Atlantic salmon (Salmo salar) mounts systemic and mucosal stress responses to peracetic acid

Malene Soleng, Lill-Heidi Johansen, Hanne Johnsen, Gunhild S Johansson, Mette W Breiland, Lisbeth Rørmark, Karin Pittman, Lars-Flemming Pedersen, Carlo Cabacang Lazado*

*Corresponding author for this work

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Abstract

Peracetic acid (PAA), a strong organic peroxide, is considered a relatively sustainable disinfectant in aquaculture because of its broad effectivity against many pathogens at low concentrations and because it degrades spontaneously to harmless residues. The impacts of PAA on fish health must be determined before its use as either a routine disinfectant or chemotherapeutant. Here we investigated the systemic and mucosal stress responses of Atlantic salmon (Salmo salar) to PAA. In experiment 1, salmon were exposed to different nominal concentrations (0, 0.6, and 2.4 ppm) of PAA for 5 min, followed by a re-exposure to the same concentrations for 30 min 2 weeks later. Sampling was performed before exposure to PAA and at 2 h, 48 h, and 2 w after exposures. In experiment 2, fish were subjected to crowding stress prior to PAA exposure at 4.8 ppm for 30 min. The fish were sampled before exposure and 1 h, 4 h, and 2 w after. The two trials were performed in a recirculation system. Both systemic (i.e., plasma cortisol, glucose, lactate, total antioxidant capacity) and mucosal (i.e., expression of antioxidant coding genes in the skin and gills) stress indicators were affected by the treatments at varying levels, and it was apparent that the fish were able to mount a robust response to the physiological demands of PAA exposure. The cortisol levels increased in the early hours after exposure and returned to basal level afterwards. Prior exposure history to PAA did not markedly affect the levels of plasma lactate and glucose when fish were re-exposed to PAA. Crowding stress before PAA treatment, however, did alter some of the stress indicators (i.e., lactate, glucose and expression of antioxidant genes in the gills), suggesting that stress history serves as both a confounding and compounding factor on how stress responses to PAA are mobilised. Nonetheless, the changes were not substantial. Gene expression profile analyses revealed that the antioxidant system was more responsive to PAA in the gills than in the skin. The increased antioxidant capacity in the plasma, particularly at 2.4 ppm and higher, indicates that antioxidants were produced to neutralise the internal redox imbalance resulting from PAA exposure. In conclusion, the results show that salmon were able to mount a robust adaptive response to different PAA doses and exposure times, and a combined exposure to stress and PAA. These results underscore the potential of PAA as a chemotherapeutant for salmon at PAA concentrations commonly applied to control parasitic infestations.
Original languageEnglish
JournalFish and Shellfish Immunology
Volume93
Pages (from-to)895-903
ISSN1050-4648
DOIs
Publication statusPublished - 2019

Keywords

  • Amoebic gill disease
  • Disinfectant
  • Peracetic acid
  • Peroxide
  • Stress response

