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.
The authors thank all of the animal staff at Kårvik havbruksstasjonen for their expert care of the research animals, and the University of Manchester Genomics Technology core facility (UK) for performing chromium 10x library preparation for snRNAseq. We also thanks the reviewers for their constructive comments on the original manuscript
AW is supported by the Tromsø forskningsstiftelse (TFS) grant awarded to DH (TFS2016DH). The Sentinel North Transdisciplinary Research Program Université Laval and UiT awarded to DH supports this work. SW is supported a grant from the Tromsø forskningsstiftelse (TFS) starter grant TFS2016SW. Experimental costs were covered by HFSP grant “Evolution of seasonal timers” RGP0030/2015 awarded to AL and DH. Storage resources were provided by the Norwegian National Infrastructure for Research Data (NIRD, project NS9055K).
- Atlantic salmon (Salmo salar)
- immune cells
- single nuclei RNA sequencing