Sleep deprivation-induced anxiety-like behaviors are associated with alterations in the gut microbiota and metabolites

From BugSigDB
Needs review
study design
Citation
PMID PubMed identifier for scientific articles.
DOI Digital object identifier for electronic documents.
URI
Authors
Zhang N, Gao X, Li D, Xu L, Zhou G, Xu M, Peng L, Sun G, Pan F, Li Y, Ren R, Huang R, Yang Y, Wang Z
Journal
Microbiology spectrum
Year
2024
Keywords:
anxiety, gut microbiota, metabolomics, probiotics, sleep deprivation
UNLABELLED: The present study aimed to characterize the gut microbiota and serum metabolome changes associated with sleep deprivation (SD) as well as to explore the potential benefits of multi-probiotic supplementation in alleviating SD-related mental health disorders. Rats were subjected to 7 days of SD, followed by 14 days of multi-probiotics or saline administration. Open-field tests were conducted at baseline, end of SD (day 7), and after 14 days of saline or multi-probiotic gavage (day 21). Metagenomic sequencing was conducted on fecal samples, and serum metabolites were measured by untargeted liquid chromatography tandem-mass spectrometry. At day 7, anxiety-like behaviors, including significant decreases in total movement distance (P = 0.0002) and staying time in the central zone (P = 0.021), were observed. In addition, increased levels of lipopolysaccharide (LPS; P = 0.028) and decreased levels of uridine (P = 0.018) and tryptophan (P = 0.01) were detected in rats after 7 days of SD. After SD, the richness of the gut bacterial community increased, and the levels of Akkermansia muciniphila, Muribaculum intestinale, and Bacteroides caecimuris decreased. The changes in the host metabolism and gut microbiota composition were strongly associated with the anxiety-like behaviors caused by SD. In addition, multi-probiotic supplementation for 14 days modestly improved the anxiety-like behaviors in SD rats but significantly reduced the serum level of LPS (P = 0.045). In conclusion, SD induces changes in the gut microbiota and serum metabolites, which may contribute to the development of chronic inflammatory responses and affect the gut-brain axis, causing anxiety-like behaviors. Probiotic supplementation significantly reduces serum LPS, which may alleviate the influence of chronic inflammation. IMPORTANCE: The disturbance in the gut microbiome and serum metabolome induced by SD may be involved in anxiety-like behaviors. Probiotic supplementation decreases serum levels of LPS, but this reduction may be insufficient for alleviating SD-induced anxiety-like behaviors.

Experiment 1


Needs review

Curated date: 2024/03/18

Curator: Iman-Ngwepe

Revision editor(s): Iman-Ngwepe, Aleru Divine

Subjects

Location of subjects
China
Host species Species from which microbiome was sampled. Contact us to have more species added.
Rattus norvegicus
Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
Feces Cow dung,Cow pat,Droppings,Dung,Excrement,Excreta,Faeces,Fecal material,Fecal matter,Fewmet,Frass,Guano,Matières fécales@fr,Merde@fr,Ordure,Partie de la merde@fr,Piece of shit,Porción de mierda@es,Portion of dung,Portion of excrement,Portion of faeces,Portion of fecal material,Portion of fecal matter,Portion of feces,Portion of guano,Portion of scat,Portionem cacas,Scat,Spoor,Spraint,Stool,Teil der fäkalien@de,Feces,feces
Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
Anxiety disorder anxiety,anxiety disorder,anxiety disorders,anxiety neuroses,anxiety neurosis,anxiety state,anxiety/mood disorders,chronic stress,mood and anxiety disorder,mood and anxiety disorders,neurotic anxiety states,Anxiety disorder
Group 0 name Corresponds to the control (unexposed) group for case-control studies
Baseline samples (BSL)
Group 1 name Corresponds to the case (exposed) group for case-control studies
Post sleep deprivation samples (7d-SD)
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Samples collected from rats after being subjected to 7 days of sleep deprivation (7d-SD).
Group 0 sample size Number of subjects in the control (unexposed) group
30
Group 1 sample size Number of subjects in the case (exposed) group
29

Lab analysis

Sequencing type
WMS
16S variable region One or more hypervariable region(s) of the bacterial 16S gene
Not specified
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).
centered log-ratio
Statistical test
LEfSe
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
3

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Chao1 Abundance-based estimator of species richness
increased

Signature 1

Needs review

Curated date: 2024/03/18

Curator: Iman-Ngwepe

Revision editor(s): Iman-Ngwepe, Aleru Divine

Source: Fig.3d

Description: LEfSe analysis identified bacteria species that significantly differed (FDR <0.05 and LDA >3) among samples.

