Abstract
The shallow water bivalve Codakia orbicularis lives in symbiotic association with a sulfur-oxidizing bacterium in its gills. The endosymbiont fixes CO2 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.
Highlights
Mutualistic associations between marine invertebrates and sulfur-oxidizing bacteria are a well-documented and widespread phenomenon in a variety of sulfidic habitats ranging from hydrothermal vents to shallow-water coastal ecosystems[1,2,3]
To reconstruct the C. orbicularis symbiont’s metabolism, we sequenced the genome of purified bacteria to provide a basis for subsequent global proteomic analyses
The respective enzymes were expressed in high concentrations, as detected at the protein level
Summary
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[1,2,3]. Symbiotic nitrogen-fixers are known to be associated with a variety of invertebrates, such as wood-boring bivalves (shipworms)[19], corals, sponges and sea urchins[20] Coastal seagrass beds, such as those inhabited by Codakia species, are areas of high microbial nitrogen fixation activity[14], as the plants’ rhizosphere is densely populated by a complex diazotrophic bacterial community[22,23]. We show, in a combined proteogenomic and experimental approach, that the thioautotrophic gill endosymbiont of C. orbicularis, ‘Candidatus Thiodiazotropha endolucinida’, expresses nitrogen fixation proteins and exhibits nitrogenase activity under its natural ambient conditions in the host This finding adds a novel feature to the picture of the Codakia symbiosis and enhances our understanding of its role in the seagrass ecosystem
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