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Exploring the Lipidomes of Shallow-Water and Deep-Sea Hydrothermal Systems

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Exploring the Lipidomes of Shallow-Water and Deep-Sea Hydrothermal Systems Exploring the lipidomes of shallow-water and deep-sea hydrothermal systems Dissertation zur Erlangung des Doktorgrades der Naturwissenschaften - Dr. rer. nat. - Am Fachbereich Geowissenschaften der Universität Bremen vorgelegt von Miriam Sollich Bremen Mai 2018 1. Gutachter: Dr. Solveig I. Bühring 2. Gutachter: Associate Prof. Dr. Eoghan P. Reeves Tag des Promotionskolloquiums:16. Februar 2018 Den Wissenschaftlern geht es wie den Chaoten. Es ist alles da, man muss es nur suchen. - Franz Kern - CONTENTS Abstract Zusammenfassung Acknowledgements List of Abbreviations Chapter I 1 Introduction and Methods Chapter II 37 Scope and Outline Chapter III 43 Heat stress dictates the microbial lipid composition along a thermal gradient in marine sediments Chapter IV 91 Shallow-water hydrothermal systems offer ideal conditions to study archaeal lipid membrane adaptations to environmental extremes Chapter V 113 Transfer of chemosynthetic fixed carbon and its ecological significance revealed by lipid analysis of fluids at diffuse flow deep-sea vents (East Pacific Rise 9°50’N) Chapter VI 143 Concluding Remarks and Future Perspectives ABSTRACT Shallow-water and deep-sea hydrothermal systems are environments where seawater percolates downward through fractures in the oceanic crust, and becomes progressively heated and chemically altered. Finally, the entrained water is expelled into the overlying water column as a hydrothermal fluid. Hydrothermal circulation occurs at all active plate boundaries like mid-ocean ridges, submarine volcanic arcs and backarc basins. They represent one of the most extreme and dynamic ecosystems on the planet with steep physico-chemical gradients. Nevertheless, these environments are characterized by exceptional high biomass representing hotspots of life in the mostly hostile and desolated deep sea. Although shallow-water and deep-sea hydrothermal systems share basic physical processes regarding heat transfer and water circulation they differ in various physico-chemical parameters. The cut-off between “shallow” and “deep” was defined to ~200 m water depth, which loosely correlates with the extent of the photic zone and results in striking differences of species community structures. This dissertation is focused on the microbial ecology in hydrothermal systems, more specifically on the lipidome and encoded lipid structure-functions of microbial membranes. The first study examines sediments from the shallow-water hydrothermal sediments off the coast of Milos along a temperature gradient from 18 to 101 °C [Chapter III]. The rationale was to test the concept that membrane lipids dictate the thermodynamic ecology of bacteria and archaea, by minimizing loss of energy by ion diffusion across the membrane. A detailed investigation of archaeal and bacterial polar lipids revealed a membrane quandary: not only the expected low permeability, but also increased fluidity of membranes are required as a unified property of microbial membranes for energy conservation under heat stress. For instance, bacterial fatty acids were composed of longer chain lengths in concert with a higher degree of unsaturation while archaea modified their tetraethers by incorporation of additional methyl groups at elevated sediment temperatures. These configurations toward a more fluidized membrane at elevated temperatures were observed with a concomitantly high abundance of archaeal glycolipids and bacterial sphingolipids. It is suggested that glycolipids and sphingolipids could reduce membrane permeability through strong intermolecular hydrogen bonding. Results of this chapter provide a new angle for interpreting membrane lipid structure-function enabling archaea and bacteria to survive and grow in hydrothermal systems. In chapter III, the modifications observed for abundant archaeal glycosidic tetraethers (e.g., increase in “H-shaped” structures and number of methyl groups and cyclopentane rings) were correlated with elevated sediment temperatures. This result was reproduced in another shallow-water hydrothermal system sampled along a thermal gradient off Dominica in the second study of this thesis [Chapter IV]. Furthermore, statistical multivariate analyses helped to identify additional geochemical key players which strongly impacted the lipid distribution in hydrothermally-influenced sediments. H-shaped structures clearly correlated with temperature, while H-shaped methylated GDGT showed a strong correlation with increasing hydrogen sulfide concentrations and salinity. The last study of this thesis investigated, for the first time, the lipid diversity in diffuse flow fluids and adjacent bottom water from the East Pacific Rise [Chapter