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A novel gnotobiotic experimental system for Atlantic salmon (Salmo salar L.) reveals a microbial influence on mucosal barrier function and adipose tissue accumulation during the yolk sac stage

Gnotobiotic models have had a crucial role in studying the effect that commensal microbiota has on the health of their animal hosts. Despite their physiological and ecological diversity, teleost fishes are still underrepresented in gnotobiotic research. Moreover, a better understanding of host-micro...

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Autores principales: Gómez de la Torre Canny, Sol, Nordgård, Catherine Taylor, Mathisen, Amalie Johanne Horn, Degré Lorentsen, Eirik, Vadstein, Olav, Bakke, Ingrid
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9929952/
https://www.ncbi.nlm.nih.gov/pubmed/36817693
http://dx.doi.org/10.3389/fcimb.2022.1068302
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author Gómez de la Torre Canny, Sol
Nordgård, Catherine Taylor
Mathisen, Amalie Johanne Horn
Degré Lorentsen, Eirik
Vadstein, Olav
Bakke, Ingrid
author_facet Gómez de la Torre Canny, Sol
Nordgård, Catherine Taylor
Mathisen, Amalie Johanne Horn
Degré Lorentsen, Eirik
Vadstein, Olav
Bakke, Ingrid
author_sort Gómez de la Torre Canny, Sol
collection PubMed
description Gnotobiotic models have had a crucial role in studying the effect that commensal microbiota has on the health of their animal hosts. Despite their physiological and ecological diversity, teleost fishes are still underrepresented in gnotobiotic research. Moreover, a better understanding of host-microbe interactions in farmed fish has the potential to contribute to sustainable global food supply. We have developed a novel gnotobiotic experimental system that includes the derivation of fertilized eggs of farmed and wild Atlantic salmon, and gnotobiotic husbandry of fry during the yolk sac stage. We used a microscopy-based approach to estimate the barrier function of the skin mucus layer and used this measurement to select the derivation procedure that minimized adverse effects on the skin mucosa. We also used this method to demonstrate that the mucus barrier was reduced in germ-free fry when compared to fry colonized with two different bacterial communities. This alteration in the mucus barrier was preceded by an increase in the number of cells containing neutral mucosubstances in the anterior segment of the body, but without changes in the number of cells containing acidic substances in any of the other segments studied along the body axis. In addition, we showed how the microbial status of the fry temporarily affected body size and the utilization of internal yolk stores during the yolk sac stage. Finally, we showed that the presence of bacterial communities associated with the fry, as well as their composition, affected the size of adipose tissue. Fry colonized with water from a lake had a larger visceral adipose tissue depot than both conventionally raised and germ-free fry. Together, our results show that this novel gnotobiotic experimental system is a useful tool for the study of host-microbe interactions in this species of aquacultural importance.
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spelling pubmed-99299522023-02-16 A novel gnotobiotic experimental system for Atlantic salmon (Salmo salar L.) reveals a microbial influence on mucosal barrier function and adipose tissue accumulation during the yolk sac stage Gómez de la Torre Canny, Sol Nordgård, Catherine Taylor Mathisen, Amalie Johanne Horn Degré Lorentsen, Eirik Vadstein, Olav Bakke, Ingrid Front Cell Infect Microbiol Cellular and Infection Microbiology Gnotobiotic models have had a crucial role in studying the effect that commensal microbiota has on the health of their animal hosts. Despite their physiological and ecological diversity, teleost fishes are still underrepresented in gnotobiotic research. Moreover, a better understanding of host-microbe interactions in farmed fish has the potential to contribute to sustainable global food supply. We have developed a novel gnotobiotic experimental system that includes the derivation of fertilized eggs of farmed and wild Atlantic salmon, and gnotobiotic husbandry of fry during the yolk sac stage. We used a microscopy-based approach to estimate the barrier function of the skin mucus layer and used this measurement to select the derivation procedure that minimized adverse effects on the skin mucosa. We also used this method to demonstrate that the mucus barrier was reduced in germ-free fry when compared to fry colonized with two different bacterial communities. This alteration in the mucus barrier was preceded by an increase in the number of cells containing neutral mucosubstances in the anterior segment of the body, but without changes in the number of cells containing acidic substances in any of the other segments studied along the body axis. In addition, we showed how the microbial status of the fry temporarily affected body size and the utilization of internal yolk stores during the yolk sac stage. Finally, we showed that the presence of bacterial communities associated with the fry, as well as their composition, affected the size of adipose tissue. Fry colonized with water from a lake had a larger visceral adipose tissue depot than both conventionally raised and germ-free fry. Together, our results show that this novel gnotobiotic experimental system is a useful tool for the study of host-microbe interactions in this species of aquacultural importance. Frontiers Media S.A. 2023-02-01 /pmc/articles/PMC9929952/ /pubmed/36817693 http://dx.doi.org/10.3389/fcimb.2022.1068302 Text en Copyright © 2023 Gómez de la Torre Canny, Nordgård, Mathisen, Degré Lorentsen, Vadstein and Bakke https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cellular and Infection Microbiology
Gómez de la Torre Canny, Sol
Nordgård, Catherine Taylor
Mathisen, Amalie Johanne Horn
Degré Lorentsen, Eirik
Vadstein, Olav
Bakke, Ingrid
A novel gnotobiotic experimental system for Atlantic salmon (Salmo salar L.) reveals a microbial influence on mucosal barrier function and adipose tissue accumulation during the yolk sac stage
title A novel gnotobiotic experimental system for Atlantic salmon (Salmo salar L.) reveals a microbial influence on mucosal barrier function and adipose tissue accumulation during the yolk sac stage
title_full A novel gnotobiotic experimental system for Atlantic salmon (Salmo salar L.) reveals a microbial influence on mucosal barrier function and adipose tissue accumulation during the yolk sac stage
title_fullStr A novel gnotobiotic experimental system for Atlantic salmon (Salmo salar L.) reveals a microbial influence on mucosal barrier function and adipose tissue accumulation during the yolk sac stage
title_full_unstemmed A novel gnotobiotic experimental system for Atlantic salmon (Salmo salar L.) reveals a microbial influence on mucosal barrier function and adipose tissue accumulation during the yolk sac stage
title_short A novel gnotobiotic experimental system for Atlantic salmon (Salmo salar L.) reveals a microbial influence on mucosal barrier function and adipose tissue accumulation during the yolk sac stage
title_sort novel gnotobiotic experimental system for atlantic salmon (salmo salar l.) reveals a microbial influence on mucosal barrier function and adipose tissue accumulation during the yolk sac stage
topic Cellular and Infection Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9929952/
https://www.ncbi.nlm.nih.gov/pubmed/36817693
http://dx.doi.org/10.3389/fcimb.2022.1068302
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