Peripheral neuronal activation shapes the microbiome and alters gut physiology

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Reviewed Marked as Reviewed by KateRasheed on 2025-4-30
study design
laboratory experiment
Citation
PMID PubMed identifier for scientific articles.
38517896
DOI Digital object identifier for electronic documents.
https://doi.org/10.1016/j.celrep.2024.113953
URI Uniform resource identifier for web resources.
Authors
Griffiths JA, Yoo BB, Thuy-Boun P, Cantu VJ, Weldon KC, Challis C, Sweredoski MJ, Chan KY, Thron TM, Sharon G, Moradian A, Humphrey G, Zhu Q, Shaffer JP, Wolan DW, Dorrestein PC, Knight R, Gradinaru V, Mazmanian SK
Journal
Cell reports
Year
2024
Keywords:
Akkermansia muciniphila, CP: Microbiology, CP: Neuroscience, cholinergic, dopaminergic, enteric nervous system, gut microbiome, gut motility, noradrenergic, peripheral nervous system
The gastrointestinal (GI) tract is innervated by intrinsic neurons of the enteric nervous system (ENS) and extrinsic neurons of the central nervous system and peripheral ganglia. The GI tract also harbors a diverse microbiome, but interactions between the ENS and the microbiome remain poorly understood. Here, we activate choline acetyltransferase (ChAT)-expressing or tyrosine hydroxylase (TH)-expressing gut-associated neurons in mice to determine effects on intestinal microbial communities and their metabolites as well as on host physiology. The resulting multi-omics datasets support broad roles for discrete peripheral neuronal subtypes in shaping microbiome structure, including modulating bile acid profiles and fungal colonization. Physiologically, activation of either ChAT+ or TH+ neurons increases fecal output, while only ChAT+ activation results in increased colonic contractility and diarrhea-like fluid secretion. These findings suggest that specific subsets of peripherally activated neurons differentially regulate the gut microbiome and GI physiology in mice without involvement of signals from the brain.

Experiment 1


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Reviewed Marked as Reviewed by KateRasheed on 2025-4-30

Curated date: 2025/04/17

Curator: PreciousChijioke

Revision editor(s): PreciousChijioke, KateRasheed

Subjects

Location of subjects
United States of America
Host species Species from which microbiome was sampled. Contact us to have more species added.
Mus musculus
Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
Cecum mucosa Caecum mucosa,Caecum mucosa of organ,Caecum mucous membrane,Caecum organ mucosa,Cecal mucosa,Cecum mucosa of organ,Cecum mucous membrane,Cecum organ mucosa,Intestinum crassum caecum mucosa,Intestinum crassum caecum mucosa of organ,Intestinum crassum caecum mucous membrane,Intestinum crassum caecum organ mucosa,Mucosa of caecum,Mucosa of cecum,Mucosa of intestinum crassum caecum,Mucosa of organ of caecum,Mucosa of organ of cecum,Mucosa of organ of intestinum crassum caecum,Mucous membrane of caecum,Mucous membrane of cecum,Mucous membrane of intestinum crassum caecum,Organ mucosa of caecum,Organ mucosa of cecum,Organ mucosa of intestinum crassum caecum,Cecum mucosa,cecum mucosa
Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
Peripheral neuron Peripheral neuron,peripheral neuron
Group 0 name Corresponds to the control (unexposed) group for case-control studies
Control mice
Group 1 name Corresponds to the case (exposed) group for case-control studies
ChAT+ (Choline acetyltransferase) -activated mice
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
ChAT+ (Choline acetyltransferase) -activated mice were treated with C21 ( compound 21) (3 mg/kg) administered daily for 10 consecutive days.

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)?
No
LDA Score above Threshold for the linear discriminant analysis (LDA) score for studies using the popular LEfSe tool
2


Signature 1

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Reviewed Marked as Reviewed by KateRasheed on 2025-4-30

Curated date: 2025/04/17

Curator: PreciousChijioke

Revision editor(s): PreciousChijioke, KateRasheed

Source: Fig 2K

Description: Gut-associated ChAT+ and TH+ neuronal activation alters the gut microbiome

Abundance in Group 1: increased abundance in ChAT+ (Choline acetyltransferase) -activated mice

NCBI Quality ControlLinks
Akkermansiaceae   
Bifidobacteriaceae   
Marinilabiliaceae   

Revision editor(s): PreciousChijioke, KateRasheed

Signature 2

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Reviewed Marked as Reviewed by KateRasheed on 2025-4-30

Curated date: 2025/04/17

Curator: PreciousChijioke

Revision editor(s): PreciousChijioke

Source: Fig 2K

Description: Gut-associated ChAT+ and TH+ neuronal activation alters the gut microbiome

Abundance in Group 1: decreased abundance in ChAT+ (Choline acetyltransferase) -activated mice

NCBI Quality ControlLinks
Barnesiellaceae   
Clostridiaceae   
Enterococcaceae   
Erysipelotrichaceae   
Eubacteriaceae   
Lachnospiraceae   
Odoribacteraceae   
Oscillospiraceae   
Prevotellaceae   
Rikenellaceae   
Eubacteriales Family XIII. Incertae Sedis bacterium   

