Marine shallow hydrothermal systems: imprint of their exclusive biogeochemistry on dissolved organic matter and chemosynthesis

Shallow submarine hydrothermal systems are extreme environments with unique biogeochemical conditions, originating from (1) the interaction of hot, reduced fluids and cold, oxygenated seawater, and (2) the possibility of simultaneous primary production by photo- and chemosynthesis. The flux of carbon, reduced molecules and trace elements from hydrothermal vents is mainly controlled by dissolved organic matter (DOM), which is one of the largest pools of organic carbon in the oceans and therefore plays a major role in key biogeochemical cycles. However, the influence of hydrothermal activity on DOM at a molecular level has not been investigated, and an holistic understanding of the functioning of marine shallow systems is currently lacking. The aim of this thesis was to investigate the imprint of the exclusive biogeochemistry of marine shallow hydrothermal systems on (1) the DOM molecular signature and associated redox processes at the interface between fluids and seawater (Chapters 3, 4, S8), and (2) the role of chemoautotrophy in carbon fixation at hydrothermally influenced sediments (Chapters 5, S7). The study sites were three contrasting shallow systems off Dominica (Caribbean Sea), Milos (Eastern Mediterranean) and Iceland (North Atlantic). In contrast to the predominantly meteoric fluids from Dominica and Iceland, hydrothermal fluids from Milos were mainly fed by recirculating seawater. Milos fluids were also strongly enriched in hydrogen sulfide (H2S) and dissolved organic sulfur (DOS), as indicated by high DOS/DOC ratios and by the fact that 93% of all assigned DOM molecular formulas exclusively present in the fluids contained sulfur. Evaluation of hypothetical pathways suggested DOM reduction and sulfurization during seawater recirculation in Milos seafloor. The four most effective pathways were those exchanging an O atom by one S atom in the formula or the equivalent H2S reaction. In all three systems, low O/C molar ratios in the fluids suggested shallow hydrothermal systems as a source of reduced DOM and DOS, which will likely get oxidized upon contact with oxygenated seawater (Chapter 3). In Dominica, hydrothermal fluids were strongly enriched in dissolved Fe(II), leading to the precipitation of Fe(III) oxides in the oxic surface sediment. The marine hydrothermal iron-DOM interaction was characterized at a molecular level and the role of chemosynthesis in carbon fixation was investigated. The formation of Fe(III) oxides upon aeration of the hydrothermal fluids for 10 h led to an 8% decrease in dissolved organic carbon (DOC), indicating co-precipitation of iron and DOM. Re-solubilization of iron precipitates revealed increased relative abundance of aromatic compounds in co-precipitated DOM, which is in accordance with iron-coagulation observed in terrestrial environments (Chapter 4). On the other hand, bacterial community structure analysis revealed the presence of key players in iron cycling generally known from deep-sea vents (e.g. Zetaproteobacteria), suggesting biologically mediated iron redox processes in the Dominica system. Uptake of 13C-bicarbonate into fatty acids under light and dark conditions revealed the potential of active photo- and chemoautotrophic communities, indicating that chemosynthesis was responsible for up to 65% of total carbon fixation (Chapter 5). In conclusion, this thesis (1) reveals novel insights about DOM and DOS dynamics in marine hydrothermal ecosystems, suggesting a conceptual framework for molecular-scale mechanisms in organic sulfur geochemistry; (2) provides evidence for co-precipitation of DOM with iron at hydrothermal systems as a selective process, which characteristically alters the molecular composition of DOM released with hydrothermal fluids; and (3) highlights shallow hydrothermal systems as hotspots for chemoautotrophy, emphasizing chemosynthesis as a major process of primary production in marine coastal environments with hydrothermalism.