Investigation of Capitella spp. symbionts in the context of varying anthropic pressures: First occurrence of a transient advantageous epibiosis with the giant bacteria Thiomargarita sp. to survive seasonal increases of sulfides in sediments.

Capitella spp. is considered as an important ecological indicator of eutrophication due to its high densities in organic-rich, reduced, and sometimes polluted coastal ecosystems. We investigated whether such ability to cope with adverse ecological contexts might be a response to the microorganisms these worms are associated with. In populations from the French Atlantic coast (Roscoff, Brittany), we observed an epibiotic association covering the tegument of 20-30% specimens from an anthropized site while individuals from a reference, non-anthropized site were devoid of any visible epibionts. Using RNAseq, molecular and microscopic analyses, we described and compared the microbial communities associated with the epibiotic versus the non-epibiotic specimens at both locations. Interestingly, data showed that the epibiosis is characterized by sulfur-oxidizing bacteria among which the giant bacterium Thiomargarita sp., to date only described in deep sea habitats. Survey of Capitella combined with the geochemical analysis of their sediment revealed that epibiotic specimens are always found in muds with the highest concentration of sulfides, mostly during the summer. Concomitantly, tolerance tests demonstrated that the acquisition of epibionts increased survival against toxic level of sulfides. Overall, the present data highlight for the first time a peculiar plastic adaptation to seasonal variations of the habitat based on a transcient epibiosis allowing a coastal species to survive temporary harsher conditions.