Microbiome inception: an intestinal cestode shapes a hierarchical landscape of distinct microbial communities nested within the host

Background. Cestodes represent major health concerns for both human and animal populations. As intestinal parasites, cestodes share space with the gut microbiome of their primary hosts. There is growing recognition that such parasitic helminths can harbour an internal endomicrobiome, creating a system of nested microbiomes within the primary host. However, how the cestode and its associated microorganisms interact with the host gut microbiome remains unclear, as do the consequences of these interactions for host health. Material and Methods. In the first such study performed in a cestode, we characterised the microbial communities in an intestinal parasite, a cestode of the genus Eubothrium, and its primary host, Atlantic salmon (Salmo salar). We sampled the host gut mucosa, the surface of the cestode (the tegument) and the cestode endomicrobiome in 30 sea-farmed, harvest-aged salmon and characterised the microbiomes with 16S amplicon and shotgun metagenomics sequencing. Results. Cestode presence altered the salmon gut microbiome, with an increase in putative pathobionts and a decrease in the dominating commensal Mycoplasma phylotypes. The cestode also carried a distinct endomicrobiome, while the tegument included bacteria from both the cestode and the salmon microbiomes. Shotgun metagenomics revealed distinct Mycoplasma phylotypes in the cestode endomicrobiome with functional potential that differed from the Mycoplasma phylotypes abundant in the salmon gut. Conclusion. Our results indicate that cestode infection is associated with gut dysbiosis in the salmon host, by simultaneously serving as a potential source of novel bacterial species, as well as a selective force benefiting putative pathogens. Our study highlights the importance of taking a hologenomic approach to understanding parasite infections, where the parasite and its associated microorganisms are considered as a holobiont nested within the host holobiont, with combined effects on the host microbiome and overall host health.