Modulation of gut microbiota composition and predicted metabolic capacity after nutritional programming with a plant-rich diet in Atlantic salmon (Salmo salar): insights across developmental stages.

To promote sustainable aquaculture, the formulation of Atlantic salmon (Salmo salar) feeds has changed in recent decades, focusing on replacing standard marine-based ingredients with plant-based alternatives, increasingly demonstrating successful outcomes in terms of fish performance. However, littl...

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Published in:Animal Microbiome
Main Authors: Tawfik, Marwa Mamdouh, Lorgen-Ritchie, Marlene, Król, Elżbieta, McMillan, Stuart, Norambuena, Fernando, Bolnick, Daniel I, Douglas, Alex, Tocher, Douglas R, Betancor, Mónica B, Martin, Samuel A M
Format: Article in Journal/Newspaper
Language:English
Published: BioMed Central 2024
Subjects:
Online Access:https://doi.org/10.1186/s42523-024-00321-8
https://pubmed.ncbi.nlm.nih.gov/38951941
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11218362/
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spelling ftpubmed:38951941 2024-09-09T19:30:27+00:00 Modulation of gut microbiota composition and predicted metabolic capacity after nutritional programming with a plant-rich diet in Atlantic salmon (Salmo salar): insights across developmental stages. Tawfik, Marwa Mamdouh Lorgen-Ritchie, Marlene Król, Elżbieta McMillan, Stuart Norambuena, Fernando Bolnick, Daniel I Douglas, Alex Tocher, Douglas R Betancor, Mónica B Martin, Samuel A M 2024 Jul 01 https://doi.org/10.1186/s42523-024-00321-8 https://pubmed.ncbi.nlm.nih.gov/38951941 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11218362/ eng eng BioMed Central https://doi.org/10.1186/s42523-024-00321-8 https://pubmed.ncbi.nlm.nih.gov/38951941 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11218362/ © 2024. The Author(s). Anim Microbiome ISSN:2524-4671 Volume:6 Issue:1 Atlantic salmon First feeding Fishmeal Intestinal microbiota Metabolic programming Microbio Nutritional history Nutritional programming Plant-based diet Vegetable-based diet Journal Article 2024 ftpubmed https://doi.org/10.1186/s42523-024-00321-8 2024-07-04T16:01:00Z To promote sustainable aquaculture, the formulation of Atlantic salmon (Salmo salar) feeds has changed in recent decades, focusing on replacing standard marine-based ingredients with plant-based alternatives, increasingly demonstrating successful outcomes in terms of fish performance. However, little is known about how these plant-based diets may impact the gut microbiota at first feeding and onwards. Nutritional programming (NP) is one strategy applied for exposing fish to a plant-based (V) diet at an early stage in life to promote full utilisation of plant-based ingredients and prevent potential adverse impacts of exposure to a plant-rich diet later in life. We investigated the impact of NP on gut microbiota by introducing fish to plant ingredients (V fish) during first feeding for a brief period of two weeks (stimulus phase) and compared those to fish fed a marine-based diet (M fish). Results demonstrated that V fish not only maintained growth performance at 16 (intermediate phase) and 22 (challenge phase) weeks post first feeding (wpff) when compared to M fish but also modulated gut microbiota. PERMANOVA general effects revealed gut microbiota dissimilarity by fish group (V vs. M fish) and phases (stimulus vs. intermediate vs. challenge). However, no interaction effect of both groups and phases was demonstrated, suggesting a sustained impact of V diet (nutritional history) on fish across time points/phases. Moreover, the V diet exerted a significant cumulative modulatory effect on the Atlantic salmon gut microbiota at 16 wpff that was not demonstrated at two wpff, although both fish groups were fed the M diet at 16 wpff. The nutritional history/dietary regime is the main NP influencing factor, whereas environmental and host factors significantly impacted microbiota composition in M fish. Microbial metabolic reactions of amino acid metabolism were higher in M fish when compared to V fish at two wpff suggesting microbiota played a role in digesting the essential amino acids of M feed. The excessive mucin O-degradation revealed in V fish at two wpff was mitigated in later life stages after NP, suggesting physiological adaptability and tolerance to V diet. Future studies are required to explore more fully how the microbiota functionally contributes to the NP. Article in Journal/Newspaper Atlantic salmon Salmo salar PubMed Central (PMC) Animal Microbiome 6 1
institution Open Polar
collection PubMed Central (PMC)
op_collection_id ftpubmed
language English
topic Atlantic salmon
First feeding
Fishmeal
Intestinal microbiota
Metabolic programming
Microbio
Nutritional history
Nutritional programming
Plant-based diet
Vegetable-based diet
spellingShingle Atlantic salmon
First feeding
Fishmeal
Intestinal microbiota
Metabolic programming
Microbio
Nutritional history
Nutritional programming
Plant-based diet
Vegetable-based diet
Tawfik, Marwa Mamdouh
Lorgen-Ritchie, Marlene
Król, Elżbieta
McMillan, Stuart
Norambuena, Fernando
Bolnick, Daniel I
Douglas, Alex
Tocher, Douglas R
Betancor, Mónica B
Martin, Samuel A M
Modulation of gut microbiota composition and predicted metabolic capacity after nutritional programming with a plant-rich diet in Atlantic salmon (Salmo salar): insights across developmental stages.
