Investigation of the Bathymodiolus symbiosis at the Mid-Atlantic Ridge - from environment to host and symbionts

Deep-sea mussels from a hybrid zone on the Mid-Atlantic Ridge host genetically indistinguishable symbionts

The composition and diversity of animal microbiomes is shaped by a variety of factors, many of them interacting, such as host traits, the environment, and biogeography. Hybrid zones, in which the ranges of two host species meet and hybrids are found, provide natural experiments for determining the drivers of microbiome communities, but have not been well studied in marine environments. Here, we analysed the composition of the symbiont community in two deep-sea, Bathymodiolus mussel species along their known distribution range at hydrothermal vents on the Mid-Atlantic Ridge, with a focus on the hybrid zone where they interbreed. In-depth metagenomic analyses of the sulphur-oxidising symbionts of 30 mussels from the hybrid zone, at a resolution of single nucleotide polymorphism analyses of ~2500 orthologous genes, revealed that parental and hybrid mussels have genetically indistinguishable symbionts. While host genetics does not appear to affect symbiont composition in these mussels, geographic location of the mussels on the Mid-Atlantic Ridge explained 45 % of symbiont genetic variability based on redundancy analyses. We hypothesize that geographic structuring of the free-living symbiont population plays a major role in driving the composition of the microbiome in these deep-sea mussels.

Life outside the host – on the free-living stage of horizontally transmitted symbionts of the deep-sea mussel Bathymodiolus

In marine animal-microbe symbioses, horizontal transmission is the most common way of symbiont transfer between host generations. The sulphur-oxidising symbionts of the deep-sea mussel Bathymodiolus, one of the most successful fauna at hydrothermal vents worldwide, are one of the associations that undergo horizontal transmission. Despite the importance of the free-living stage on the symbiosis, only a few studies investigated the symbionts in the surrounding seawater, and their geographic distribution is unresolved. In our study, we analysed in-situ filtered seawater samples from seven vent sites along the northern Mid-Atlantic Ridge. We used phylogenetic analyses and screened for small ribosomal subunits and marker genes to resolve the diversity of free-living bacteria surrounding the mussels and the geographic distribution of different symbiont subspecies in the water column. We found a high diversity of bacteria that are closely related to Bathymodiolus symbionts, which contrasts the low diversity community within the mussel gills and highlights the specificity of the association. Our results revealed that symbiont DNA was present in the water column and co-occurred with mussel DNA, suggesting a symbiont transmission via host material. We established a workflow to find marker genes specific to symbiont subspecies and found that their distribution in water metagenomes resembled the distribution observed in mussel metagenomes. Our results point towards a scenario, in which all symbiont subspecies might be everywhere but only one dominant type occurs in higher abundance. Our study provides further insights into the free-living stage of Bathymodiolus symbionts, discusses concepts of horizontal transmission in this symbiosis and provides suggestions for future sampling campaigns.

Contacts: Merle Ücker, Nicole Dubilier