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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Published in:Frontiers in Cellular and Infection Microbiology
Main Authors: Gómez de la Torre Canny, Sol, Nordgård, Catherine Taylor, Mathisen, Amalie Johanne Horn, Degré Lorentsen, Eirik, Vadstein, Olav, Bakke, Ingrid
Other Authors: Norges Forskningsråd
Format: Article in Journal/Newspaper
Language:unknown
Published: Frontiers Media SA 2023
Subjects:
Online Access:http://dx.doi.org/10.3389/fcimb.2022.1068302
https://www.frontiersin.org/articles/10.3389/fcimb.2022.1068302/full
id crfrontiers:10.3389/fcimb.2022.1068302
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spelling crfrontiers:10.3389/fcimb.2022.1068302 2024-04-28T08:13:34+00:00 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 Norges Forskningsråd 2023 http://dx.doi.org/10.3389/fcimb.2022.1068302 https://www.frontiersin.org/articles/10.3389/fcimb.2022.1068302/full unknown Frontiers Media SA https://creativecommons.org/licenses/by/4.0/ Frontiers in Cellular and Infection Microbiology volume 12 ISSN 2235-2988 Infectious Diseases Microbiology (medical) Immunology Microbiology journal-article 2023 crfrontiers https://doi.org/10.3389/fcimb.2022.1068302 2024-04-02T07:43:56Z 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. Article in Journal/Newspaper Atlantic salmon Salmo salar Frontiers (Publisher) Frontiers in Cellular and Infection Microbiology 12
institution Open Polar
collection Frontiers (Publisher)
op_collection_id crfrontiers
language unknown
topic Infectious Diseases
Microbiology (medical)
Immunology
Microbiology
spellingShingle Infectious Diseases
Microbiology (medical)
Immunology
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
topic_facet Infectious Diseases
Microbiology (medical)
Immunology
Microbiology
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.
author2 Norges Forskningsråd
format Article in Journal/Newspaper
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
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_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_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_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
publisher Frontiers Media SA
publishDate 2023
url http://dx.doi.org/10.3389/fcimb.2022.1068302
https://www.frontiersin.org/articles/10.3389/fcimb.2022.1068302/full
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_source Frontiers in Cellular and Infection Microbiology
volume 12
ISSN 2235-2988
op_rights https://creativecommons.org/licenses/by/4.0/
op_doi https://doi.org/10.3389/fcimb.2022.1068302
container_title Frontiers in Cellular and Infection Microbiology
container_volume 12
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