Exploring gut microbiota in adult Atlantic salmon (Salmo salar L.): Associations with gut health and dietary prebiotics

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Needs review
study design
Citation
PMID PubMed identifier for scientific articles.
DOI Digital object identifier for electronic documents.
Authors
Wang J, Li Y, Jaramillo-Torres A, Einen O, Jakobsen JV, Krogdahl Å, Kortner TM
Journal
Animal microbiome
Year
2023
Keywords:
Atlantic salmon, Gut health, Gut microbiota, Lactic acid bacteria, Mycoplasma, Yeast cell wall based-prebiotics
BACKGROUND: The importance of the gut microbiota for physiological processes in mammals is well established, but the knowledge of their functional roles in fish is still limited. The aims of this study were to investigate associations between variation in taxonomical composition of the gut microbiota and gut health status in Atlantic salmon and to explore possible modulatory effects of dietary prebiotics in one net-pen farm in open water. The fish with initial mean body weight of around 240 g were fed diets based on the same basal composition, either without (Ref diet) or with (Test diet) yeast cell wall based-prebiotics, during the marine production phase from December to September the following year. Sampling was conducted at three sampling time points: January, April, and September, with average water temperature of 3.9 ℃, 3.4 ℃ and 9.6 ℃, respectively. RESULTS: As the fish progressed towards September, growth, brush border membrane enzyme activities, and the expression in the gut of most of the observed genes involved in immune (e.g., il8, cd4a, myd88, il1b, gilt, tgfb, cd8b and cd3), barrier (e.g., zo1, occludin, ecad, claudin25b and claudin15), and metabolism increased significantly. Lipid accumulation in pyloric enterocytes decreased remarkably, suggesting improvement of gut health condition. The growth of the fish did not differ between dietary treatments. Further, dietary prebiotics affected the gut health only marginally regardless of duration of administration. Regarding gut microbiota composition, a decrease in alpha diversity (Observed species, Pielou and Shannon) over time was observed, which was significantly associated with an increase in the relative abundance of genus Mycoplasma and decrease in 32 different taxa in genus level including lactic acid bacteria (LAB), such as Lactobacillus, Leuconostoc, and Lactococcus. This indicates that developmental stage of Atlantic salmon is a determinant for microbial composition. Multivariate association analysis revealed that the relative abundance of Mycoplasma was positively correlated with gut barrier gene expression, negatively correlated with plasma glucose levels, and that its relative abundance slightly increased by exposure to prebiotics. Furthermore, certain LAB (e.g., Leuconostoc), belonging to the core microbiota, showed a negative development with time, and significant associations with plasma nutrients levels (e.g., triglyceride and cholesterol) and gene expression related to gut immune and barrier function. CONCLUSIONS: As Atlantic salmon grew older under large-scale, commercial farm settings, the Mycoplasma became more prominent with a concomitant decline in LAB. Mycoplasma abundance correlated positively with time and gut barrier genes, while LAB abundance negatively correlated to time. Dietary prebiotics affected gut health status only marginally.

Experiment 1


Needs review

Curated date: 2024/03/11

Curator: Bolanle

Revision editor(s): Bolanle, Omojokunoluwatomisin

Subjects

Location of subjects
Norway
Host species Species from which microbiome was sampled. Contact us to have more species added.
Salmo salar
Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
Intestine Bowel,Intestinal tract,Intestine,intestine
Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
Diet Dietary,Diets,Diet,diet
Group 0 name Corresponds to the control (unexposed) group for case-control studies
Reference diet
Group 1 name Corresponds to the case (exposed) group for case-control studies
Test diet
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Atlantic Salmon fed with Yeast cell-wall based prebiotics diet with average water temperature of 3.9, 3.4 and 9.6 degree celsius respectively.
Group 0 sample size Number of subjects in the control (unexposed) group
36
Group 1 sample size Number of subjects in the case (exposed) group
36
Antibiotics exclusion Number of days without antibiotics usage (if applicable) and other antibiotics-related criteria used to exclude participants (if any)
None

Lab analysis

Sequencing type
16S
16S variable region One or more hypervariable region(s) of the bacterial 16S gene
V1-V2
Sequencing platform Manufacturer and experimental platform used for quantifying microbial abundance
Illumina

