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Differential Gene Expression in Liver, Gill, and Olfactory Rosettes of Coho Salmon (Oncorhynchus kisutch) After Acclimation to Salinity

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Abstract

Most Pacific salmonids undergo smoltification and transition from freshwater to saltwater, making various adjustments in metabolism, catabolism, osmotic, and ion regulation. The molecular mechanisms underlying this transition are largely unknown. In the present study, we acclimated coho salmon (Oncorhynchus kisutch) to four different salinities and assessed gene expression through microarray analysis of gills, liver, and olfactory rosettes. Gills are involved in osmotic regulation, liver plays a role in energetics, and olfactory rosettes are involved in behavior. Between all salinity treatments, liver had the highest number of differentially expressed genes at 1616, gills had 1074, and olfactory rosettes had 924, using a 1.5-fold cutoff and a false discovery rate of 0.5. Higher responsiveness of liver to metabolic changes after salinity acclimation to provide energy for other osmoregulatory tissues such as the gills may explain the differences in number of differentially expressed genes. Differentially expressed genes were tissue- and salinity-dependent. There were no known genes differentially expressed that were common to all salinity treatments and all tissues. Gene ontology term analysis revealed biological processes, molecular functions, and cellular components that were significantly affected by salinity, a majority of which were tissue-dependent. For liver, oxygen binding and transport terms were highlighted. For gills, muscle, and cytoskeleton-related terms predominated and for olfactory rosettes, immune response-related genes were accentuated. Interaction networks were examined in combination with GO terms and determined similarities between tissues for potential osmosensors, signal transduction cascades, and transcription factors.

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Acknowledgments

This work was supported by the University of Washington Superfund Research Program (NIEHS P42ES04696) and the University of California, Riverside Agricultural Experiment Station (RSAP). L.A.M. was supported by a National Research Service Award Institutional Training Grant (T32 ES018827). GH gratefully acknowledges support from National Institutes of Health grants DK063491, CA023100, and DK080506 and UC Senate grant RK126H-HARDIMAN. We would also like to thank Dr. Roman Sasik from The University of California, San Diego, for his help with this project.

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Authors and Affiliations

  1. Department of Environmental Sciences, University of California, 2258 Geology Building, 900 University Ave, Riverside, CA, 92521, USA

    Lindley A. Maryoung, Ramon Lavado & Daniel Schlenk

  2. Department of Environmental and Occupational Health Sciences, University of Washington, Seattle, WA, 98195, USA

    Theo K. Bammler, Evan P. Gallagher, Patricia L. Stapleton, Richard P. Beyer & Federico M. Farin

  3. Department of Medicine and Public Health and Center for Genomics Medicine, Medical University of South Carolina, 135 Cannon Street, Suite 303 MSC 835, Charleston, SC, 29425, USA

    Gary Hardiman

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  1. Lindley A. Maryoung
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Correspondence to Lindley A. Maryoung.

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Supplemental Figure 1

Interaction network pathway using MetaCore™ knowledge base (Bugrim et al. 2004) for liver comparing freshwater acclimated fish to fish acclimated to high (32 ppth) salinity using a 1.75 fold cutoff. Blue signifies down regulation and red signifies upregulation. A link show an interaction, a bullet is binding of protein products, an arrow mean regulation of transcription or activation, and a hammer means inhibition or deactivation. (JPEG 1112 kb)

Supplemental Figure 2

Interaction network pathway using MetaCore™ knowledge base (Bugrim et al. 2004) for gills comparing freshwater acclimated fish to fish acclimated to high (32 ppth) salinity using a 1.50 fold cutoff. Blue signifies down regulation and red signifies upregulation. A link show an interaction, a bullet is binding of protein products, an arrow mean regulation of transcription or activation, and a hammer means inhibition or deactivation. (EPS 21881 kb)

High resolution image (GIF 166 kb)

Supplemental Figure 3

Interaction network pathway using MetaCore™ knowledge base (Bugrim et al. 2004) for olfactory rosettes comparing freshwater acclimated fish to fish acclimated to high (32 ppth) salinity using a 1.25 fold cutoff. Blue signifies down regulation and red signifies upregulation. A link show an interaction, a bullet is binding of protein products, an arrow mean regulation of transcription or activation, and a hammer means inhibition or deactivation. (GIF 714 kb)

High resolution image (EPS 5455 kb)

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Maryoung, L.A., Lavado, R., Bammler, T.K. et al. Differential Gene Expression in Liver, Gill, and Olfactory Rosettes of Coho Salmon (Oncorhynchus kisutch) After Acclimation to Salinity. Mar Biotechnol 17, 703–717 (2015). https://doi.org/10.1007/s10126-015-9649-5

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