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Impact of Thermal Stress on Kidney-Specific Gene Expression in Farmed Regional and Imported Rainbow Trout

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Abstract

Seasonal water temperatures can be stressful for fish in aquaculture and can therefore negatively influence their welfare. Although the kidney is the crucial organ associated with the primary stress response, knowledge about the stress-modulated kidney transcriptome in salmonids is limited. In the present study, we used a comparative microarray approach to characterize the general gene expression profiles of rainbow trout trunk kidney after a 2-week acclimation to mild heat (23 °C) and cold stress (8 °C). Hypothesizing that local adaptation influences stress performance, we aimed to identify differences in the temperature-induced gene expression in the regional trout strain BORN, in addition to a common imported strain. Moderate temperature challenge provoked typical stress response clusters, including heat-shock proteins or cold-inducible factors, in addition to altered energy metabolism in trout kidney. Mild cold, in particular, enhanced renal protein degradation processes, as well as mRNA and protein synthesis, while it also triggered fatty acid biosynthesis. Mild heat led to cytoskeleton-stabilizing processes and might have facilitated cell damage and infection. Furthermore, both breeding lines used different strategies for energy provision, cellular defense, and cell death/survival pathways. As a main finding, the genes involved in energy provision showed generally higher transcript levels at both temperatures in BORN trout compared to imported trout, indicating adjusted metabolic rates under local environmental conditions. Altogether, this study provides a general overview of stress-induced transcriptional patterns in rainbow trout trunk kidney, in addition to identifying genes and networks that contribute to the robustness of the BORN strain. Our analyses suggest SERPINH1 and CIRBP as general marker genes for heat stress and cold stress in trout, respectively.

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Acknowledgments

The Campus bioFISCH-MV coordinated this work, and funding came from the European Fisheries Fund (EFF) and the Ministry of Agriculture, the Environment and Consumer Protection Mecklenburg-Western Pomerania (pilot project: Rainbow trout BORN). We kindly thank I. Hennings and B. Schöpel for expert technical assistance.

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  1. Tomáš Korytář

    Present address: Department of Pathobiology, School of Veterinary Medicine, University of Pennsylvania, 3800 Spruce street, Philadelphia, PA, USA

Authors and Affiliations

  1. Institute for Genome Biology, Leibniz Institute for Farm Animal Biology (FBN), Wilhelm-Stahl-Allee 2, 18196, Dummerstorf, Germany

    Marieke Verleih, Andreas Borchel, Alexander Rebl & Tom Goldammer

  2. Norwegian Institute of Food, Fisheries and Aquaculture Research (Nofima), Osloveien 1, NO-1430, Ås, Norway

    Aleksei Krasnov

  3. Institute of Immunology, Friedrich-Loeffler-Institute (FLI), Federal Research Institute for Animal Health, Südufer 10, 17493, Greifswald, Insel Riems, Germany

    Tomáš Korytář

  4. Institute for Fishery, State Research Centre for Agriculture and Fishery (LFA-MV), Fischerweg 408, 18096, Rostock, Germany

    Carsten Kühn

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  1. Marieke Verleih
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Correspondence to Tom Goldammer.

Electronic supplementary material

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Online Resource 1

Pooling and hybridization scheme of samples used for analysis by 4×44K Salmon Gene Expression Microarray slides (Agilent Technologies). Determined gender (♀,♂) is given for each fish used in this study. (XLSX 13 kb)

Online Resource 2

Primers used in this study. (DOCX 29 kb)

Online Resource 3

Overview of all temperature-regulated genes in the rainbow trout kidney (fold change ≥3; bonferroni-corrected p-value ≤0.05).Genes discussed or mentioned in the manuscript are underlined in black. (XLSX 101 kb)

Online Resource 4

Number of (A) heat- and cold-induced and (B)strain-specific array-predicted features in BORN and imported trout. (XLSX 10 kb)

Online Resource 5

Overview of annotated genes grouped by their cellular functions (fold change ≥3; bonferroni-corrected p-value ≤0.05). The genes discussed or mentioned in the manuscript are underlined in black. (XLSX 60 kb)

Online Resource 6

Expression ratios of microarray-predicted candidate genes between 15°C and challenging temperatures of 8°C (15°C/8°C) or 23°C (15°C/23°C), as well as ratios between imported trout and BORN trout at 15°C (Import/BORN). Data are given as fold changes (FC) with their respective significant levels (p-values). (DOCX 37 kb)

Online Resource 7

Potential interaction of temperature-regulated genes (bold letters, shaded in red) involved in cell death in BORN (a) and imported trout (b). IPA (Ingenuity® Systems, www.ingenuity.com) generated networks. Full and broken lines indicate direct or indirect interactions, respectively. Arrows specify the orientation of regulations. (GIF 330 kb)

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Verleih, M., Borchel, A., Krasnov, A. et al. Impact of Thermal Stress on Kidney-Specific Gene Expression in Farmed Regional and Imported Rainbow Trout. Mar Biotechnol 17, 576–592 (2015). https://doi.org/10.1007/s10126-015-9640-1

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