Metagenomic Analyses of a Deep-Sea Mussel Symbiosis Merle Ücker

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Metagenomic Analyses of a Deep-Sea Mussel Symbiosis Merle Ücker Metagenomic analyses of a deep-sea mussel symbiosis Dissertation zur Erlangung des Grades eines Doktors der Naturwissenschaften – Dr. rer. nat. – dem Fachbereich Biologie / Chemie der Universität Bremen vorgelegt von Merle Ücker Bremen März 2021 Die vorliegende Doktorarbeit wurde von Juni 2017 bis März 2021 in der Abteilung Symbiose am Max-Planck-Institut für Marine Mikrobiologie unter der Leitung von Prof. Dr. Nicole Dubilier und direkter Betreuung von Dr. Rebecca Ansorge und Dr. Yui Sato angefertigt. The research presented in this thesis was performed from June 2017 until March 2021 at the Max Planck Institute for Marine Microbiology in the Department of Symbiosis under leadership of Prof. Dr. Nicole Dubilier and direct supervision of Dr. Rebecca Ansorge and Dr. Yui Sato. Gutachter*innen | reviewers Prof. Dr. Nicole Dubilier Prof. Dr. Thorsten Reusch Assist. Prof. Dr. Roxanne Beinart Tag des Promotionskolloquiums | date of doctoral defence 21 April 2021 Diese zur Veröffentlichung erstellte Version der Dissertation enthält Korrekturen. To the ocean. Contents Contents Summary .................................................................................................................................... 1 Zusammenfassung...................................................................................................................... 2 Chapter I | Introduction .............................................................................................................. 4 Aims of this thesis ................................................................................................................ 19 List of publications .............................................................................................................. 34 Chapter II | Symbionts in a mussel hybrid zone ...................................................................... 36 Chapter III | Symbionts in the water column ........................................................................... 80 Chapter IV | Hosts from the Mid-Atlantic Ridge ................................................................... 130 Chapter V | Discussion, future directions, and concluding remarks ...................................... 196 Acknowledgements ................................................................................................................ 223 Contribution to manuscripts ................................................................................................... 227 Versicherung an Eides Statt ................................................................................................... 228 Summary Summary Symbiosis is ubiquitous across all domains of life. Deep-sea hydrothermal vents are home to extraordinary examples of symbiosis. Fascinating symbiotic communities are fuelled by reduced chemical compounds released from fissures in the oceanic crust. Chemosynthetic symbionts use the energy of reduced chemicals energy to produce biomass and to support their animal hosts to thrive in environments where nutrients are scarce. Bathymodiolus mussels are among the most successful fauna in such habitats. Within their gills, they host sulphur- and methane-oxidising symbionts, among others. These symbiotic bacteria are acquired from the environment, suggesting the existence of a free-living stage. The mussels are well studied for their symbionts’ physiology, host-symbiont interaction and the host's immune system. Some interesting questions, however, have remained unresolved. I used metagenomics, a versatile and cultivation-independent approach, to address some of these questions: What can a mussel hybrid zone reveal about factors driving symbiont composition? Hybrid zones provide an opportune system to study evolutionary processes in their natural context. Analysis of symbionts from co-occurring hybrid and parental mussels at the Broken Spur vent field allowed me to identify whether host genetics, geography, or the environment, is driving the symbiont community composition. Phylogenomics revealed the presence of a new location-specific symbiont subspecies. Symbionts of hybrids and parental mussels could not be distinguished genetically. Thus, host genetics seem to have little influence on the symbiont community. Instead, geography explained much of the observed symbiont variation. Whether the symbiont population structure results from a geographical structuring of the free-living pool of symbionts remains to be elucidated. Are free-living symbionts present in the water column? Knowledge about the free-living stage of horizontally transmitted symbionts can give insights into the symbiont uptake and the specificity of the association. To investigate the