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Nusuttodinium Aeruginosum/Acidotum As a Case Study

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Nusuttodinium Aeruginosum/Acidotum As a Case Study Acquisition of Photoautotrophy in Kleptoplastic Dinoflagellates – Nusuttodinium aeruginosum/acidotum as a case study I n a u g u r a l – D i s s e r t a t i o n zur Erlangung des Doktorgrades der Mathematisch-Naturwissenschaftlichen Fakultät der Universität zu Köln vorgelegt von Sebastian Wittek aus Krefeld 2018 Berichterstatter: Prof. Dr. Michael Melkonian Prof. Dr. Hartmut Arndt Prof. Dr. John M. Archibald Tag der mündlichen Prüfung: 16.01.2017 Kurzzusammenfassung in deutscher Sprache ------------------------------------------------------------------------------------------------------------------------------ Kurzzusammenfassung in deutscher Sprache Die Integrierung stabiler Plastiden durch Endosymbiosen führte zu einer enormen Vielfalt an photosynthetischen eukaryotischen Organismen auf der Erde. Allerdings sind die Schritte während der Etablierung stabiler Endosymbiosen nur schlecht verstanden. Um Licht auf diesen frühen Schritt der Evolution zu werfen, wurden viele Studien an Organismen mit vorübergehenden Plastiden durchgeführt. Ursprünglich heterotroph, sind diese Organismen in der Lage, Photoautotrophie durch die Aufnahme photosynthetischer Beute zu erwerben. Anstatt verdaut zu werden, behält die Beute ihre Fähigkeit zur Photosynthese bei und versorgt den Wirt mit Photosyntheseprodukten. Der Beuteorganismus kann entweder zu einem Endosymbiont oder sogar zu einem Plastid reduziert werden. Im letzteren Fall werden die Plastiden der photosynthetischen Beute gestohlen und daher ‚Kleptoplastiden‘ genannt. Kleptoplastiden sind innerhalb der Eukaryoten weit verbreitet und kommen in vielzelligen, wie auch in einzelligen Organismen vor. Eine der bekanntesten Gruppen, welche Kleptoplastiden beherbergt, sind die Dinoflagellaten. Diese Studie fokussiert auf Süßwasserisolate der Kleptoplastiden beherbergenden Gattung Nusuttodinium mit einem besonderen Fokus auf die Art N. aeruginosum/acidotum, welche ihre Kleptoplastiden von der blau-grünen cryptophytischen Gattung Chroomonas erlangt. Es wurden von N. aeruginosum/acidotum, sowie einer weiteren Art, N. amphidinoides stabile, bakterienfreie Co-Kulturen etabliert und ihr Lebenszyklus wurde untersucht. Im Gegensatz zu allen anderen Systemen, welche bis heute beschrieben wurden, ist N. aeruginosum/acidotum in der Lage, Kleptoplastiden unterschiedlicher Morphologie und Stabilität zu beherbergen, wodurch diese Art ein ideales Modellsystem für die Untersuchung möglicher Schritte während der Erlangung stabiler, permanenter Plastiden ist. Abhängig von der phylogenetischen Stellung der Beute können entweder sogenannte ‚granuläre‘ oder U-förmige‘ Kleptoplastiden gebildet werden. Morphologisch sind granuläre Kleptoplastiden durch ihre erhöhte Anzahl und geringe Größe charakterisiert. Jeder Kleptoplast ist mit einem kleinen cryptophytischen Zellkern, dem sogenannten ‚Kleptokaryon‘ assoziiert und ähnelt frisch aufgenommener Beute. Kleptokarya sind für bis zu 10 - und die Kleptoplastiden für bis zu 14 Tage stabil. Im granulären Zustand nehmen die Zellen permanent Beute auf, ganz besonders kurz nach der Zellteilung, die während der Dunkelphase stattfindet. Im Gegensatz dazu ist die U-förmige Situation durch einen einzigen, großen U-förmigen Plastiden gekennzeichnet, welcher die Zelle ausfüllt, sowie durch einen einzigen großen Kleptokaryon, welcher sich antapikal in dem Bogen des U befindet. Verglichen zur freilebenden Beute und granulären Situation nimmt die Größe des Kleptoplasten um das bis zu 20 fache - und die des Kleptokaryon um das bis zu 16 fache zu. I Kurzzusammenfassung in deutscher Sprache ------------------------------------------------------------------------------------------------------------------------------ Während der Kleptoplast bei der Zellteilung gleichermaßen an beide Tochterzellen vererbt wird, erhält nur eine den Kleptokaryon. Für den Kleptokaryon wurde eine Stabilität von bis zu 50 Tagen- und für den Kleptoplasten von bis zu 60 Tagen beobachtet. DNA- Fluoreszenzmessungen, sowie eine auf PCR basierende Herangehensweise mit Primern, spezifisch für den Cryptophyten-Zellkern deuten auf eine Polyploidisierung des cryptophytischen Zellkerns nach Aufnahme durch den Dinoflagellaten hin. Zusätzlich erhöhen die vergrößerten Kleptokarya die Stabilität der Kleptoplasten und beeinflussen das Verhalten von N. aeruginosum/acidotum. Die Aufnahme von Beute wird gehemmt und die Dinoflagellaten zeigen größtenteils ein gerades Schwimmverhalten, welches sich deutlich von dem in der granulären Situation unterscheidet. Herrscht eine sehr hohe Beuteverfügbarkeit, formt N. aeruginosum/acidotum anstelle der U-förmigen Kleptoplasten granuläre, welche verdaut werden, falls die Beuteverügbarkeit hoch bleibt