Geobiological Coupling of Hydrothermal Vent Fluids with Endosymbiotic Primary Producers of Bathymodiolus Mussels from Hydrothermal Vents on the Mid-Atlantic Ridge

Abstract

This thesis was accomplished within the Priority Program SPP 1144 "From Mantle to Ocean" which investigates the energy-, material-, and life cycles at hydrothermal vents on the slow-spreading Mid-Atlantic Ridge. Two hydrothermal settings which differ prominently in their fluid composition are examined within the SPP: the ultramafic-hosted Logatchev vent field (14 45'N) and a cluster of basalt-hosted vent fields at 4 48'S. In contribution to the SPP the research group "Hydrothermal Symbioses" investigates the conversion of geochemical energy into biomass, particularly of hydrothermal vent mussels belonging to the genus Bathymodiolus through their chemoautotrophic and methanotrophic endosymbionts. To address this energy transfer the symbiosis research project focuses on the diversity, abundance, distribution, biomass, and activity of these endosymbiotic bacteria in regard to differing physico-chemical conditions. This PhD project aimed to (i) describe the physico-chemical conditions in Logatchev mussel habitats by means of in situ measurements, (ii) investigate the endosymbiotic diversity of B. puteoserpentis (Logatchev) using the 16S rRNA gene as a phylogenetic marker, and (iii) evaluate the activity of endosymbiotic bacteria as judged from H2 and H2S consumption and CO2 assimilation in response to the two differing hydrothermal settings. (I) In situ measurements using microsensors revealed abundant H2S and O2 in diffuse fluids emanating from the mussel beds. Thus, Logatchev mussel habitats, previously suggested to be deficient in free sulfide, comply with the requirements of aerobic sulfur-oxidation. (II) Cloning and sequencing of the 16S rRNA gene revealed three phylotypes in B. puteoserpentis. Two were related to sulfur- and methane-oxidizing symbionts. The third phylotype was identified as an intranuclear bacterial parasite which was subsequently found to be widespread in hydrothermal vent and cold seep mussels of the genus Bathymodiolus and termed "Candidatus Endonucleobacter bathymodioli". FISH and deconvolution microscopy revealed an unusual cell cycle, the first to be reported from an intranuclear parasite of metazoans. (III) Consumption of H2 and H2S along with CO2 assimilation, indicative of energy conservation and thus actively metabolizing endosymbionts, implied that endosymbiotic chemoautotrophy may be sulfur-based at basalt-hosted vent settings but hydrogen-based at ultramafic-hosted vents. Indeed, the mussel population inhabiting the ultramafic-hosted Logatchev vent field may oxidize 270-670 liters of hydrogen per hour. Endosymbionts of B. puteoserpentis may therefore play an appreciable role as H2-oxidizing primary producers and thus in converting H2-derived geochemical energy into biomass. In fact, H2 has not been shown previously to be utilized by symbionts of invertebrates from reducing environments.