Abundance in Group 1: increased abundance in Post sleep deprivation samples (7d-SD)

NCBI Quality ControlLinks
Escherichia coli
Bacteroides uniformis
Oligella ureolytica
Prevotella sp. MGM2
Streptococcus hyointestinalis
Phocaeicola vulgatus
Desulfovibrionaceae bacterium
Adlercreutzia equolifaciens
Bifidobacterium pseudolongum
Vagococcus lutrae

Revision editor(s): Iman-Ngwepe, Aleru Divine

Signature 2

Needs review

Curated date: 2024/03/18

Curator: Iman-Ngwepe

Revision editor(s): Iman-Ngwepe, Aleru Divine

Source: Fig.3d

Description: LEfSe analysis identified bacteria species that significantly differed (FDR <0.05 and LDA >3) among samples.

Abundance in Group 1: decreased abundance in Post sleep deprivation samples (7d-SD)

NCBI Quality ControlLinks
Prevotella sp. P2-180
Akkermansia muciniphila
Phocaeicola sartorii
Lactobacillus johnsonii
Corynebacterium stationis
Parabacteroides distasonis
Prevotella sp. CAG:1031
Bacteroides caecimuris
Psychrobacter pasteurii
Phocaeicola dorei
Bacteroides thetaiotaomicron
Aerococcaceae bacterium

Revision editor(s): Iman-Ngwepe, Aleru Divine

Experiment 2


Needs review

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine

Differences from previous experiment shown

Subjects

Group 1 name Corresponds to the case (exposed) group for case-control studies
Saline supplementation - SA (21d-SA)
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Samples collected from rats after 14 days of saline supplementation (21d-SA).
Group 1 sample size Number of subjects in the case (exposed) group
15

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Chao1 Abundance-based estimator of species richness
unchanged

Signature 1

Needs review

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine

Source: Fig.3d

Description: LEfSe analysis identified bacteria species that significantly differed (FDR <0.05 and LDA >3) among samples.

Abundance in Group 1: increased abundance in Saline supplementation - SA (21d-SA)

NCBI Quality ControlLinks
Prevotella sp. P2-180
Corynebacterium stationis
Oligella ureolytica
Prevotella sp. MGM2
Streptococcus hyointestinalis
Prevotella sp. CAG:1031
Desulfovibrionaceae bacterium
Adlercreutzia equolifaciens
Aerococcaceae bacterium
Bifidobacterium pseudolongum
Vagococcus lutrae

Revision editor(s): Aleru Divine

Signature 2

Needs review

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine

Source: Fig.3d

Description: LEfSe analysis identified bacteria species that significantly differed (FDR <0.05 and LDA >3) among samples.

Abundance in Group 1: decreased abundance in Saline supplementation - SA (21d-SA)

NCBI Quality ControlLinks
Akkermansia muciniphila
Bifidobacterium pseudolongum
Vagococcus lutrae
Escherichia coli
Bacteroides uniformis
Phocaeicola sartorii
Lactobacillus johnsonii
Parabacteroides distasonis
Bacteroides caecimuris
Phocaeicola vulgatus
Psychrobacter pasteurii
Phocaeicola dorei
Bacteroides thetaiotaomicron

Revision editor(s): Aleru Divine

Experiment 3


Needs review

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine

Differences from previous experiment shown

Subjects

Group 1 name Corresponds to the case (exposed) group for case-control studies
Multi-probiotic supplementation - MP (21d-MP)
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Samples collected from rats after 14 days of multi-probiotic supplementation (21d-MP).
Group 1 sample size Number of subjects in the case (exposed) group
14

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Chao1 Abundance-based estimator of species richness
unchanged

Signature 1

Needs review

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine

Source: Fig.3d

Description: LEfSe analysis identified bacteria species that significantly differed (FDR <0.05 and LDA >3) among samples.

Abundance in Group 1: increased abundance in Multi-probiotic supplementation - MP (21d-MP)

NCBI Quality ControlLinks
Prevotella sp. CAG:1031
Prevotella sp. MGM2
Prevotella sp. P2-180
Escherichia coli
Lactobacillus johnsonii
Corynebacterium stationis
Oligella ureolytica
Streptococcus hyointestinalis
Psychrobacter pasteurii
Adlercreutzia equolifaciens
Bifidobacterium pseudolongum
Aerococcaceae bacterium
Vagococcus lutrae

Revision editor(s): Aleru Divine

Signature 2

Needs review

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine

Source: Fig.3d

Description: LEfSe analysis identified bacteria species that significantly differed (FDR <0.05 and LDA >3) among samples.

Abundance in Group 1: decreased abundance in Multi-probiotic supplementation - MP (21d-MP)

NCBI Quality ControlLinks
Akkermansia muciniphila
Bacteroides uniformis
Phocaeicola sartorii
Parabacteroides distasonis
Bacteroides caecimuris
Phocaeicola vulgatus
Phocaeicola dorei
Desulfovibrionaceae bacterium
Bacteroides thetaiotaomicron

Revision editor(s): Aleru Divine

Experiment 4


Needs review

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
Post sleep deprivation samples (7d-SD)
Group 1 name Corresponds to the case (exposed) group for case-control studies
Saline supplementation - SA (21d-SA)
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Samples collected from rats after 14 days of saline supplementation (21d-SA).
Group 0 sample size Number of subjects in the control (unexposed) group
29
Group 1 sample size Number of subjects in the case (exposed) group
15

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Chao1 Abundance-based estimator of species richness
unchanged

Signature 1

Needs review

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine

Source: Fig.3d

Description: LEfSe analysis identified bacteria species that significantly differed (FDR <0.05 and LDA >3) among samples.

