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: Sol Gómez de la Torre Canny, Catherine Taylor Nordgård, Amalie Johanne Horn Mathisen, Eirik Degré Lorentsen, Olav Vadstein, Ingrid Bakke
Format: Article in Journal/Newspaper
Language:English
Published: Frontiers Media S.A. 2023
Subjects:
Online Access:https://doi.org/10.3389/fcimb.2022.1068302
https://doaj.org/article/85fcc5f571a6431fb86b00d9d9cf4aa4
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spelling ftdoajarticles:oai:doaj.org/article:85fcc5f571a6431fb86b00d9d9cf4aa4 2023-05-15T15:31:16+02:00 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 Sol Gómez de la Torre Canny Catherine Taylor Nordgård Amalie Johanne Horn Mathisen Eirik Degré Lorentsen Olav Vadstein Ingrid Bakke 2023-02-01T00:00:00Z https://doi.org/10.3389/fcimb.2022.1068302 https://doaj.org/article/85fcc5f571a6431fb86b00d9d9cf4aa4 EN eng Frontiers Media S.A. https://www.frontiersin.org/articles/10.3389/fcimb.2022.1068302/full https://doaj.org/toc/2235-2988 2235-2988 doi:10.3389/fcimb.2022.1068302 https://doaj.org/article/85fcc5f571a6431fb86b00d9d9cf4aa4 Frontiers in Cellular and Infection Microbiology, Vol 12 (2023) gnotobiotic Atlantic salmon (Salmo salar L.) skin mucus microbiome yolk sac fry adipose tissue Microbiology QR1-502 article 2023 ftdoajarticles https://doi.org/10.3389/fcimb.2022.1068302 2023-02-05T01:30:47Z 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 Directory of Open Access Journals: DOAJ Articles Frontiers in Cellular and Infection Microbiology 12
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic gnotobiotic
Atlantic salmon (Salmo salar L.)
skin mucus
microbiome
yolk sac fry
adipose tissue
Microbiology
QR1-502
spellingShingle gnotobiotic
Atlantic salmon (Salmo salar L.)
skin mucus
microbiome
yolk sac fry
adipose tissue
Microbiology
QR1-502
Sol Gómez de la Torre Canny
Catherine Taylor Nordgård
Amalie Johanne Horn Mathisen
Eirik Degré Lorentsen
Olav Vadstein
Ingrid Bakke
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 gnotobiotic
Atlantic salmon (Salmo salar L.)
skin mucus
microbiome
yolk sac fry
adipose tissue
Microbiology
QR1-502
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.
format Article in Journal/Newspaper
author Sol Gómez de la Torre Canny
Catherine Taylor Nordgård
Amalie Johanne Horn Mathisen
Eirik Degré Lorentsen
Olav Vadstein
Ingrid Bakke
author_facet Sol Gómez de la Torre Canny
Catherine Taylor Nordgård
Amalie Johanne Horn Mathisen
Eirik Degré Lorentsen
Olav Vadstein
Ingrid Bakke
author_sort Sol Gómez de la Torre Canny
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 S.A.
publishDate 2023
url https://doi.org/10.3389/fcimb.2022.1068302
https://doaj.org/article/85fcc5f571a6431fb86b00d9d9cf4aa4
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_source Frontiers in Cellular and Infection Microbiology, Vol 12 (2023)
op_relation https://www.frontiersin.org/articles/10.3389/fcimb.2022.1068302/full
https://doaj.org/toc/2235-2988
2235-2988
doi:10.3389/fcimb.2022.1068302
https://doaj.org/article/85fcc5f571a6431fb86b00d9d9cf4aa4
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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