presence of symbionts in the free-living stage, I screened for symbiont marker genes in water metagenomes. While symbiont-related genes were detected, they always co-occurred with host DNA. This raises the question whether the symbionts in my data are free-living or still associated with their hosts. The results suggest that transmission via host particles may be more important than anticipated. To further future research based on the experiences of this work, I suggest sampling schemes to learn more about the free-living stage. Are mitochondrial and nuclear genomes congruent in Bathymodiolus? Species assignment is often performed using mitochondrial marker genes. Mitochondrial inheritance in bivalves is often complex, and incongruent nuclear and mitochondrial genomes have been described for the Bathymodiolus hybrid zone. I compared mitochondrial clades to clustering based on the nuclear genome and found incongruences for 10 % of the 175 analysed mussels. The high- resolution analysis further revealed a lack of subpopulation structure in conspecific mussels from different sites. Both findings suggest a strong genetic connectivity of populations at the Mid-Atlantic Ridge, probably enabled by long-distance migration of planktotrophic larvae. The biological processes underlying the mitonuclear discordance are exciting topics for future analyses. Altogether, the research presented in this thesis enhances our understanding of the symbiotic association in Bathymodiolus mussels and provides the basis for further population genomic studies of host, symbionts and the free-living bacterial community. 1 Zusammenfassung Zusammenfassung Symbiosen sind allgegenwärtig. Besondere Beispiele finden sich an Tiefsee- Hydrothermalquellen, wo reduzierte chemische Stoffe aus Rissen der Ozeankruste entweichen und die Grundlage für Gemeinschaften faszinierender symbiotischer Tiere bilden. Bathymodiolus Muscheln gehören zu den wenigen Tieren, die in diesem Lebensraum erfolgreich sind. Ihre chemosynthetische Symbionten nutzen chemische Energie, um Biomasse herzustellen. So unterstützen sie ihren tierischen Wirt dabei, in einem Lebensraum zu gedeihen, der sonst lebensfeindlich wäre. Die Sulfat- und Methan-oxidierende Symbionten werden aus der Umwelt aufgenommen, was die Existenz eines freilebenden Stadiums voraussetzt. Viele Studien haben sich mit der Bathymodiolus Symbiose auseinandergesetzt, doch einige Fragen blieben bisher ungelöst. Mithilfe von Metagenomik, einem vielseitigen Ansatz, der unabhängig von Kultivierung ist, habe ich mich mit folgenden Fragen beschäftigt: Welche Faktoren bestimmen die Zusammensetzung von Symbiontengemeinschaften? Hybridzonen bieten die Möglichkeit, evolutionäre Prozesse in ihrem natürlichen Kontext zu erforschen. Anhand einer Analyse der Symbionten von zusammen vorkommenden Hybriden und Eltern im Broken Spur Hydrothermalfeld habe ich untersucht, ob Wirtsgenetik, Geographie oder Umweltfaktoren die Symbiontenzusammensetzung bestimmen. Mit Phylogenomik habe ich eine neue, ortsspezifische Symbiontenunterart entdeckt. Die Symbionten von Hybriden und Eltern unterscheiden sich genetisch nicht. Scheinbar ist die Wirtsgenetik für die Zusammensetzung der Symbiontengemeinschaft weniger wichtig als die Geographie, die einen Großteil der Symbionten-Variation erklärt. Ob die Populationsstruktur der Symbionten durch die geographische Struktur von freilebenden Symbionten bestimmt wird, muss in zukünftigen Studien geklärt werden. Gibt es freilebende Symbionten in der Wassersäule? In horizontal übertragenen Symbiosen ermöglicht Wissen über das freilebende Stadium Rückschlüsse auf die Symbiontenaufnahme und die Spezifität der Symbiose. Um die Existenz von Symbionten im freilebenden Stadium zu erforschen, habe ich Metagenome von Wasserproben auf Symbionten Markergene untersucht. Dabei wurden Symbionten-bezogene Gene gefunden. Sie traten allerdings immer zusammen mit der DNA des Wirtes auf. Dies lässt vermuten, dass eine Symbiontenübertragung über Wirtspartikel eine wichtigere Rolle spielen könnte als bisher vermutet. Für zukünftige Forschungsprojekte habe ich Vorschläge für die Beprobung erarbeitet, um dem freilebenden Symbiontenstadium weiter auf den Grund zu gehen. Stimmen mitochondriale und nukleare Genome von Bathymodiolus überein? Mitochondrien werden häufig zur Artenbestimmung herangezogen, ihre Vererbung in Muscheln ist aber zum Teil sehr komplex. Außerdem passen nukleare und mitochondriale Genome in der Hybridzone nicht zusammen. Ich habe das mitochondriale mit dem nuklearen Genom verglichen und dabei entdeckt, dass diese in 10 % der untersuchten Muscheln nicht zusammenpassten. Zudem hat die Analyse gezeigt, dass sich Muscheln der gleichen Art von verschiedenen Orten kaum unterscheiden. Beide Ergebnisse deuten darauf hin, dass die Muschelpopulationen am Mittelatlantischen Rücken stark
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