, many of the current phylogenies available for organism groups across the tree of life are not well-resolved. They are mainly based on limited data sets and additional phylogenetic work is needed to get more accurate representations of the real organismal histories. One group of organisms for which the evolutionary picture seems complex is the social amoebae, Dictyostelia. They are eukaryotic microbes placed within the amoebozoan lineage, the closest sister group to the clade with fungi and animals (Baldauf et al. 2000). Dictyostelids were first described in 1869 (O. Brefeld) and ever since they have been studied with a focus on their unique life history, a strategy lying on the border between uni- and multicellularity (Raper 1984). The evolution of multicellularity is a striking question in biology for which the social amoebae serve as an important model system (Eichinger et al. 2005). In addition, they are uniquely useful for studying the evolution of social behaviour and basic cell biology such as cell-cell communication, cell movement and cell differentiation (Raper 1984; Kaushik and Nanjundiah 2003). According to traditional taxonomy based on morphological data, the Dictyostelia is subdivided into three separate genera: Dictyostelium, Polysphondylium and Acytostelium (Raper 1984). The first molecular phylogeny of the group was published by Schaap et al. in 2006. The work is based on parallel small subunit ribosomal DNA and alpha tubulin data sets, and it clearly indicates that the old classification of the social amoebae is deeply flawed. Instead of three distinct subdivisions, the dictyostelids comprise four major groups of which none correspond to the three traditionally proposed genera. Furthermore, Schaap et al. (2006) showed that Dictyostelia is an extremely deep taxon that is likely to have a large amount of hidden diversity. During the last years, a substantial amount of additional dictyostelid data have been added to the data set of Schaap et al. (2006), and today nearly all branches within the four higher-level taxa are fully resolved (Romeralo et al. 2010a). Furthermore, another three well-supported major clades have been distinguished in addition to the original four, giving a total of seven major clades (Romeralo et al.
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