Morphology, Transcriptomics and In Vitro Model of Skin from Polar Cod (Boreogadus Saida) and Atlantic Cod (Gadus Morhua)

Abstract

Fish skin is a multifunctional barrier tissue with high regeneration capacity that interacts with the surrounding environment and provides protection. Functional importance, high complexity and activity make skin an attractive tissue for studying the effects of environmental challenges and chemical stressors in fish. The aim of this work was to characterize skin from polar cod (Boreogadus saida) and Atlantic cod (Gadus morhua), and to test cod skin as an in vitro model in exposure studies. Both species have similar skin structures including epidermis, mucous cells, club cells and scales. However, microarchitectural differences were detected; Atlantic cod has a smooth epidermal surface and overlapping scales, whereas polar cod has a folded outer surface and discontinuous scales. Genome-wide microarray found 6.5k genes with expression differences, which suggested more active turnover of proteins, proliferation and motility of cells in skin of polar cod. Hydrogen peroxide (H2O2) was used to examine skin responses. Transcriptome response was stronger in the skin of polar cod, with 155 differentially expressed genes. The skin from Atlantic cod was further used to develop a cell culture. H2O2 decreased the cell migration rate in a dose-dependent manner, which could indicate reduced skin healing capacity. The results revealed novel skin structures and confirmed that the skin from cod is a promising tissue for evaluation of stressors.

The Effect of Stress on the Skin Welfare of Lumpfish (Cyclopterus lumpus Linnaeus, 1758) Broodstock

“…These Q cells have also previously been referred to as vacuoles [39] or club cells and have been shown to vary in abundance, size and distribution between individuals, where the typical feature was numerous vacuoles layered in the epidermis for small fry (<5 g) and fewer, smaller and more dispersed vacuoles in larger fish (>50 g). Whether the observed variation in Q cells was associated with stress and varying environmental conditions was not investigated in the study of Ytteborg et al [24]. Overall, these previous observations on juvenile lumpfish (>50 g) are consistent with the picture from broodstock in the present study.…”

The Effect of Stress on the Skin Welfare of Lumpfish (Cyclopterus lumpus Linnaeus, 1758) Broodstock

“…These Q cells have also previously been referred to as vacuoles [39] or club cells and have been shown to vary in abundance, size and distribution between individuals, where the typical feature was numerous vacuoles layered in the epidermis for small fry (<5 g) and fewer, smaller and more dispersed vacuoles in larger fish (>50 g). Whether the observed variation in Q cells was associated with stress and varying environmental conditions was not investigated in the study of Ytteborg et al [24]. Overall, these previous observations on juvenile lumpfish (>50 g) are consistent with the picture from broodstock in the present study.…”

Climate change with increasing seawater temperature will challenge the health of farmed Atlantic Cod (Gadus morhua L.)

“…Further evaluating skin from the different temperature regimes showed reduced thickness of the epidermis, reduced number of sensory cells and increased number of club cells in the outer border of the epidermis of fish exposed to high temperature. Similar alterations in skin have previously been connected with increased stress response in Atlantic cod (Ytteborg et al, 2020), as well as in lumpfish (Cyclopterus lumpus) and salmon (Karlsen et al, 2021;Ytteborg et al, 2023). Interestingly, severe morphological changes in skin were not observed until the end of the trial, at week 8, indicating long term effects of 17°C and highlighting the importance of running temperature exposure trials for longer periods.…”

“…With increasing temperature and H 2 O 2 exposure, epidermis got more fragmented, keratocytes lost their defined structures of microridges, and detached from the continuous outermost epidermal layer, leaving breaches and exposed areas. Similar changes have already been shown after exposure to oxidative stress at low temperatures (Ytteborg et al, 2020), but it is of interest that elevated temperature worsened the effect of oxidative stress. The microridges have several functions in fish skin, i.e.…”

Long-Term Influence of PCB- and PBDE-Spiked Microplastic Spheres Fed through Rotifers to Atlantic Cod (Gadus morhua) Larvae

“…The skin had a rougher structure with detaching keratocytes in the outermost epidermal layer compared to the control group. A similar skin surface had previously been shown in cod exposed to oxidative stress, and it was indicated that this might weaken the barrier properties of the epidermis [28]). The morphology was further confirmed using SEM, where breaches between the individual keratocytes were found.…”

The Effect of Stress on the Skin Welfare of Lumpfish (Cyclopterus lumpus Linnaeus, 1758) Broodstock

“…These Q cells have also previously been referred to as vacuoles [39] or club cells and have been shown to vary in abundance, size and distribution between individuals, where the typical feature was numerous vacuoles layered in the epidermis for small fry (<5 g) and fewer, smaller and more dispersed vacuoles in larger fish (>50 g). Whether the observed variation in Q cells was associated with stress and varying environmental conditions was not investigated in the study of Ytteborg et al [24]. Overall, these previous observations on juvenile lumpfish (>50 g) are consistent with the picture from broodstock in the present study.…”

Climate change with increasing seawater temperature will challenge the health of farmed Atlantic Cod (Gadus morhua L.)

