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Transcriptomic profiling and IgM and IgT repertoire dynamics in rainbow trout gills following primary and secondary challenge with Lactococcus petauri

ABSTRACT: Fish mucosal tissues lack the organized lymphoid structures present in mammals. Although this is also true for the gills, with the gill-associated lymphoid tissue (GIALT) being mainly composed of B and T cells scattered throughout the epithelium and the lamellae, in some species such as rainbow trout (Oncorhynchus mykiss) or Atlantic salmon (Salmo salar), a more organized structure designated as the interbranchial lymphoid tissue (ILT) is also identified. Yet, although many studies have investigated the immune response of the gill to stimulation or pathogen encounter, which have revealed the activation of both innate and adaptive immune elements, how the gills respond to secondary stimulation or whether memory responses are locally orchestrated is still unknown. To provide insights into this matter, in the current study, we have infected rainbow trout by bath with Lactococcus petauri and then re-infected or mock-infected the survivor fish as well as mock-infected controls. At day 4 after the last infection, the fish were sacrificed and gills used to perform an RNAseq transcriptomic analysis and an IgM and IgT repertoire analysis. The number of cells secreting total and specific IgM in gills was also established by ELIspot. Our results demonstrate that memory responses are locally organized in the rainbow trout gills, given that re-infected fish did not up-regulate genes related to inflammation (as happens in the primary infection), but preferentially modified genes related to adaptive immunity, mainly to B cell function, experiencing a significant IgM and IgT clonal expansion. Accordingly, re-infected fish produced increased levels of specific IgM both locally and in serum, although no clonal selection was apparent. These findings advance our understanding of mucosal immunological memory in teleost fish and reveal the gills as a site of localized adaptive immune regulation during secondary responses.

ORGANISM(S): Oncorhynchus mykiss

PROVIDER: GSE328875 | GEO | 2026/06/14

REPOSITORIES: GEO

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Project description:Rainbow trout (Oncorhynchus mykiss), an important economically fish with high food value in China, is very sensitive to hypoxia. The gills are the first tissue to be attacked after hypoxia stress. However, the regulatory mechanisms in gills of rainbow trout to moderate and severe hypoxia stress are unclear. In this study, we determined the changes of biochemical parameters and gene expression in gills of rainbow trout during different periods of hypoxia (4, 8, 12, 24 h, and 1 month) and reoxygenation for 24 h, and analyzed the tissue and transcriptomic changes under moderate hypoxia for 12 h (Tm12G) and severe hypoxia for 12 h (Ts12G) compared with control (CG). The results showed that gill lamellae were bent and ILCM was reduced in the Tm12G group, while this phenomenon was more pronounced in the Ts12G group. At one month of hypoxia, we found that the gill lamellae epithelium was detached. Based on biochemical parameters and transcriptomic analysis, we found that the antioxidant and immune responses were activated, and glucose metabolism, lipid metabolism, and amino acid metabolism were enhanced, however, vitamin metabolism was suppressed under moderate hypoxia stress. Antioxidant and immune responses were activated, and glucose metabolism, lipid metabolism, and amino acid metabolism were enhanced, and nucleotide metabolism also was activated under severe hypoxia stress. From the analysis of gene expression pattern, we found that the expression of hsp90a, tnf, caspase3, mgst1, fih1, hif1a, ddit4, and egln3 showed a tendency to increase and then decrease and recovered after reoxygenation under moderate and severe hypoxia stress. Except for mgst1, the expression of other genes was significantly higher than the control at 12 h of stress. Under hypoxia stress, antioxidant and metabolic responses were first elevated and then decreased with time, and metabolic and immune pathways were activated, which coordinated with each other in response to hypoxia stress. These results provide basic information for an in-depth investigation of the physiological and molecular mechanisms in gills of rainbow trout under hypoxia stress.

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Transcriptomic profiling and IgM and IgT repertoire dynamics in rainbow trout gills following primary and secondary challenge with Lactococcus petauri

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