Bathymodiolin mussels occur at hydrothermal vents and cold seeps, where they thrive thanks to symbiotic associations with chemotrophic bacteria. Closely related genera Idas and Adipicola are associated with organic falls, ecosystems that have been suggested as potential evolutionary 'stepping stones' in the colonization of deeper and more sulphide-rich environments. Such a scenario should result from specializations to given environments from species with larger ecological niches. This study provides molecular-based evidence for the existence of two mussel species found both on sunken wood and bones. Each species specifically harbours one bacterial phylotype corresponding to thioautotrophic bacteria related to other bathymodiolin symbionts. Phylogenetic patterns between hosts and symbionts are partially congruent. However, active endocytosis and occurrences of minor symbiont lineages within species which are not their usual host suggest an environmental or horizontal rather than strictly vertical transmission of symbionts. Although the bacteria are close relatives, their localization is intracellular in one mussel species and extracellular in the other, suggesting that habitat choice is independent of the symbiont localization. The variation of bacterial densities in host tissues is related to the substrate on which specimens were sampled and could explain the abilities of host species to adapt to various substrates.
The shallow water bivalve Codakia orbicularis lives in symbiotic association with a sulfur-oxidizing bacterium in its gills. The endosymbiont fixes CO 2 and thus generates organic carbon compounds, which support the host's growth. To investigate the uncultured symbiont's metabolism and symbiont-host interactions in detail we conducted a proteogenomic analysis of purified bacteria. Unexpectedly, our results reveal a hitherto completely unrecognized feature of the C. orbicularis symbiont's physiology: the symbiont's genome encodes all proteins necessary for biological nitrogen fixation (diazotrophy). Expression of the respective genes under standard ambient conditions was confirmed by proteomics. Nitrogenase activity in the symbiont was also verified by enzyme activity assays. Phylogenetic analysis of the bacterial nitrogenase reductase NifH revealed the symbiont's close relationship to free-living nitrogen-fixing Proteobacteria from the seagrass sediment. The C. orbicularis symbiont, here tentatively named 'Candidatus Thiodiazotropha endolucinida', may thus not only sustain the bivalve's carbon demands. C. orbicularis may also benefit from a steady supply of fixed nitrogen from its symbiont-a scenario that is unprecedented in comparable chemoautotrophic symbioses. Mutualistic associations between marine invertebrates and sulfur-oxidizing (thiotrophic) bacteria are a well-documented and widespread phenomenon in a variety of sulfidic habitats ranging from hydrothermal vents to shallow-water coastal ecosystems 1-3 . Thioautotrophic symbionts generate energy through sulfide oxidation and provide their hosts with organic carbon. In the Lucinidae, a diverse family of marine bivalves, all members are obligatorily dependent on their bacterial gill endosymbionts after larval development and metamorphosis 4 . The shallowwater lucinid Codakia orbicularis, which lives in the sediment beneath the tropical seagrass Thalassia testudinum along the Caribbean and Western Atlantic coast 5 , harbours a single species of endosymbionts in its gills 6 . The symbiont has been shown to be newly acquired by each clam generation 7,8 from a pool of freeliving symbiosis-competent bacteria in the environment 9 , rather than being inherited from clam parents. C. orbicularis appears not to release its endosymbionts, even under adverse conditions, but can digest them as a source of nutrition [10][11][12] . Moreover, bacterial cell division seems to be inhibited inside the host tissue. The majority of the symbiont population was shown to be polyploid (that is, containing multiple genome copies), while dividing symbiont cell stages are very rarely observed in host bacteriocytes 13 . The host undoubtedly benefits from the symbiont both by way of detoxification of its sulfidic environment and by supply of organic compounds through the bacterial Calvin-Benson cycle. It remains questionable, however, whether the symbiont gains any advantage from this association in evolutionary terms 11 .Biological nitrogen fixation (diazotrophy) is the conversion of ...
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