Statistical Analysis

Data transformation Data transformation applied to microbial abundance measurements prior to differential abundance testing (if any).
relative abundances
Statistical test
MaAsLin2
Significance threshold p-value or FDR threshold used for differential abundance testing (if any)
0.05
MHT correction Have statistical tests be corrected for multiple hypothesis testing (MHT)?
Yes
LDA Score above Threshold for the linear discriminant analysis (LDA) score for studies using the popular LEfSe tool
2

Alpha Diversity

Pielou Quantifies how equal the community is numerically
unchanged
Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Richness Number of species
unchanged

Signature 1

Needs review

Curated date: 2024/03/11

Curator: Bolanle

Revision editor(s): Bolanle

Source: General Performance

Description: Effects of diets containing yeast cell-wall based prebiotics on the gut microbiota of Atlantic Salmon in September: Mycoplasma became more prominent as fish progressed towards April and September.

Abundance in Group 1: increased abundance in Test diet

NCBI Quality ControlLinks
Mycoplasma

Revision editor(s): Bolanle

Signature 2

Needs review

Curated date: 2024/03/11

Curator: Bolanle

Revision editor(s): Bolanle

Source: Supplementary material 3

Description: Relative abundance of all Amplicon sequence variants (ASVs) for each sample; life stage dietary treatmet LAB decreasing trend suggests a change in the gut microbiome composition of Atlantic Salmon in response to diets

Abundance in Group 1: decreased abundance in Test diet

NCBI Quality ControlLinks
Lactobacillus
Lactococcus
Leuconostoc

Revision editor(s): Bolanle

Experiment 2


Needs review

Curated date: 2024/04/18

Curator: Bolanle

Revision editor(s): Bolanle

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
January Reference diet
Group 1 name Corresponds to the case (exposed) group for case-control studies
January Test diet
Group 0 sample size Number of subjects in the control (unexposed) group
18
Group 1 sample size Number of subjects in the case (exposed) group
18

Lab analysis

Statistical Analysis

Alpha Diversity

Pielou Quantifies how equal the community is numerically
unchanged
Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Richness Number of species
unchanged

Signature 1

Needs review

Curated date: 2024/04/18

Curator: Bolanle

Revision editor(s): Bolanle

Source: Figure 7

Description: most abundant taxa at genus level of all samples relative abundance of each taxon

Abundance in Group 1: increased abundance in January Test diet

NCBI Quality ControlLinks
Lactobacillus
Leuconostoc
Lactococcus
Peptostreptococcaceae
Peptostreptococcus
Weissella
Bacillus
Geobacillus
Clostridium
Photobacterium
Halomonas
Fusobacterium
Psychrilyobacter

Revision editor(s): Bolanle

Signature 2

Needs review

Curated date: 2024/04/18

Curator: Bolanle

Revision editor(s): Bolanle

Source: Figure 7

Description: most abundant taxa at genus level of all samples relative abundance of each taxon

Abundance in Group 1: decreased abundance in January Test diet

NCBI Quality ControlLinks
Ureibacillus

Revision editor(s): Bolanle

Experiment 3


Needs review

Curated date: 2024/03/14

Curator: Bolanle

Revision editor(s): Bolanle, Omojokunoluwatomisin

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
Fishes fed with test diet in January
Group 1 name Corresponds to the case (exposed) group for case-control studies
Fishes fed with test diet in April
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Atlantic Salmon fed with yeast cell wall based-prebiotics diet in January
Antibiotics exclusion Number of days without antibiotics usage (if applicable) and other antibiotics-related criteria used to exclude participants (if any)
Not specified

Lab analysis

Statistical Analysis

Alpha Diversity

Pielou Quantifies how equal the community is numerically
unchanged
Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Simpson Estimator of species richness and species evenness: more weight on species evenness
unchanged

Signature 1

Needs review

Curated date: 2024/03/14

Curator: Bolanle

Revision editor(s): Bolanle

Source: FIgure 7

Description: Compared to January fish, April fish showed a slight increase in genera Proteobacteria (15% and 10% in Reference fed and Test-fed fish, respectively) and Mycoplasma (4% and 29.5% in Reference fed and Test- fed fish, respectively)

Abundance in Group 1: increased abundance in Fishes fed with test diet in April

NCBI Quality ControlLinks
Photobacterium

Revision editor(s): Bolanle

Experiment 4


Needs review

Curated date: 2024/03/14

Curator: Bolanle

Revision editor(s): Bolanle, Omojokunoluwatomisin

Differences from previous experiment shown

Subjects

Group 1 name Corresponds to the case (exposed) group for case-control studies
Fishes fed with test diet in September
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Atlantic Salmon fed with yeast cell wall based-prebiotics diet in September

Lab analysis

Statistical Analysis

Significance threshold p-value or FDR threshold used for differential abundance testing (if any)
0.001

Alpha Diversity

Pielou Quantifies how equal the community is numerically
unchanged
Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Simpson Estimator of species richness and species evenness: more weight on species evenness
unchanged

Signature 1

Needs review

Curated date: 2024/03/17

Curator: Bolanle

Revision editor(s): Bolanle

Source: Figure 7

Description: As fish subject progressed towards september, Mycoplasma (50% and 47% in Reference diet fish and Test dit fish respectively) became more prominent.