V]. Lipids in these samples were dominated by triacylglycerols, wax esters and alkyldiacylglycerols (> 90% of total lipids), rarely found in bacteria – especially in Epsilonproteobacteria, which are the most prevalent chemosynthetic taxa in these systems. Moreover, polyunsaturated fatty acids (PUFA, both ω-3 and ω-6) represented up to 20% of total fatty acids linked to major phospholipids such as phosphatidyl-choline and -ethanolamine, an uncommon feature among bacterial membranes. Thus the high abundance of storage lipids and PUFA linked to phospholipids indicate eukaryotes rather than bacteria as the major source of lipids in diffuse hydrothermal fluids and adjacent bottom water. Stable carbon isotopic analysis of fatty acids, which are mainly derived from storage lipids, revealed an intimate energy flux from chemosynthetic fixed carbon to higher trophic levels in diffuse flow systems. Chapter V highlights the trophic transfer in these diffuse flow systems and addresses the origin of PUFA in deep-sea hydrothermal vents. ZUSAMMENFASSUNG Flachwasser- und Tiefseehydrothermalsysteme sind Gebiete in denen Meerwasser durch Spalten und Risse tief in die Ozeankruste eindringt. Auf dem Weg tiefer in die Ozeankruste wird das Meerwasser kontinuierlich erwärmt und auch die chemische Zusammensetzung verändert sich bevor es zurück an die Oberfläche gelangt und dort als hydrothermales Fluid an das Meerwasser abgegeben wird. Hydrothermale Zirkulation findet an allen aktiven Plattenrändern statt zu denen Mittelozeanische Rücken, Backarc- Becken und unterseeische vulkanische Inselbögen zählen. Hydrothermalsysteme weisen ausgeprägte physikalische und chemische Gradienten auf und stellen eines der extremsten und dynamischsten Ökosysteme dieser Welt dar. Trotzdem sind diese Gebiete durch eine atemberaubende Vielfalt an Lebewesen charakterisiert und stellen sogenannte Oasen in der sonst öden und lebensfeindlichen Tiefsee dar. Obwohl Flachwasser- und Tiefseehydrothermalsysteme auf den gleichen physikalischen Prozessen des Wärmetransfers und der Wasserzirkulation beruhen, unterscheiden sie sich stark in einigen physikalischen und chemischen Parametern. Die Grenze zwischen „Flach“ und „Tief“ verläuft bei ~200 m Wassertiefe, ungefähr bis zu der Tiefe in der maximal das Sonnenlicht vordingen kann. Dies wiederum hat erhebliche Auswirkungen auf die Artenzusammensetzung, die sehr unterschiedlich in beiden Systemen ist. Diese Dissertation fokussierte sich auf die mikrobielle Ökologie von Hydrothermalsystemen, insbesondere des Lipidoms und den in mikrobiellen Membranen enthaltenden Informationen über die Struktur und Funktion von Lipiden. Die erste Studie untersuchte Sedimente eines Flachwasserhydrothermalsystems entlang eines Temperaturgradienten von 18 bis 101 °C vor der Küste von Milos. Es sollte das Konzept getestet werden, ob Membranlipide die thermodynamische Ökologie von Bakterien und Archaeen dadurch bestimmen, dass sie den Energieverlust mittels Ionendiffusion durch die Membran minimieren. Eine detaillierte Untersuchung archaeeller und bakterieller Polarlipide brachte jedoch eine konträre Situation zum Vorschein: neben der bereits erwarteten geringen Permeabilität, konnte eine zeitgleiche erhöhte Fluidität der Membran als einheitlicher Code mikrobieller Membranen zur Energiekonservierung unter Temperaturstress beobachtet werden. Zum Beispiel bestanden bakterielle Fettsäuren aus längeren Ketten bei zeitgleichem höheren Unsättigungsgrad, während Archaeen ihre Tetraether dadurch modifizierten, indem sie zusätzliche Methylgruppen bei höherer Temperatur einbauten. Diese Konfigurationen in Richtung einer erhöhten Fluidität bei höheren Temperaturen wurde bei zeitgleicher erhöhter Abundanz glykosidischer achaeeller Lipide und bakterieller Sphingolipide beobachtet. Es wird diskutiert ob Glykolipide und Sphingolipide die Membranpermeabilität dadurch verringern, indem sie die Ausbildung intermolekularer Wasserstoffbrückenbindungen intensivieren. Diese Ergebnisse eröffnen völlig neue Interpretationsmöglichkeiten bezüglich der Untersuchung gewisser Abhängigkeiten von Struktur und Funktionalität von Membranlipiden, die Archaeen und Bakterien überhaupt erst ermöglichen in Hydrothermalgebieten erfolgreich zu gedeihen. Die in Kapitel III beobachteten Modifikationen archaeeller glykosidischer Tetraether (Abundanz der „H-shape“ Struktur und Anzahl zusätzlicher Methylgruppen und Cyclopentanringe), korrelierten positiv mit ansteigender Sedimenttemperatur. Diese Ergebnisse konnten in einem anderen Flachwasserhydrothermalsystem entlang eines Temperaturgradienten vor der Küste Dominicas in einer zweiten Studie reproduziert werden [Kapitel IV]. Darüber hinaus konnten multivariate Analysemethoden weitere geochemische Schlüsselparameter identifizieren, die die Lipidverteilung in hydrothermalen Sedimenten stark beeinflussten. H-shape Strukturen zeigten eine deutliche
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