Interactions Between Gilthead Seabream Intestinal Transcriptome and Microbiota Upon Enteromyxum Leei Infection: a Multi-omic Approach

Background: The enteric myxozoan parasite Enteromyxum leei is an important problem in gilthead seabream aquaculture invading the intestinal epithelium and leading to chronic intestinal inflammation, poor food conversion rates, cachexia, and mortalities, with no treatments available, resulting in significant economic losses. It is known that myxozoan infections are affected by factors such as temperature, duration of exposure, stocking densities, and seasonality. Gut microbiota has key effects on host health, including disease resistance and immune system training and development, tightly interacting with the host, affecting systemic and local physiological functions. This study aimed to gain insights into the host-microbiota-parasite interactions integrating metataxonomics, host transcriptomics, and metatranscriptomics within this disease model.

Results: Exposure to E. leei together with temperature and age differences led to alterations in gilthead seabream intestinal microbiota. Samples from 240 g fish kept at 18ºC during a winter trial at 10 weeks post-parasite exposure showed the highest significant changes in their microbial composition with Proteobacteria increasing in abundance from 32.3% in the control group up to 89.8% in the infected group, while Firmicutes and Actinobacteria significantly decreased in relative abundance from 23% and 37.8-2.4% and 1.1%, respectively. After LEfSe analysis, Acinetobacter was identified as the best biomarker for the parasite-exposed group. Parasite exposure also altered the expression of 935 host genes, highlighting genes involved in immune responses such as pathways related to Interleukins, MHCI and Interferons. Microbial transcripts, also showed significant changes upon parasite infection. Integration of the results revealed differential effects on the host induced directly by the parasite or indirectly by parasite-induced microbial shift.

Conclusions: Intestinal microbiota and local host gene expression showed significant changes upon en enteromyxosis. The detected activation of the host immune response was not exclusively linked to the parasite infection but also to changes in microbiota, demonstrating the key role of the different components of the mucosal system during disease. These results provided different datasets of bacterial taxa and microbial and host transcripts that will allow a better understanding of host-microbiota-parasite interactions and can serve as starting points for studying and evaluating mucosal health in aquaculture during parasitosis or other diseases.