Cite this

Soleng, M., Johansen, L-H., Johnsen, H., Johansson, G. S., Breiland, M. W., Rørmark, L., ... Lazado, C. C. (2019). Atlantic salmon (Salmo salar) mounts systemic and mucosal stress responses to peracetic acid. Fish and Shellfish Immunology, 93, 895-903. https://doi.org/10.1016/j.fsi.2019.08.048
Soleng, Malene ; Johansen, Lill-Heidi ; Johnsen, Hanne ; Johansson, Gunhild S ; Breiland, Mette W ; Rørmark, Lisbeth ; Pittman, Karin ; Pedersen, Lars-Flemming ; Lazado, Carlo Cabacang. / Atlantic salmon (Salmo salar) mounts systemic and mucosal stress responses to peracetic acid. In: Fish and Shellfish Immunology. 2019 ; Vol. 93. pp. 895-903.
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title = "Atlantic salmon (Salmo salar) mounts systemic and mucosal stress responses to peracetic acid",
abstract = "Peracetic acid (PAA), a strong organic peroxide, is considered a relatively sustainable disinfectant in aquaculture because of its broad effectivity against many pathogens at low concentrations and because it degrades spontaneously to harmless residues. The impacts of PAA on fish health must be determined before its use as either a routine disinfectant or chemotherapeutant. Here we investigated the systemic and mucosal stress responses of Atlantic salmon (Salmo salar) to PAA. In experiment 1, salmon were exposed to different nominal concentrations (0, 0.6, and 2.4 ppm) of PAA for 5 min, followed by a re-exposure to the same concentrations for 30 min 2 weeks later. Sampling was performed before exposure to PAA and at 2 h, 48 h, and 2 w after exposures. In experiment 2, fish were subjected to crowding stress prior to PAA exposure at 4.8 ppm for 30 min. The fish were sampled before exposure and 1 h, 4 h, and 2 w after. The two trials were performed in a recirculation system. Both systemic (i.e., plasma cortisol, glucose, lactate, total antioxidant capacity) and mucosal (i.e., expression of antioxidant coding genes in the skin and gills) stress indicators were affected by the treatments at varying levels, and it was apparent that the fish were able to mount a robust response to the physiological demands of PAA exposure. The cortisol levels increased in the early hours after exposure and returned to basal level afterwards. Prior exposure history to PAA did not markedly affect the levels of plasma lactate and glucose when fish were re-exposed to PAA. Crowding stress before PAA treatment, however, did alter some of the stress indicators (i.e., lactate, glucose and expression of antioxidant genes in the gills), suggesting that stress history serves as both a confounding and compounding factor on how stress responses to PAA are mobilised. Nonetheless, the changes were not substantial. Gene expression profile analyses revealed that the antioxidant system was more responsive to PAA in the gills than in the skin. The increased antioxidant capacity in the plasma, particularly at 2.4 ppm and higher, indicates that antioxidants were produced to neutralise the internal redox imbalance resulting from PAA exposure. In conclusion, the results show that salmon were able to mount a robust adaptive response to different PAA doses and exposure times, and a combined exposure to stress and PAA. These results underscore the potential of PAA as a chemotherapeutant for salmon at PAA concentrations commonly applied to control parasitic infestations.",
keywords = "Amoebic gill disease, Disinfectant, Peracetic acid, Peroxide, Stress response",
author = "Malene Soleng and Lill-Heidi Johansen and Hanne Johnsen and Johansson, {Gunhild S} and Breiland, {Mette W} and Lisbeth R{\o}rmark and Karin Pittman and Lars-Flemming Pedersen and Lazado, {Carlo Cabacang}",
year = "2019",
doi = "10.1016/j.fsi.2019.08.048",
language = "English",
volume = "93",
pages = "895--903",
journal = "Fish and Shellfish Immunology",
issn = "1050-4648",
publisher = "Academic Press",

}

Soleng, M, Johansen, L-H, Johnsen, H, Johansson, GS, Breiland, MW, Rørmark, L, Pittman, K, Pedersen, L-F & Lazado, CC 2019, 'Atlantic salmon (Salmo salar) mounts systemic and mucosal stress responses to peracetic acid', Fish and Shellfish Immunology, vol. 93, pp. 895-903. https://doi.org/10.1016/j.fsi.2019.08.048

Atlantic salmon (Salmo salar) mounts systemic and mucosal stress responses to peracetic acid. / Soleng, Malene; Johansen, Lill-Heidi; Johnsen, Hanne; Johansson, Gunhild S; Breiland, Mette W; Rørmark, Lisbeth; Pittman, Karin; Pedersen, Lars-Flemming; Lazado, Carlo Cabacang.

In: Fish and Shellfish Immunology, Vol. 93, 2019, p. 895-903.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Atlantic salmon (Salmo salar) mounts systemic and mucosal stress responses to peracetic acid

