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Microbiota in intestinal digesta of Atlantic salmon (Salmo salar), observed from late freshwater stage until one year in seawater, and effects of functional ingredients: a case study from a commercial sized research site in the Arctic region

BACKGROUND: The importance of the gut microbiota for health and wellbeing is well established for humans and some land animals. The gut microbiota is supposedly as important for fish, but existing knowledge has many gaps, in particular for fish in the Arctic areas. This study addressed the dynamics...

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Autores principales: Wang, Jie, Jaramillo-Torres, Alexander, Li, Yanxian, Kortner, Trond M., Gajardo, Karina, Brevik, Øyvind Jakobsen, Jakobsen, Jan Vidar, Krogdahl, Åshild
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7841887/
https://www.ncbi.nlm.nih.gov/pubmed/33509296
http://dx.doi.org/10.1186/s42523-021-00075-7
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author Wang, Jie
Jaramillo-Torres, Alexander
Li, Yanxian
Kortner, Trond M.
Gajardo, Karina
Brevik, Øyvind Jakobsen
Jakobsen, Jan Vidar
Krogdahl, Åshild
author_facet Wang, Jie
Jaramillo-Torres, Alexander
Li, Yanxian
Kortner, Trond M.
Gajardo, Karina
Brevik, Øyvind Jakobsen
Jakobsen, Jan Vidar
Krogdahl, Åshild
author_sort Wang, Jie
collection PubMed
description BACKGROUND: The importance of the gut microbiota for health and wellbeing is well established for humans and some land animals. The gut microbiota is supposedly as important for fish, but existing knowledge has many gaps, in particular for fish in the Arctic areas. This study addressed the dynamics of Atlantic salmon digesta-associated gut microbiota assemblage and its associations with host responses from freshwater to seawater life stages under large-scale, commercial conditions in the Arctic region of Norway, and explored the effects of functional ingredients. The microbiota was characterized by 16S rRNA gene sequencing in distal intestinal digesta at four time points: 2 weeks before seawater transfer (in May, FW); 4 weeks after seawater transfer (in June, SW1); in November (SW2), and in April (SW3) the following year. Two series of diets were fed, varying throughout the observation time in nutrient composition according to the requirements of fish, one without (Ref diet), and the other with functional ingredients (Test diet). The functional ingredients, i.e. nucleotides, yeast cell walls, one prebiotic and essential fatty acids, were supplemented as single or mixtures based on the strategies from the feed company. RESULTS: Overall, the fish showed higher microbial richness and lactic acid bacteria (LAB) abundance after seawater transfer, while Simpson’s diversity decreased throughout the observation period. At SW1, the gut microbiota was slightly different from those at FW, and was dominated by the genera Lactobacillus and Photobacterium. As the fish progressed towards SW2 and SW3, the genera Lactobacillus and Mycoplasma became more prominent, with a corresponding decline in genus Photobacterium. The overall bacterial profiles at these time points showed a clear distinction from those at FW. A significant effect of functional ingredients (a mixture of nucleotides, yeast cell walls and essential fatty acids) was observed at SW2, where Test-fed fish showed lower microbial richness, Shannon’s diversity, and LAB abundance. The multivariate association analysis identified differentially abundant taxa, especially Megasphaera, to be significantly associated with gut immune and barrier gene expressions, and plasma nutrients. CONCLUSIONS: The gut microbiota profile varied during the observation period, and the Mycoplasma became the dominating bacteria with time. Megasphaera abundance was associated with gut health and plasma nutrient biomarkers. Functional ingredients modulated the gut microbiota profile during an important ongrowing stage. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-021-00075-7.