topic_facet Atlantic salmon
First feeding
Fishmeal
Intestinal microbiota
Metabolic programming
Microbio
Nutritional history
Nutritional programming
Plant-based diet
Vegetable-based diet
description To promote sustainable aquaculture, the formulation of Atlantic salmon (Salmo salar) feeds has changed in recent decades, focusing on replacing standard marine-based ingredients with plant-based alternatives, increasingly demonstrating successful outcomes in terms of fish performance. However, little is known about how these plant-based diets may impact the gut microbiota at first feeding and onwards. Nutritional programming (NP) is one strategy applied for exposing fish to a plant-based (V) diet at an early stage in life to promote full utilisation of plant-based ingredients and prevent potential adverse impacts of exposure to a plant-rich diet later in life. We investigated the impact of NP on gut microbiota by introducing fish to plant ingredients (V fish) during first feeding for a brief period of two weeks (stimulus phase) and compared those to fish fed a marine-based diet (M fish). Results demonstrated that V fish not only maintained growth performance at 16 (intermediate phase) and 22 (challenge phase) weeks post first feeding (wpff) when compared to M fish but also modulated gut microbiota. PERMANOVA general effects revealed gut microbiota dissimilarity by fish group (V vs. M fish) and phases (stimulus vs. intermediate vs. challenge). However, no interaction effect of both groups and phases was demonstrated, suggesting a sustained impact of V diet (nutritional history) on fish across time points/phases. Moreover, the V diet exerted a significant cumulative modulatory effect on the Atlantic salmon gut microbiota at 16 wpff that was not demonstrated at two wpff, although both fish groups were fed the M diet at 16 wpff. The nutritional history/dietary regime is the main NP influencing factor, whereas environmental and host factors significantly impacted microbiota composition in M fish. Microbial metabolic reactions of amino acid metabolism were higher in M fish when compared to V fish at two wpff suggesting microbiota played a role in digesting the essential amino acids of M feed. The excessive mucin O-degradation revealed in V fish at two wpff was mitigated in later life stages after NP, suggesting physiological adaptability and tolerance to V diet. Future studies are required to explore more fully how the microbiota functionally contributes to the NP.
format Article in Journal/Newspaper
author Tawfik, Marwa Mamdouh
Lorgen-Ritchie, Marlene
Król, Elżbieta
McMillan, Stuart
Norambuena, Fernando
Bolnick, Daniel I
Douglas, Alex
Tocher, Douglas R
Betancor, Mónica B
Martin, Samuel A M
author_facet Tawfik, Marwa Mamdouh
Lorgen-Ritchie, Marlene
Król, Elżbieta
McMillan, Stuart
Norambuena, Fernando
Bolnick, Daniel I
Douglas, Alex
Tocher, Douglas R
Betancor, Mónica B
Martin, Samuel A M
author_sort Tawfik, Marwa Mamdouh
title Modulation of gut microbiota composition and predicted metabolic capacity after nutritional programming with a plant-rich diet in Atlantic salmon (Salmo salar): insights across developmental stages.
title_short Modulation of gut microbiota composition and predicted metabolic capacity after nutritional programming with a plant-rich diet in Atlantic salmon (Salmo salar): insights across developmental stages.
title_full Modulation of gut microbiota composition and predicted metabolic capacity after nutritional programming with a plant-rich diet in Atlantic salmon (Salmo salar): insights across developmental stages.
title_fullStr Modulation of gut microbiota composition and predicted metabolic capacity after nutritional programming with a plant-rich diet in Atlantic salmon (Salmo salar): insights across developmental stages.
title_full_unstemmed Modulation of gut microbiota composition and predicted metabolic capacity after nutritional programming with a plant-rich diet in Atlantic salmon (Salmo salar): insights across developmental stages.
title_sort modulation of gut microbiota composition and predicted metabolic capacity after nutritional programming with a plant-rich diet in atlantic salmon (salmo salar): insights across developmental stages.
publisher BioMed Central
publishDate 2024
url https://doi.org/10.1186/s42523-024-00321-8
https://pubmed.ncbi.nlm.nih.gov/38951941
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11218362/
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_source Anim Microbiome
ISSN:2524-4671
Volume:6
Issue:1
op_relation https://doi.org/10.1186/s42523-024-00321-8
https://pubmed.ncbi.nlm.nih.gov/38951941
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11218362/
op_rights © 2024. The Author(s).
op_doi https://doi.org/10.1186/s42523-024-00321-8
container_title Animal Microbiome
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