AU - Soleng, Malene

AU - Johansen, Lill-Heidi

AU - Johnsen, Hanne

AU - Johansson, Gunhild S

AU - Breiland, Mette W

AU - Rørmark, Lisbeth

AU - Pittman, Karin

AU - Pedersen, Lars-Flemming

AU - Lazado, Carlo Cabacang

PY - 2019

Y1 - 2019

N2 - Peracetic acid (PAA), a strong organic peroxide, is considered a relatively sustainable disinfectant in aquaculture because of its broad effectivity against many pathogens at low concentrations and because it degrades spontaneously to harmless residues. The impacts of PAA on fish health must be determined before its use as either a routine disinfectant or chemotherapeutant. Here we investigated the systemic and mucosal stress responses of Atlantic salmon (Salmo salar) to PAA. In experiment 1, salmon were exposed to different nominal concentrations (0, 0.6, and 2.4 ppm) of PAA for 5 min, followed by a re-exposure to the same concentrations for 30 min 2 weeks later. Sampling was performed before exposure to PAA and at 2 h, 48 h, and 2 w after exposures. In experiment 2, fish were subjected to crowding stress prior to PAA exposure at 4.8 ppm for 30 min. The fish were sampled before exposure and 1 h, 4 h, and 2 w after. The two trials were performed in a recirculation system. Both systemic (i.e., plasma cortisol, glucose, lactate, total antioxidant capacity) and mucosal (i.e., expression of antioxidant coding genes in the skin and gills) stress indicators were affected by the treatments at varying levels, and it was apparent that the fish were able to mount a robust response to the physiological demands of PAA exposure. The cortisol levels increased in the early hours after exposure and returned to basal level afterwards. Prior exposure history to PAA did not markedly affect the levels of plasma lactate and glucose when fish were re-exposed to PAA. Crowding stress before PAA treatment, however, did alter some of the stress indicators (i.e., lactate, glucose and expression of antioxidant genes in the gills), suggesting that stress history serves as both a confounding and compounding factor on how stress responses to PAA are mobilised. Nonetheless, the changes were not substantial. Gene expression profile analyses revealed that the antioxidant system was more responsive to PAA in the gills than in the skin. The increased antioxidant capacity in the plasma, particularly at 2.4 ppm and higher, indicates that antioxidants were produced to neutralise the internal redox imbalance resulting from PAA exposure. In conclusion, the results show that salmon were able to mount a robust adaptive response to different PAA doses and exposure times, and a combined exposure to stress and PAA. These results underscore the potential of PAA as a chemotherapeutant for salmon at PAA concentrations commonly applied to control parasitic infestations.

AB - Peracetic acid (PAA), a strong organic peroxide, is considered a relatively sustainable disinfectant in aquaculture because of its broad effectivity against many pathogens at low concentrations and because it degrades spontaneously to harmless residues. The impacts of PAA on fish health must be determined before its use as either a routine disinfectant or chemotherapeutant. Here we investigated the systemic and mucosal stress responses of Atlantic salmon (Salmo salar) to PAA. In experiment 1, salmon were exposed to different nominal concentrations (0, 0.6, and 2.4 ppm) of PAA for 5 min, followed by a re-exposure to the same concentrations for 30 min 2 weeks later. Sampling was performed before exposure to PAA and at 2 h, 48 h, and 2 w after exposures. In experiment 2, fish were subjected to crowding stress prior to PAA exposure at 4.8 ppm for 30 min. The fish were sampled before exposure and 1 h, 4 h, and 2 w after. The two trials were performed in a recirculation system. Both systemic (i.e., plasma cortisol, glucose, lactate, total antioxidant capacity) and mucosal (i.e., expression of antioxidant coding genes in the skin and gills) stress indicators were affected by the treatments at varying levels, and it was apparent that the fish were able to mount a robust response to the physiological demands of PAA exposure. The cortisol levels increased in the early hours after exposure and returned to basal level afterwards. Prior exposure history to PAA did not markedly affect the levels of plasma lactate and glucose when fish were re-exposed to PAA. Crowding stress before PAA treatment, however, did alter some of the stress indicators (i.e., lactate, glucose and expression of antioxidant genes in the gills), suggesting that stress history serves as both a confounding and compounding factor on how stress responses to PAA are mobilised. Nonetheless, the changes were not substantial. Gene expression profile analyses revealed that the antioxidant system was more responsive to PAA in the gills than in the skin. The increased antioxidant capacity in the plasma, particularly at 2.4 ppm and higher, indicates that antioxidants were produced to neutralise the internal redox imbalance resulting from PAA exposure. In conclusion, the results show that salmon were able to mount a robust adaptive response to different PAA doses and exposure times, and a combined exposure to stress and PAA. These results underscore the potential of PAA as a chemotherapeutant for salmon at PAA concentrations commonly applied to control parasitic infestations.

KW - Amoebic gill disease

KW - Disinfectant

KW - Peracetic acid

KW - Peroxide

KW - Stress response

U2 - 10.1016/j.fsi.2019.08.048

DO - 10.1016/j.fsi.2019.08.048

M3 - Journal article

VL - 93

SP - 895

EP - 903

JO - Fish and Shellfish Immunology

JF - Fish and Shellfish Immunology

SN - 1050-4648

ER -