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spelling pubmed-78418872021-02-01 Microbiota in intestinal digesta of Atlantic salmon (Salmo salar), observed from late freshwater stage until one year in seawater, and effects of functional ingredients: a case study from a commercial sized research site in the Arctic region Wang, Jie Jaramillo-Torres, Alexander Li, Yanxian Kortner, Trond M. Gajardo, Karina Brevik, Øyvind Jakobsen Jakobsen, Jan Vidar Krogdahl, Åshild Anim Microbiome Research Article BACKGROUND: The importance of the gut microbiota for health and wellbeing is well established for humans and some land animals. The gut microbiota is supposedly as important for fish, but existing knowledge has many gaps, in particular for fish in the Arctic areas. This study addressed the dynamics of Atlantic salmon digesta-associated gut microbiota assemblage and its associations with host responses from freshwater to seawater life stages under large-scale, commercial conditions in the Arctic region of Norway, and explored the effects of functional ingredients. The microbiota was characterized by 16S rRNA gene sequencing in distal intestinal digesta at four time points: 2 weeks before seawater transfer (in May, FW); 4 weeks after seawater transfer (in June, SW1); in November (SW2), and in April (SW3) the following year. Two series of diets were fed, varying throughout the observation time in nutrient composition according to the requirements of fish, one without (Ref diet), and the other with functional ingredients (Test diet). The functional ingredients, i.e. nucleotides, yeast cell walls, one prebiotic and essential fatty acids, were supplemented as single or mixtures based on the strategies from the feed company. RESULTS: Overall, the fish showed higher microbial richness and lactic acid bacteria (LAB) abundance after seawater transfer, while Simpson’s diversity decreased throughout the observation period. At SW1, the gut microbiota was slightly different from those at FW, and was dominated by the genera Lactobacillus and Photobacterium. As the fish progressed towards SW2 and SW3, the genera Lactobacillus and Mycoplasma became more prominent, with a corresponding decline in genus Photobacterium. The overall bacterial profiles at these time points showed a clear distinction from those at FW. A significant effect of functional ingredients (a mixture of nucleotides, yeast cell walls and essential fatty acids) was observed at SW2, where Test-fed fish showed lower microbial richness, Shannon’s diversity, and LAB abundance. The multivariate association analysis identified differentially abundant taxa, especially Megasphaera, to be significantly associated with gut immune and barrier gene expressions, and plasma nutrients. CONCLUSIONS: The gut microbiota profile varied during the observation period, and the Mycoplasma became the dominating bacteria with time. Megasphaera abundance was associated with gut health and plasma nutrient biomarkers. Functional ingredients modulated the gut microbiota profile during an important ongrowing stage. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-021-00075-7. BioMed Central 2021-01-28 /pmc/articles/PMC7841887/ /pubmed/33509296 http://dx.doi.org/10.1186/s42523-021-00075-7 Text en © The Author(s) 2021 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Research Article
Wang, Jie
Jaramillo-Torres, Alexander
Li, Yanxian
Kortner, Trond M.
Gajardo, Karina
Brevik, Øyvind Jakobsen
Jakobsen, Jan Vidar
Krogdahl, Åshild
Microbiota in intestinal digesta of Atlantic salmon (Salmo salar), observed from late freshwater stage until one year in seawater, and effects of functional ingredients: a case study from a commercial sized research site in the Arctic region
title Microbiota in intestinal digesta of Atlantic salmon (Salmo salar), observed from late freshwater stage until one year in seawater, and effects of functional ingredients: a case study from a commercial sized research site in the Arctic region
title_full Microbiota in intestinal digesta of Atlantic salmon (Salmo salar), observed from late freshwater stage until one year in seawater, and effects of functional ingredients: a case study from a commercial sized research site in the Arctic region
title_fullStr Microbiota in intestinal digesta of Atlantic salmon (Salmo salar), observed from late freshwater stage until one year in seawater, and effects of functional ingredients: a case study from a commercial sized research site in the Arctic region
title_full_unstemmed Microbiota in intestinal digesta of Atlantic salmon (Salmo salar), observed from late freshwater stage until one year in seawater, and effects of functional ingredients: a case study from a commercial sized research site in the Arctic region
title_short Microbiota in intestinal digesta of Atlantic salmon (Salmo salar), observed from late freshwater stage until one year in seawater, and effects of functional ingredients: a case study from a commercial sized research site in the Arctic region
title_sort microbiota in intestinal digesta of atlantic salmon (salmo salar), observed from late freshwater stage until one year in seawater, and effects of functional ingredients: a case study from a commercial sized research site in the arctic region
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7841887/
https://www.ncbi.nlm.nih.gov/pubmed/33509296
http://dx.doi.org/10.1186/s42523-021-00075-7
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