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Immunologic Profiling of the Atlantic Salmon Gill by Single Nuclei Transcriptomics.

ABSTRACT: Anadromous salmonids begin life adapted to the freshwater environments of their natal streams before a developmental transition, known as smoltification, transforms them into marine-adapted fish. In the wild, smoltification is a photoperiod-regulated process, involving radical remodeling of gill function to cope with the profound osmotic and immunological challenges of seawater (SW) migration. While prior work has highlighted the role of specialized "mitochondrion-rich" cells (MRCs) and accessory cells (ACs) in delivering this phenotype, recent RNA profiling experiments suggest that remodeling is far more extensive than previously appreciated. Here, we use single-nuclei RNAseq to characterize the extent of cytological changes in the gill of Atlantic salmon during smoltification and SW transfer. We identify 20 distinct cell clusters, including known, but also novel gill cell types. These data allow us to isolate cluster-specific, smoltification-associated changes in gene expression and to describe how the cellular make-up of the gill changes through smoltification. As expected, we noted an increase in the proportion of seawater mitochondrion-rich cells, however, we also identify previously unknown reduction of several immune-related cell types. Overall, our results provide fresh detail of the cellular complexity in the gill and suggest that smoltification triggers unexpected immune reprogramming.

SUBMITTER: West AC

PROVIDER: S-EPMC8129531 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Various agents including Ca. Piscichlamydia salmonis, Ca. Branchiomonas cysticola, Desmozoon lepeophtherii, Paramoeba perurans and salmon gill poxvirus may be associated with complex gill disease in Atlantic salmon. Co-infections involving two or more of these agents are common and histopathological interpretation of lesions is therefore challenging. In this study, we developed a semi-quantitative scoring system for examination of histopathological gill lesions in sea-farmed Atlantic salmon suffering from gill disease. Following qPCR analysis of gills sampled for Ca. P. salmonis, Ca. B. cysticola, D. lepeophtherii and P. perurans from 22 geographically spread outbreaks, five cases representing different infectious loads and combinations of agents were chosen for histopathological scoring. Twenty-eight histological features were evaluated and potential associations between individual pathological changes and the occurrence of individual agents studied. The inter-observer agreement in interpretation of histological parameters between the three pathologists involved, was calculated to validate robustness of the scoring scheme. Seventeen histological parameters met the criteria for inter-observer agreement analysis and were included in the calculation. The three most frequent findings were identification of subepithelial leukocytes, epithelial cell hyperplasia and mucus cell hyperplasia. While few findings could be specifically related to particular agents, necrosis in hyperplastic lesions, pustules and necrosis of subepithelial cells appeared to be associated with the presence of Ca. B. cysticola. Further, lesion profiles clearly support the previously identified association between P. perurans and pathological changes associated with AGD. Very few pathological changes were observed in the single case in which Ca. P. salmonis was the dominating agent. Some lesions were only very rarely observed e.g. chloride cell necrosis, epithelial cell apoptosis, lamellar deposition of melanin and haemophagocytosis. The scoring scheme developed and applied was robust and sensitive. A less extensive scheme for routine diagnostic use is proposed.

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Immunologic Profiling of the Atlantic Salmon Gill by Single Nuclei Transcriptomics.

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