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A microbiological and biogeochemical investigation of the cold seep tubeworm Escarpia southwardae (Annelida: Siboglinidae): Symbiosis and trace element composition of the tube
Institution:1. Westfälische Wilhelms-Universität Münster, Institut für Geologie und Paläontologie, Corrensstr. 24, 48149 Münster, Germany;2. Institute for Applied Geosciences, Graz University of Technology, Rechbauerstraße 12, 8010 Graz, Austria;3. Paul Scherrer Institut, Swiss Light Source, 5232 Villigen PSI, Switzerland;4. Centre for Microscopy, Characterisation and Analysis, University of Western Australia, Perth 6009, Australia;5. ANKA Synchrotron Radiation Facility, Karlsruhe Institute of Technology, Karlsruhe, Germany;6. Ruhr-University Bochum, Department of Geology, Mineralogy, and Geophysics, Universitätsstr. 150, 44801 Bochum, Germany;7. Department of Earth and Environmental Sciences and GeoBioCenter, Ludwig-Maximilians-Universität München, Germany;1. MLR Key Laboratory of Marine Mineral Resources, Guangzhou Marine Geological Survey, Guangzhou 510075, China;2. Shanghai Engineering Research Center of Hadal Science and Technology, College of Marine Sciences, Shanghai Ocean University, Shanghai 201306, China;3. CAS Key Laboratory of Marginal Sea Geology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China;1. MARUM — Center for Marine and Environmental Sciences and Department of Geosciences, University of Bremen, 28334 Bremen, Germany;2. IFREMER, Unité de Recherche Géosciences Marines, 29280 Plouzané, France;3. Institute of Geology, University of Hamburg, 20146 Hamburg, Germany;4. State Key Laboratory for Mineral Deposits Research, Department of Earth Sciences, Nanjing University, Nanjing 210093, China;5. Department of Geodynamics and Sedimentology, Center for Earth Sciences, University of Vienna, 1090 Vienna, Austria
Abstract:Tubeworms within the annelid family Siboglinidae rely on sulfur-oxidizing autotrophic bacterial symbionts for their nutrition, and are among the dominant metazoans occurring at deep-sea hydrocarbon seeps. Contrary to their relatives from hydrothermal vents, sulfide uptake for symbionts occurs within the anoxic subsurface sediment, in the posterior ‘root’ region of the animal. This study reports on an integrated microbiological and geochemical investigation of the cold seep tubeworm Escarpia southwardae collected at the Regab pockmark (Gulf of Guinea). Our aim was to further constrain the links between the animal and its symbiotic bacteria, and their environment. We show that E. southwardae harbors abundant sulfur-oxidizing bacterial symbionts in its trophosome. Symbionts are able to fix inorganic carbon using the Calvin-Benson cycle, as reported in most other Siboglinidae, but can also use the reverse Tricarboxilic Acid Cycle. Surprisingly, the observed bacteria appear to be more closely related to symbionts of Escarpia and Lamellibrachia species from very distant sites located in the Gulf of Mexico and eastern Pacific, than to symbionts of a siboglinid occurring at a nearby methane seep site, only a few hundred km away from Regab. Then, by combining scanning electron microscopy and trace element (Mn, Fe, Sr, Zr) analyses of E. southwardae tube, we also show that two distinct oxidation fronts occur along the tube. The first one, near the posterior end of the tube, corresponds to the interface between oxic bottom waters and the underlying anoxic sediment. In contrast, the second redox front is located in the most anterior part of the tube, and could result from active oxygen uptake by the plume of the tubeworm. We speculate that intense oxygen consumption in this region could create favorable conditions for sulfate reduction by specialized bacteria associated with the plume, possibly leading to an additional source of dissolved sulfide that would further enhance the productivity of bacterial symbionts.
Keywords:Sulfur-oxidizing bacteria  rTCA  Trace elements  RubisCO  Symbiosis
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