oder, falls die Beuteverfügbarkeit abnimmt, gleichermaßen auf die Tochterzellen verteilt werden, in welchen sie sich letztendlich zu U-förmigen, stabilen Kleptoplasten entwickeln. Im Gegensatz zu N. aeruginosum/acidotum repräsentiert N. amphidinoides ein primitiveres Stadium während der Erlangung von Plastiden, da die Kleptokarya kurz nach der Beuteaufnahme verdaut werden und die Kleptoplasten weniger modifiziert und unstabiler, als die U-Plastiden sind. Der Vergleich der ‚pimitiven‘ granulären Situation mit der ‚fortgeschritteneren‘ U-förmigen Situation unter Rücksichtnahme der Literatur erlaubt die Aufstellung einer neue Hypothese, nach der Beutemangel ein Auslöser- und Polyploidisierung einer der wichtigsten Schritte zur Erlangung stabiler Plastiden sind. II Abstract in englischer Sprache --------------------------------------------------------------------------------------------------------------------------- Abstract in englischer Sprache The integration of stable plastids by endosymbiosis led to an enormous diversity of photosynthetic eukaryotic organisms on earth. However, the steps during the establishment of a stable endosymbiosis are poorly understood. To address this early step of evolution, many studies have been performed on organisms with transient plastids. Originally heterotrophic, are these organisms able to acquire photoautotrophy through the uptake of photosynthetic prey. In contrast to being digested, the prey preserves its photosynthetic ability and supplies the host with photosynthetic products. The prey can either be reduced to an endosymbiont or even to a single plastid. In the latter case the plastids are stolen from photosynthetic prey and therefore called ‘kleptoplasts’. Kleptoplasts are widespread among eukaryotes and occur in multicellular as well as in unicellular organisms. One of the most prominent groups harboring kleptoplasts is the dinoflagellates. This study focuses on freshwater isolates of the kleptoplastic genus Nusuttodinium with a special focus on the species N. aeruginosum/acidotum that acquires its kleptoplasts from the blue-green cryptophyte genus Chroomonas. Stable axenic co-cultures from different locations were established for N. aeruginosum/acidotum and for another species N. amphidinoides and their live cycles were studied. In contrast to all other systems described until now, N. aeruginosum/acidotum is able to harbor kleptoplasts of different morphology and stability making it an ideal model system to study possible steps during the acquisition of stable permanent plastids. Depending on the phylogenetic position of the prey either ‘granular’ or ‘U-shaped’ kleptoplasts are formed. Granular kleptoplasts are characterized morphologically by their multiple number and small size. Each kleptoplast is associated with a small cryptophyte nucleus, the ‘kleptokaryon’ and resembles recently ingested prey. Kleptokarya are stable for up to 10 days and kleptoplasts for up to 14 days. In the granular stage cells took up prey permanently, especially just after cell division that takes place during the dark phase. In contrast, the U-shaped situation is characterized by just one large U-shaped kleptoplast filling out the cell and a single large kleptokaryon located antapically in the curve of the U. Compared to the free living prey and the granular situation, the kleptoplast increases up to 20 fold in size and the kleptokaryon up to 16 fold. Whereas the kleptoplast is distributed equally to both daughter cells during cell division, just one inherits the kleptokaryon. A stability of up to 50 days was recorded for the kleptokaryon and up to 60 days for the kleptoplast. DNA fluorescence measurements and a PCR based approach with primers specific to the cryptophyte nucleus indicate polyploidization of the cryptophyte nucleus after ingestion by the dinoflagellate. In addition enlarged kleptokarya increase kleptoplast stability and influence the behavior of N. III Abstract in englischer Sprache --------------------------------------------------------------------------------------------------------------------------- acidotum/aeruginosum. Prey uptake is inhibited by intact kleptokarya and dinoflagellates mostly show straight swimming behavior that clearly differs from the behavior in the granular situation. If prey availability is very high N. aeruginosum/acidotum does not form U-shaped kleptoplasts but instead forms granular kleptoplasts that are digested if prey availability remains high or, if prey availability decreases, are distributed equally to the daughter cells in which they develop into stable U-shaped kleptoplasts. In contrast to N. aeruginosum/acidotum, N. amphidinoides represents a more primitive stage during plastid acquisition as kleptokarya are digested shortly after ingestion and kleptoplasts are less modified and stable than the U-shaped plastids.
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