Mucosal immune and stress responses of Neoparamoeba perurans-infected Atlantic salmon (Salmo salar) treated with peracetic acid shed light on the host-parasite-oxidant interactions
Treatment development for parasitic infestation is often limited to disease resolution as an endpoint response, and physiological and immunological consequences are not thoroughly considered. Here, we report the impact of exposing Atlantic salmon affected with amoebic gill disease (AGD) to peracetic...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-08-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2022.948897/full |
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| author | Carlo C. Lazado David A. Strand Mette W. Breiland Francisco Furtado Francisco Furtado Gerrit Timmerhaus Mona C. Gjessing Sigurd Hytterød Grigory V. Merkin Lars-Flemming Pedersen Karin A. Pittman Karin A. Pittman Aleksei Krasnov |
| author_facet | Carlo C. Lazado David A. Strand Mette W. Breiland Francisco Furtado Francisco Furtado Gerrit Timmerhaus Mona C. Gjessing Sigurd Hytterød Grigory V. Merkin Lars-Flemming Pedersen Karin A. Pittman Karin A. Pittman Aleksei Krasnov |
| author_sort | Carlo C. Lazado |
| collection | DOAJ |
| description | Treatment development for parasitic infestation is often limited to disease resolution as an endpoint response, and physiological and immunological consequences are not thoroughly considered. Here, we report the impact of exposing Atlantic salmon affected with amoebic gill disease (AGD) to peracetic acid (PAA), an oxidative chemotherapeutic. AGD-affected fish were treated with PAA either by exposing them to 5 ppm for 30 min or 10 ppm for 15 min. Unexposed fish from both infected and uninfected groups were also included. Samples for molecular, biochemical, and histological evaluations were collected at 24 h, 2 weeks, and 4 weeks post-treatment. Behavioral changes were observed during PAA exposure, and post-treatment mortality was higher in the infected and PAA treated groups, especially in 10 ppm for 15 min. Plasma indicators showed that liver health was affected by AGD, though PAA treatment did not exacerbate the infection-related changes. Transcriptome profiling in the gills showed significant changes, triggered by AGD and PAA treatments, and the effects of PAA were more notable 24 h after treatment. Genes related to immune pathways of B- and T- cells and protein synthesis and metabolism were downregulated, where the magnitude was more remarkable in 10 ppm for 15 min group. Even though treatment did not fully resolve the pathologies associated with AGD, 5 ppm for 30 min group showed lower parasite load at 4 weeks post-treatment. Mucous cell parameters (i.e., size and density) increased within 24 h post-treatment and were significantly higher at termination, especially in AGD-affected fish, with some treatment effects influenced by the dose of PAA. Infection and treatments resulted in oxidative stress—in the early phase in the gill mucosa, while systemic reactive oxygen species (ROS) dysregulation was evident at the later stage. Infected fish responded to elevated circulating ROS by increasing antioxidant production. Exposing the fish to a crowding stress revealed the interference in the post-stress responses. Lower cortisol response was displayed by AGD-affected groups. Collectively, the study established that PAA, within the evaluated treatment protocols, could not provide a convincing treatment resolution and, thus, requires further optimization. Nonetheless, PAA treatment altered the mucosal immune and stress responses of AGD-affected Atlantic salmon, shedding light on the host-parasite-treatment interactions. |
| first_indexed | 2024-04-14T02:28:04Z |
| format | Article |
| id | doaj.art-b045e03c065447cd964baa6f89e42020 |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-04-14T02:28:04Z |
| publishDate | 2022-08-01 |
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| series | Frontiers in Immunology |
| spelling | doaj.art-b045e03c065447cd964baa6f89e420202022-12-22T02:17:49ZengFrontiers Media S.A.Frontiers in Immunology1664-32242022-08-011310.3389/fimmu.2022.948897948897Mucosal immune and stress responses of Neoparamoeba perurans-infected Atlantic salmon (Salmo salar) treated with peracetic acid shed light on the host-parasite-oxidant interactionsCarlo C. Lazado0David A. Strand1Mette W. Breiland2Francisco Furtado3Francisco Furtado4Gerrit Timmerhaus5Mona C. Gjessing6Sigurd Hytterød7Grigory V. Merkin8Lars-Flemming Pedersen9Karin A. Pittman10Karin A. Pittman11Aleksei Krasnov12Nofima, The Norwegian Institute of Food, Fisheries and Aquaculture Research, Ås, NorwayNorwegian Veterinary Institute, Ås, NorwayNofima, The Norwegian Institute of Food, Fisheries and Aquaculture Research, Tromsø, NorwayNofima, The Norwegian Institute of Food, Fisheries and Aquaculture Research, Ås, NorwayCentre for Interdisciplinary Research in Animal Health (CIISA), Faculty of Veterinary Medicine, University of Lisbon, Lisbon, PortugalNofima, The Norwegian Institute