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A single nuclei transcriptomic analysis of the Atlantic salmon gill through smoltification and seawater transfer

View ORCID ProfileAlexander C. West, Yasutaka Mizoro, Shona H. Wood, Louise Ince, Marianne Iversen, Even H. Jørgensen, Torfinn Nome, Simen Rød Sandve, Andrew S. I. Loudon, David G. Hazlerigg
doi: https://doi.org/10.1101/2020.09.03.281337
Alexander C. West
1Arctic Chronobiology and Physiology, University of Tromsø, 9019 Tromsø, Norway
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  • ORCID record for Alexander C. West
Yasutaka Mizoro
2Unit of Animal Genomics, GIGA Institute, University of Liège, Liège, Belgium
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Shona H. Wood
1Arctic Chronobiology and Physiology, University of Tromsø, 9019 Tromsø, Norway
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Louise Ince
3University of Geneva, Centre Médical Universitaire (CMU), Department of Pathology and Immunology, Switzerland
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Marianne Iversen
1Arctic Chronobiology and Physiology, University of Tromsø, 9019 Tromsø, Norway
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Even H. Jørgensen
1Arctic Chronobiology and Physiology, University of Tromsø, 9019 Tromsø, Norway
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Torfinn Nome
4Centre for Integrative Genetics, Department of Animal and Aquaculture Sciences, Norwegian University of Life Sciences, 1432 Ås, Norway
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Simen Rød Sandve
4Centre for Integrative Genetics, Department of Animal and Aquaculture Sciences, Norwegian University of Life Sciences, 1432 Ås, Norway
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Andrew S. I. Loudon
3University of Geneva, Centre Médical Universitaire (CMU), Department of Pathology and Immunology, Switzerland
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David G. Hazlerigg
1Arctic Chronobiology and Physiology, University of Tromsø, 9019 Tromsø, Norway
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  • For correspondence: david.hazlerigg@uit.no
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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, the extending photoperiods of spring stimulates smoltification, typified by radical reprogramming of the gill from an ion-absorbing organ to ion-excreting organ. Prior work has highlighted the role of specialized “mitochondrion-rich” cells in delivering this phenotype. However, transcriptomic studies identify thousands of smoltification-driven differentially regulated genes, indicating that smoltification causes a multifaceted, multicellular change; but direct evidence of this is lacking.

Here, we use single-nuclei RNAseq to characterize the Atlantic salmon gill during smoltification and seawater transfer. We identify 20 distinct clusters of nuclei, including known, but also novel gill cell types. These data allow us to isolate cluster-specific, smoltification-induced changes in gene expression. We also show how 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 a reduction of several immune-related cells. Overall, our results provide unrivaled detail of the cellular complexity in the gill, and suggest that smoltification triggers unexpected immune reprogramming directly preceding seawater entry.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted September 03, 2020.
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A single nuclei transcriptomic analysis of the Atlantic salmon gill through smoltification and seawater transfer
Alexander C. West, Yasutaka Mizoro, Shona H. Wood, Louise Ince, Marianne Iversen, Even H. Jørgensen, Torfinn Nome, Simen Rød Sandve, Andrew S. I. Loudon, David G. Hazlerigg
bioRxiv 2020.09.03.281337; doi: https://doi.org/10.1101/2020.09.03.281337
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A single nuclei transcriptomic analysis of the Atlantic salmon gill through smoltification and seawater transfer
Alexander C. West, Yasutaka Mizoro, Shona H. Wood, Louise Ince, Marianne Iversen, Even H. Jørgensen, Torfinn Nome, Simen Rød Sandve, Andrew S. I. Loudon, David G. Hazlerigg
bioRxiv 2020.09.03.281337; doi: https://doi.org/10.1101/2020.09.03.281337

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