Abundance in Group 1: increased abundance in Fishes fed with test diet in September

NCBI Quality ControlLinks
Mycoplasma

Revision editor(s): Bolanle

Signature 2

Needs review

Curated date: 2024/03/17

Curator: Bolanle

Revision editor(s): Bolanle

Source: Figure 7

Description: there was reduction in Lactic acid bacteria(LAB), for example Lactobacillus (12%), Leuconostoc (0.03%) and Lactococcus(0.02%) in Reference diet fish, and Lactobacillus (12%), Leuconostoc (0.05%) and Lactococcus (0.02%) in Test diet fish, respectively.

Abundance in Group 1: decreased abundance in Fishes fed with test diet in September

NCBI Quality ControlLinks
Leuconostoc
Lactobacillus
Lactococcus

Revision editor(s): Bolanle

Experiment 5


Needs review

Curated date: 2024/04/18

Curator: Bolanle

Revision editor(s): Bolanle

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
April Reference diet
Group 1 name Corresponds to the case (exposed) group for case-control studies
April Test diet
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Atlantic Salmon fed with Yeast cell-wall based prebiotics diet with average water temperature of 3.9, 3.4 and 9.6 degree celsius respectively.
Antibiotics exclusion Number of days without antibiotics usage (if applicable) and other antibiotics-related criteria used to exclude participants (if any)
None

Lab analysis

Statistical Analysis

Significance threshold p-value or FDR threshold used for differential abundance testing (if any)
0.05

Alpha Diversity

Pielou Quantifies how equal the community is numerically
unchanged
Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Richness Number of species
unchanged

Signature 1

Needs review

Curated date: 2024/04/18

Curator: Bolanle

Revision editor(s): Bolanle

Source: Figure 7

Description: most abundant taxa at genus level of all samples relative abundance of each taxon

Abundance in Group 1: increased abundance in April Test diet

NCBI Quality ControlLinks
Fusobacterium
Halomonas
Mycoplasma
Shewanella
Weissella
Oscillospiraceae bacterium
Aliivibrio

Revision editor(s): Bolanle

Signature 2

Needs review

Curated date: 2024/04/18

Curator: Bolanle

Revision editor(s): Bolanle

Source: Figure 7

Description: most abundant taxa at genus level of all samples relative abundance of each taxon

Abundance in Group 1: decreased abundance in April Test diet

NCBI Quality ControlLinks
Lactobacillus
Leuconostoc
Lactococcus
Peptostreptococcaceae
Peptostreptococcus
Bacillus
Ureibacillus
Photobacterium
Psychrilyobacter
Clostridium

Revision editor(s): Bolanle

Experiment 6


Needs review

Curated date: 2024/04/18

Curator: Bolanle

Revision editor(s): Bolanle

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
september Reference diet
Group 1 name Corresponds to the case (exposed) group for case-control studies
september Test diet

Lab analysis

Statistical Analysis

Alpha Diversity

Pielou Quantifies how equal the community is numerically
unchanged
Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Richness Number of species
unchanged

Signature 1

Needs review

Curated date: 2024/04/18

Curator: Bolanle

Revision editor(s): Bolanle

Source: Figure 7

Description: most abundant taxa at genus level of all samples relative abundance of each taxon

Abundance in Group 1: increased abundance in september Test diet

NCBI Quality ControlLinks
Ureibacillus
Photobacterium
Lactobacillus
Shewanella
Psychrilyobacter

Revision editor(s): Bolanle

Signature 2

Needs review

Curated date: 2024/04/18

Curator: Bolanle

Revision editor(s): Bolanle

Source: Figure 7

Description: most abundant taxa at genus level of all samples relative abundance of each taxon

Abundance in Group 1: decreased abundance in september Test diet

NCBI Quality ControlLinks
Halomonas
Mycoplasma

Revision editor(s): Bolanle