Symmetry of tissue-specific immune expression and microbiota profiles across mucosal tissues of Atlantic salmon (Salmo salar) highlight host-microbe coadaptations that are marginally perturbed by functional feeds

Authors: BLEDSOE, JACOB - University Of Idaho; Pietrak, Michael; Burr, Gary; Peterson, Brian; SMALL, BRIAN - University Of Idaho

Submitted to: Animal Microbiome
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/20/2022
Publication Date: 3/11/2022
Citation: Bledsoe, J.W., Pietrak, M.R., Burr, G.S., Peterson, B.C., Small, B.C. 2022. Symmetry of tissue-specific immune expression and microbiota profiles across mucosal tissues of Atlantic salmon (Salmo salar) highlight host-microbe coadaptations that are marginally perturbed by functional feeds. Animal Microbiome. https://doi.org/10.1186/s42523-022-00173-0.
DOI: https://doi.org/10.1186/s42523-022-00173-0.

Interpretive Summary: Mucosal surfaces of fish provide cardinal defense against environmental pathogens and toxins, yet these external mucosa are also responsible for maintaining and regulating beneficial microbiota. To better our understanding of interactions between host and microbiota in finfish and how those interactions may vary by mucosal tissue, we used an integrative approach to characterize and compare immune biomarkers and microbiota across three mucosal tissues (skin, gill, and gut) in Atlantic salmon fed either a control or diets supplemented with mannooligosaccharides, coconut oil, or both. Impacts of functional feeds on mucosal immunity were further evaluated through an experimental challenge with ectoparasitic salmon louse. Fish grew 288.2 g to a final size of 646.5 g during the 12-week trial, with no dietary differences in growth. Bacterial richness and diversity were reduced in the gut compared to skin and gill, with dietary effects detected on richness, but not diversity. Microbiota communities clustered separately by tissue, yet dietary impacts on phylogenetic composition were only detected among skin samples. Predicted metagenomic gene-level functions showed significant concordance with bacterial phylogeny, though when summarized as pathways, functions were highly conserved. Although, key metagenomic pathways related to the physiology of each tissue were identified as enriched among the microbiota present in the corresponding mucosa. Host immune expression profiles showed tissue specific signatures, though dietary treatments also influenced gene expression within each tissue and in peripheral blood leukocytes. Mapping host immune expression profiles to microbiota composition indicated a highly significant correlation in sample ordinations across tissues. Despite differences in skin microbiota and gene expression, diets had no effect on parasitic salmon louse counts or density. Effects of functional feed ingredients were minor and primarily relegated to alterations in host expression profiles, although mucosal tissues showed differences in immune regulation with corresponding differences in bacterial phylogeny. Inferred metagenomic pathways showed greater conservation across mucosal tissue, though adaptive metagenomic functions related to the physiology of each tissue were also detected. Symmetry in ordinations of host and microbiota samples suggests mucosal immune regulation and microbiota composition have coadapted in a tissue-specific manner.

Technical Abstract: Background: Mucosal surfaces of fish provide cardinal defense against environmental pathogens and toxins, yet these external mucosa are also responsible for maintaining and regulating beneficial microbiota. To better our understanding of interactions between host and microbiota in finfish and how those interactions may vary by mucosal tissue, we used an integrative approach to characterize and compare immune biomarkers and microbiota across three mucosal tissues (skin, gill, and gut) in Atlantic salmon fed either a control or diets supplemented with mannooligosaccharides, coconut oil, or both. Impacts of functional feeds on mucosal immunity were further evaluated through an experimental challenge with ectoparasitic salmon louse. Results: Fish grew 288.2 g ± 38.3 (mean ± SD) to a final size of 646.5 g ± 35.8 during the 12-week trial, with no dietary differences in growth. Bacterial richness and diversity were reduced in the gut compared to skin and gill, with dietary effects detected on richness, but not diversity. Microbiota communities clustered separately by tissue, yet dietary impacts on phylogenetic composition were only detected among skin samples. Predicted metagenomic gene-level functions showed significant concordance with bacterial phylogeny, though when summarized as pathways, functions were highly conserved. Although, key metagenomic pathways related to the physiology of each tissue were identified as enriched among the microbiota present in the corresponding mucosa. Host immune expression profiles showed tissue specific signatures, though dietary treatments also influenced gene expression within each tissue and in peripheral blood leukocytes. Mapping host immune expression profiles to microbiota composition indicated a highly significant correlation in sample ordinations across tissues. Despite differences in skin microbiota and gene expression, diets had no effect on parasitic salmon louse counts or density. Conclusions: Effects of functional feed ingredients were minor and primarily relegated to alterations in host expression profiles, although mucosal tissues showed differences in immune regulation with corresponding differences in bacterial phylogeny and KEGG function. Inferred metagenomic pathways showed greater conservation across mucosal tissue, though adaptive metagenomic functions related to the physiology of each tissue were also detected. Symmetry in ordinations of host and microbiota samples suggests mucosal immune regulation and microbiota composition have coadapted in a tissue-specific manner.