“…Further evaluating skin from the different temperature regimes showed reduced thickness of the epidermis, reduced number of sensory cells and increased number of club cells in the outer border of the epidermis of fish exposed to high temperature. Similar alterations in skin have previously been connected with increased stress response in Atlantic cod (Ytteborg et al, 2020), as well as in lumpfish (Cyclopterus lumpus) and salmon (Karlsen et al, 2021;Ytteborg et al, 2023). Interestingly, severe morphological changes in skin were not observed until the end of the trial, at week 8, indicating long term effects of 17°C and highlighting the importance of running temperature exposure trials for longer periods.…”

“…With increasing temperature and H 2 O 2 exposure, epidermis got more fragmented, keratocytes lost their defined structures of microridges, and detached from the continuous outermost epidermal layer, leaving breaches and exposed areas. Similar changes have already been shown after exposure to oxidative stress at low temperatures (Ytteborg et al, 2020), but it is of interest that elevated temperature worsened the effect of oxidative stress. The microridges have several functions in fish skin, i.e.…”

Long-Term Influence of PCB- and PBDE-Spiked Microplastic Spheres Fed through Rotifers to Atlantic Cod (Gadus morhua) Larvae

“…The skin had a rougher structure with detaching keratocytes in the outermost epidermal layer compared to the control group. A similar skin surface had previously been shown in cod exposed to oxidative stress, and it was indicated that this might weaken the barrier properties of the epidermis [28]). The morphology was further confirmed using SEM, where breaches between the individual keratocytes were found.…”

The Effect of Stress on the Skin Welfare of Lumpfish (Cyclopterus lumpus Linnaeus, 1758) Broodstock

“…These Q cells have also previously been referred to as vacuoles [39] or club cells and have been shown to vary in abundance, size and distribution between individuals, where the typical feature was numerous vacuoles layered in the epidermis for small fry (<5 g) and fewer, smaller and more dispersed vacuoles in larger fish (>50 g). Whether the observed variation in Q cells was associated with stress and varying environmental conditions was not investigated in the study of Ytteborg et al [24]. Overall, these previous observations on juvenile lumpfish (>50 g) are consistent with the picture from broodstock in the present study.…”

Climate change with increasing seawater temperature will challenge the health of farmed Atlantic Cod (Gadus morhua L.)

“…Further evaluating skin from the different temperature regimes showed reduced thickness of the epidermis, reduced number of sensory cells and increased number of club cells in the outer border of the epidermis of fish exposed to high temperature. Similar alterations in skin have previously been connected with increased stress response in Atlantic cod (Ytteborg et al, 2020), as well as in lumpfish (Cyclopterus lumpus) and salmon (Karlsen et al, 2021;Ytteborg et al, 2023). Interestingly, severe morphological changes in skin were not observed until the end of the trial, at week 8, indicating long term effects of 17°C and highlighting the importance of running temperature exposure trials for longer periods.…”

“…With increasing temperature and H 2 O 2 exposure, epidermis got more fragmented, keratocytes lost their defined structures of microridges, and detached from the continuous outermost epidermal layer, leaving breaches and exposed areas. Similar changes have already been shown after exposure to oxidative stress at low temperatures (Ytteborg et al, 2020), but it is of interest that elevated temperature worsened the effect of oxidative stress. The microridges have several functions in fish skin, i.e.…”

Long-Term Influence of PCB- and PBDE-Spiked Microplastic Spheres Fed through Rotifers to Atlantic Cod (Gadus morhua) Larvae

“…The skin had a rougher structure with detaching keratocytes in the outermost epidermal layer compared to the control group. A similar skin surface had previously been shown in cod exposed to oxidative stress, and it was indicated that this might weaken the barrier properties of the epidermis [28]). The morphology was further confirmed using SEM, where breaches between the individual keratocytes were found.…”