Abundance in Group 1: increased abundance in Saline supplementation - SA (21d-SA)

NCBI Quality ControlLinks
Prevotella sp. P2-180
Lactobacillus johnsonii
Corynebacterium stationis
Prevotella sp. MGM2
Streptococcus hyointestinalis
Prevotella sp. CAG:1031
Aerococcaceae bacterium

Revision editor(s): Aleru Divine

Signature 2

Needs review

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine

Source: Fig.3d

Description: LEfSe analysis identified bacteria species that significantly differed (FDR <0.05 and LDA >3) among samples.

Abundance in Group 1: decreased abundance in Saline supplementation - SA (21d-SA)

NCBI Quality ControlLinks
Akkermansia muciniphila
Escherichia coli
Bacteroides uniformis
Phocaeicola sartorii
Bacteroides caecimuris
Phocaeicola vulgatus
Psychrobacter pasteurii
Phocaeicola dorei
Oligella ureolytica
Parabacteroides distasonis
Bifidobacterium pseudolongum
Vagococcus lutrae
Desulfovibrionaceae bacterium
Bacteroides thetaiotaomicron
Adlercreutzia equolifaciens

Revision editor(s): Aleru Divine

Experiment 5


Needs review

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine

Differences from previous experiment shown

Subjects

Group 1 name Corresponds to the case (exposed) group for case-control studies
Multi-probiotic supplementation - MP (21d-MP)
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Samples collected from rats after 14 days of multi-probiotic supplementation (21d-MP).
Group 1 sample size Number of subjects in the case (exposed) group
14

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Chao1 Abundance-based estimator of species richness
unchanged

Signature 1

Needs review

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine

Source: Fig.3d

Description: LEfSe analysis identified bacteria species that significantly differed (FDR <0.05 and LDA >3) among samples.

Abundance in Group 1: increased abundance in Multi-probiotic supplementation - MP (21d-MP)

NCBI Quality ControlLinks
Prevotella sp. P2-180
Lactobacillus johnsonii
Corynebacterium stationis
Oligella ureolytica
Prevotella sp. MGM2
Streptococcus hyointestinalis
Prevotella sp. CAG:1031
Psychrobacter pasteurii
Adlercreutzia equolifaciens
Aerococcaceae bacterium
Vagococcus lutrae

Revision editor(s): Aleru Divine

Signature 2

Needs review

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine

Source: Fig.3d

Description: LEfSe analysis identified bacteria species that significantly differed (FDR <0.05 and LDA >3) among samples.

Abundance in Group 1: decreased abundance in Multi-probiotic supplementation - MP (21d-MP)

NCBI Quality ControlLinks
Akkermansia muciniphila
Escherichia coli
Bacteroides uniformis
Phocaeicola sartorii
Parabacteroides distasonis
Bacteroides caecimuris
Phocaeicola vulgatus
Phocaeicola dorei
Desulfovibrionaceae bacterium
Bacteroides thetaiotaomicron
Bifidobacterium pseudolongum

Revision editor(s): Aleru Divine

Experiment 6


Needs review

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
Saline supplementation - SA (21d-SA)
Group 0 sample size Number of subjects in the control (unexposed) group
15

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Chao1 Abundance-based estimator of species richness
unchanged

Signature 1

Needs review

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine

Source: Fig.3d

Description: LEfSe analysis identified bacteria species that significantly differed (FDR <0.05 and LDA >3) among samples.

Abundance in Group 1: increased abundance in Multi-probiotic supplementation - MP (21d-MP)

NCBI Quality ControlLinks
Escherichia coli
Akkermansia muciniphila
Lactobacillus johnsonii
Corynebacterium stationis
Oligella ureolytica
Streptococcus hyointestinalis
Psychrobacter pasteurii
Bacteroides thetaiotaomicron
Adlercreutzia equolifaciens
Bifidobacterium pseudolongum
Aerococcaceae bacterium
Vagococcus lutrae

Revision editor(s): Aleru Divine

Signature 2

Needs review

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine

Source: Fig.3d

Description: LEfSe analysis identified bacteria species that significantly differed (FDR <0.05 and LDA >3) among samples.

Abundance in Group 1: decreased abundance in Multi-probiotic supplementation - MP (21d-MP)

NCBI Quality ControlLinks
Akkermansia muciniphila
Prevotella sp. P2-180
Bacteroides uniformis
Phocaeicola sartorii
Parabacteroides distasonis
Prevotella sp. MGM2
Prevotella sp. CAG:1031
Bacteroides caecimuris
Phocaeicola vulgatus
Phocaeicola dorei
Desulfovibrionaceae bacterium
Bacteroides thetaiotaomicron

Revision editor(s): Aleru Divine