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The Symbiome of Bathymodiolus Mussels from Hydrothermal Vents: From the Genome to the Environment

Final Report Summary - BATHYBIOME (The Symbiome of Bathymodiolus Mussels from Hydrothermal Vents: From the Genometo the Environment)

Deep-sea hydrothermal vents and hydrocarbon seeps are among the most productive ecosystems on Earth. They are based on chemosynthesis, that is the fixation of carbon dioxide into organic compounds as in photosynthesis, but using reduced chemical compounds, such as sulfide or hydrogen, as energy sources instead of sunlight. The majority of the biomass in these ecosystems is generated through symbiotic microbe-animal associations. Bathymodiolus mussels are able to build extraordinarily large and productive populations at vents and seeps because they harbor symbiotic chemosynthetic bacteria that use chemical energy sources from the vent and seep fluids to feed their hosts via carbon fixation.
The overarching goal of BathyBiome was to develop a better understanding of the processes that have contributed to the ecological and evolutionary success of the over 60 million year old symbiosis between Bathymodiolus mussels and their beneficial bacteria. We successfully completed eight research expeditions to deep-sea hydrothermal vents and hydrocarbon seeps in the Atlantic, Gulf of Mexico, East Pacific, and Southwest Pacific during which we collected 12 species of Bathymodiolus mussels and performed in-situ and on-board experiments. Comparative metagenomic, metatranscriptomic, metaproteomic and metabolomic analyses as well as imaging techniques that included fluorescence in situ hybridization, electron microscopy and spatial metablomics revealed that the diversity of Bathymodiolus symbionts and their metabolic capabilities is much higher than previously recognized.
For example, we found that a previously undescribed group of Epsilonproteobacteria colonizes the gill tissues of Bathymodiolus mussels from vents and seeps worldwide. These epibiotic bacteria differ from all other known Epsilonproteobacteria in the pathways they use for carbon fixation. The genes for this unusual carbon fixation pathway were most likely acquired through horizontal gene transfer, and we hypothesize that this acquisition was a key factor in enabling these bacteria to establish a successful symbiosis with bathymodiolin mussels.
Another discovery of unexpected symbiont diversity came from our analyses of Bathymodiolus from deep-sea oil seeps in the Gulf of Mexico. These mussels live in an intimate symbiosis with oil-degrading bacteria called Cycloclasticus. In contrast to all other known Cycloclasticus, the symbiotic Cycloclasticus lack the genes needed to degrade polycyclic aromatic hydrocarbons (PAH). Instead, these symbionts use oil-derived short-chain alkanes such as ethane and butane. We hypothesize that the symbiosis with Bathymodiolus allowed Cycloclasticus to forfeit the large suite of genes needed to degrade PAH and instead metabolize more easily degradable short-chain alkanes.
A final highlight of the insights we gained through BathyBiome, was our discovery of a remarkably high diversity of symbiont strains in Bathymodiolus. Single mussel individuals harbor as many as 16 symbiont strains that all belong to a single bacterial species. Such a high diversity of strains has not been previously observed in intracellular animal symbioses, and challenges common evolutionary theories that predict destabilization of mutualistic symbioses by symbiont strain diversity. We hypothesize that genetic differences between symbiont strains, such as genes that enable them to use different energy and carbon sources, provide a selective advantage to the mussels and promote strain diversity.
We gained our insights by using a wide range of methods, some of which we newly developed or refined for symbiosis-specific analyses, such as high throughput metagenomic and transcriptomic pipelines, or correlative imaging techniques combining fluorescence in situ hybridization with mass spectrometry imaging at micrometer scales with resolution levels down to single eukaryotic host cells. Many results are already published in high-ranking, peer-reviewed journals or submitted as manuscripts and available as online preprints, while a considerable share of our research is still in progress and will be published soon.