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The discovery of deep-sea hydrothermal vents in 1977 revolutionized our understanding of the energy sources that fuel primary productivity on Earth. Hydrothermal vent ecosystems are dominated by animals that live in symbiosis with chemosynthetic bacteria. So far, only two energy sources have been shown to power chemosynthetic symbioses: reduced sulphur compounds and methane. Using metagenome sequencing, single-gene fluorescence in situ hybridization, immunohistochemistry, shipboard incubations and in situ mass spectrometry, we show here that the symbionts of the hydrothermal vent mussel Bathymodiolus fromthe Mid-Atlantic Ridge use hydrogen to power primary production. In addition, we show that the symbionts of Bathymodiolus mussels from Pacific vents have hupL, the key gene for hydrogen oxidation. Furthermore, the symbionts of other vent animals such as the tubeworm Riftia pachyptila and the shrimp Rimicaris exoculata also have hupL. We propose that the ability to use hydrogen as an energy source is widespread in hydrothermal vent symbioses, particularly at sites where hydrogen is abundant.
Deep-sea hydrothermal vents and their associated chemosynthetic communities were discovered in 19771. Since then, two energy sources have been shown to fuel primary production by the symbiotic bacteria that form the basis of the food chain in marine chemosynthetic ecosystems. In 1981, chemolithoautotrophic bacteria that use reduced sulphur compounds as an energy source were discovered in the gutless Riftia pachyptila tubeworms from hydrothermal vents in the Pacific2,3. Five years later, the first symbionts that use methane as an energy source were discovered in mussels from hydrocarbon seeps in the Gulf of Mexico4,5. Since then, a vast array of chemosynthetic ecosystems has been explored, and novel symbioses of phylogenetically diverse hosts and symbionts are constantly being described6. Despite this, no other source of energy for metazoan chemosynthetic symbioses has yet been found. This is remarkable, given that many potential sources of energy for chemosynthesis are available, such as hydrogen, ammonium, ferrous iron and manganese(II)7, and free-living vent microbes able to use these energy sources are well known8-10.
Some hydrothermal vents produce fluids with very high hydrogen concentrations due to the interaction of seawater with mantle-derived ultramafic rocks. Fluids originating from ultramafic-hosted vents are also characterized by high methane concentrations, whereasH2S concentrations are rather low. In contrast, basalt-hosted vents produce fluids comparably high in H2S but low in H2...