of Food, Fisheries and Aquaculture Research, Ås, NorwayNorwegian Veterinary Institute, Ås, NorwayNorwegian Veterinary Institute, Ås, NorwayQuantidoc AS, Bergen, NorwayDTU Aqua, Section for Aquaculture, The North Sea Research Centre, Technical University of Denmark, Hirtshals, DenmarkQuantidoc AS, Bergen, NorwayDepartment of Biological Sciences, University of Bergen, Bergen, NorwayNofima, The Norwegian Institute of Food, Fisheries and Aquaculture Research, Ås, NorwayTreatment development for parasitic infestation is often limited to disease resolution as an endpoint response, and physiological and immunological consequences are not thoroughly considered. Here, we report the impact of exposing Atlantic salmon affected with amoebic gill disease (AGD) to peracetic acid (PAA), an oxidative chemotherapeutic. AGD-affected fish were treated with PAA either by exposing them to 5 ppm for 30 min or 10 ppm for 15 min. Unexposed fish from both infected and uninfected groups were also included. Samples for molecular, biochemical, and histological evaluations were collected at 24 h, 2 weeks, and 4 weeks post-treatment. Behavioral changes were observed during PAA exposure, and post-treatment mortality was higher in the infected and PAA treated groups, especially in 10 ppm for 15 min. Plasma indicators showed that liver health was affected by AGD, though PAA treatment did not exacerbate the infection-related changes. Transcriptome profiling in the gills showed significant changes, triggered by AGD and PAA treatments, and the effects of PAA were more notable 24 h after treatment. Genes related to immune pathways of B- and T- cells and protein synthesis and metabolism were downregulated, where the magnitude was more remarkable in 10 ppm for 15 min group. Even though treatment did not fully resolve the pathologies associated with AGD, 5 ppm for 30 min group showed lower parasite load at 4 weeks post-treatment. Mucous cell parameters (i.e., size and density) increased within 24 h post-treatment and were significantly higher at termination, especially in AGD-affected fish, with some treatment effects influenced by the dose of PAA. Infection and treatments resulted in oxidative stress—in the early phase in the gill mucosa, while systemic reactive oxygen species (ROS) dysregulation was evident at the later stage. Infected fish responded to elevated circulating ROS by increasing antioxidant production. Exposing the fish to a crowding stress revealed the interference in the post-stress responses. Lower cortisol response was displayed by AGD-affected groups. Collectively, the study established that PAA, within the evaluated treatment protocols, could not provide a convincing treatment resolution and, thus, requires further optimization. Nonetheless, PAA treatment altered the mucosal immune and stress responses of AGD-affected Atlantic salmon, shedding light on the host-parasite-treatment interactions. https://www.frontiersin.org/articles/10.3389/fimmu.2022.948897/fullamoebic gill diseaseaquaculturefish healthgill healthmucosal immunitymucous cells |
| spellingShingle | Carlo C. Lazado David A. Strand Mette W. Breiland Francisco Furtado Francisco Furtado Gerrit Timmerhaus Mona C. Gjessing Sigurd Hytterød Grigory V. Merkin Lars-Flemming Pedersen Karin A. Pittman Karin A. Pittman Aleksei Krasnov Mucosal immune and stress responses of Neoparamoeba perurans-infected Atlantic salmon (Salmo salar) treated with peracetic acid shed light on the host-parasite-oxidant interactions Frontiers in Immunology amoebic gill disease aquaculture fish health gill health mucosal immunity mucous cells |
| title | Mucosal immune and stress responses of Neoparamoeba perurans-infected Atlantic salmon (Salmo salar) treated with peracetic acid shed light on the host-parasite-oxidant interactions |
| title_full | Mucosal immune and stress responses of Neoparamoeba perurans-infected Atlantic salmon (Salmo salar) treated with peracetic acid shed light on the host-parasite-oxidant interactions |
| title_fullStr | Mucosal immune and stress responses of Neoparamoeba perurans-infected Atlantic salmon (Salmo salar) treated with peracetic acid shed light on the host-parasite-oxidant interactions |
| title_full_unstemmed | Mucosal immune and stress responses of Neoparamoeba perurans-infected Atlantic salmon (Salmo salar) treated with peracetic acid shed light on the host-parasite-oxidant interactions |
| title_short | Mucosal immune and stress responses of Neoparamoeba perurans-infected Atlantic salmon (Salmo salar) treated with peracetic acid shed light on the host-parasite-oxidant interactions |
| title_sort | mucosal immune and stress responses of neoparamoeba perurans infected atlantic salmon salmo salar treated with peracetic acid shed light on the host parasite oxidant interactions |
| topic | amoebic gill disease aquaculture fish health gill health mucosal immunity mucous cells |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2022.948897/full |
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