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

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Reviewed Marked as Reviewed by Svetlana up on 2024-7-31
study design
laboratory experiment
Citation
PMID PubMed identifier for scientific articles.
38421192
DOI Digital object identifier for electronic documents.
https://doi.org/10.1128/spectrum.01437-23
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


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Curated date: 2024/03/18

Curator: Iman-Ngwepe

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

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).
relative abundances
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

EditHistoryDelete
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Reviewed Marked as Reviewed by Svetlana up on 2024-7-31

Curated date: 2024/03/18

Curator: Iman-Ngwepe

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

Source: Fig.3d

Description: LEfSe analysis identified bacteria species that significantly differed in baseline (BSL) versus 7 days of sleep deprivation (7d-SD) samples.

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

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

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

Signature 2

EditHistoryDelete
Flag for review
Your review change was submitted
Reviewed Marked as Reviewed by Svetlana up on 2024-7-31

Curated date: 2024/03/18

Curator: Iman-Ngwepe

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

Source: Fig.3d

Description: LEfSe analysis identified bacteria species that significantly differed in baseline (BSL) versus 7 days of sleep deprivation (7d-SD) samples.

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

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

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

Experiment 2


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Reviewed Marked as Reviewed by Svetlana up on 2024-7-31

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine, Scholastica

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

EditHistoryDelete
Flag for review
Your review change was submitted
Reviewed Marked as Reviewed by Svetlana up on 2024-7-31

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine, Scholastica

Source: Fig.3d

Description: LEfSe analysis identified bacteria species that significantly differed in baseline (BSL) versus 14 days of saline supplementation (21d-SA) samples

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

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

Revision editor(s): Aleru Divine, Scholastica

Signature 2

EditHistoryDelete
Flag for review
Your review change was submitted
Reviewed Marked as Reviewed by Svetlana up on 2024-7-31

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine, Scholastica

Source: Fig.3d

Description: LEfSe analysis identified bacteria species that significantly differed in baseline (BSL) versus 14 days of saline supplementation (21d-SA) samples

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

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

Revision editor(s): Aleru Divine, Scholastica

Experiment 3


EditHistoryDelete
Flag for review
Your review change was submittedDuplicate this ExperimentAdd a new Signature
Reviewed Marked as Reviewed by Svetlana up on 2024-7-31

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine, Scholastica

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

EditHistoryDelete
Flag for review
Your review change was submitted
Reviewed Marked as Reviewed by Svetlana up on 2024-7-31

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine, Scholastica

Source: Fig.3d

Description: LEfSe analysis identified bacteria species that significantly differed in baseline (BSL) versus 14 days of multi-probiotic supplementation (21d-MP) samples.

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

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

Revision editor(s): Aleru Divine, Scholastica

Signature 2

EditHistoryDelete
Flag for review
Your review change was submitted
Reviewed Marked as Reviewed by Svetlana up on 2024-7-31

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine, Scholastica

Source: Fig.3d

Description: LEfSe analysis identified bacteria species that significantly differed in baseline (BSL) versus 14 days of multi-probiotic supplementation (21d-MP) samples.

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

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

Revision editor(s): Aleru Divine, Scholastica

Experiment 4


EditHistoryDelete
Flag for review
Your review change was submittedDuplicate this ExperimentAdd a new Signature
Reviewed Marked as Reviewed by Svetlana up on 2024-7-31

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine, Scholastica

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

EditHistoryDelete
Flag for review
Your review change was submitted
Reviewed Marked as Reviewed by Svetlana up on 2024-7-31

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine, Scholastica

Source: Fig.3d

Description: LEfSe analysis identified bacteria species that significantly differed in post sleep deprivation (7d-SD) versus 14 days of saline supplementation (21d-SA) samples

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

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

Revision editor(s): Aleru Divine, Scholastica

Signature 2

EditHistoryDelete
Flag for review
Your review change was submitted
Reviewed Marked as Reviewed by Svetlana up on 2024-7-31

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine, Scholastica

Source: Fig.3d

Description: LEfSe analysis identified bacteria species that significantly differed in post sleep deprivation (7d-SD) versus 14 days of saline supplementation (21d-SA) samples

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

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

Revision editor(s): Aleru Divine, Scholastica

Experiment 5


EditHistoryDelete
Flag for review
Your review change was submittedDuplicate this ExperimentAdd a new Signature
Reviewed Marked as Reviewed by Svetlana up on 2024-7-31

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine, Scholastica

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

EditHistoryDelete
Flag for review
Your review change was submitted
Reviewed Marked as Reviewed by Svetlana up on 2024-7-31

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine, Scholastica

Source: Fig.3d

Description: LEfSe analysis identified bacteria species that significantly differed in post sleep deprivation (7d-SD) versus 14 days of multi-probiotic supplementation (21d-MP) samples

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

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

Revision editor(s): Aleru Divine, Scholastica

Signature 2

EditHistoryDelete
Flag for review
Your review change was submitted
Reviewed Marked as Reviewed by Svetlana up on 2024-7-31

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine, Scholastica

Source: Fig.3d

Description: LEfSe analysis identified bacteria species that significantly differed in post sleep deprivation (7d-SD) versus 14 days of multi-probiotic supplementation (21d-MP) samples

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

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

Revision editor(s): Aleru Divine, Scholastica

Experiment 6


EditHistoryDelete
Flag for review
Your review change was submittedDuplicate this ExperimentAdd a new Signature
Reviewed Marked as Reviewed by Svetlana up on 2024-7-31

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine, Scholastica

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

EditHistoryDelete
Flag for review
Your review change was submitted
Reviewed Marked as Reviewed by Svetlana up on 2024-7-31

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine, Scholastica

Source: Fig.3d

Description: LEfSe analysis identified bacteria species that significantly differed in 14 days of saline supplementation (21d-SA) versus 14 days of multi-probiotic supplementation (21d-MP) samples

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

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

Revision editor(s): Aleru Divine, Scholastica

Signature 2

EditHistoryDelete
Flag for review
Your review change was submitted
Reviewed Marked as Reviewed by Svetlana up on 2024-7-31

Curated date: 2024/04/11

Curator: Aleru Divine

Revision editor(s): Aleru Divine, Scholastica

Source: Fig.3d

Description: LEfSe analysis identified bacteria species that significantly differed in 14 days of saline supplementation (21d-SA) versus 14 days of multi-probiotic supplementation (21d-MP) samples

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

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

Revision editor(s): Aleru Divine, Scholastica

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