Revision editor(s): PreciousChijioke

Experiment 2


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Reviewed Marked as Reviewed by KateRasheed on 2025-4-30

Curated date: 2025/04/17

Curator: PreciousChijioke

Revision editor(s): PreciousChijioke, KateRasheed

Differences from previous experiment shown

Subjects

Group 1 name Corresponds to the case (exposed) group for case-control studies
TH+ (Tyrosine hydroxylase) -activated mice
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
TH+ (Tyrosine hydroxylase) -activated mice were treated with C21 ( compound 21) (3 mg/kg) administered daily for 10 consecutive days.

Lab analysis

Statistical Analysis

Signature 1

EditHistoryDelete
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Reviewed Marked as Reviewed by KateRasheed on 2025-4-30

Curated date: 2025/04/17

Curator: PreciousChijioke

Revision editor(s): PreciousChijioke

Source: Fig 2M

Description: Gut-associated ChAT+ and TH+ neuronal activation alters the gut microbiome

Abundance in Group 1: increased abundance in TH+ (Tyrosine hydroxylase) -activated mice

NCBI Quality ControlLinks
Bacteroidaceae   
Prevotellaceae   
Tannerellaceae   

Revision editor(s): PreciousChijioke

Signature 2

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Reviewed Marked as Reviewed by KateRasheed on 2025-4-30

Curated date: 2025/04/17

Curator: PreciousChijioke

Revision editor(s): PreciousChijioke

Source: Fig 2M

Description: Gut-associated ChAT+ and TH+ neuronal activation alters the gut microbiome

Abundance in Group 1: decreased abundance in TH+ (Tyrosine hydroxylase) -activated mice

NCBI Quality ControlLinks
Eggerthellaceae   
Lachnospiraceae   

Revision editor(s): PreciousChijioke

Experiment 3


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Reviewed Marked as Reviewed by KateRasheed on 2025-4-30

Curated date: 2025/04/17

Curator: PreciousChijioke

Revision editor(s): PreciousChijioke, KateRasheed

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
Contol mice on day 10
Group 1 name Corresponds to the case (exposed) group for case-control studies
ChAT+ (Choline acetyltransferase) -activated mice on day 10
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
ChAT+ (Choline acetyltransferase) -activated mice were treated with C21 ( compound 21) (3 mg/kg) administered daily for 10 consecutive days.

Lab analysis

Statistical Analysis

Alpha Diversity

Faith Phylogenetic diversity, takes into account phylogenetic distance of all taxa identified in a sample
decreased

Signature 1

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Reviewed Marked as Reviewed by KateRasheed on 2025-4-30

Curated date: 2025/04/17

Curator: PreciousChijioke

Revision editor(s): PreciousChijioke

Source: Fig S6

Description: Annotated changes in gut bacteria

Abundance in Group 1: increased abundance in ChAT+ (Choline acetyltransferase) -activated mice on day 10

NCBI Quality ControlLinks
Akkermansia muciniphila   
Thomasclavelia spiroformis   
Bacillus   
Hoylesella timonensis   
Bifidobacterium pseudolongum   
Anaerostipes caccae   

Revision editor(s): PreciousChijioke

Signature 2

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Reviewed Marked as Reviewed by KateRasheed on 2025-4-30

Curated date: 2025/04/17

Curator: PreciousChijioke

Revision editor(s): PreciousChijioke

Source: Fig S6

Description: Annotated changes in gut bacteria

Abundance in Group 1: decreased abundance in ChAT+ (Choline acetyltransferase) -activated mice on day 10

NCBI Quality ControlLinks
Agathobaculum desmolans   
Alistipes communis   
Alistipes finegoldii   
Alistipes putredinis   
Alistipes senegalensis   
Allofournierella massiliensis   
Anaerotignum lactatifermentans   
Anaerotruncus sp. G3(2012)   
Bacteroides fragilis   
Barnesiella viscericola   
Blautia hansenii   
Blautia obeum   
Blautia sp. KLE 1732   
Butyricimonas synergistica   
Butyricimonas virosa   
Clostridium sp. L2-50   
Clostridium sp. SY8519   
Coprococcus comes   
Coprococcus eutactus   
Dorea sp. 5-2   
Eisenbergiella tayi   
Enterococcus faecalis   
Eubacterium plexicaudatum   
Eubacterium sp. 14-2   
Faecalicatena contorta   
Firmicutes bacterium ASF500   
Flavonifractor plautii   
Hoylesella buccalis   
Intestinimonas massiliensis (ex Afouda et al. 2020)   
Lachnospiraceae bacterium 3-1   
Lachnospiraceae bacterium A2   
Marvinbryantia formatexigens   
Merdimmobilis hominis   
Oscillibacter sp. 1-3   
Oscillibacter valericigenes   
Roseburia hominis   
Ruminococcus gauvreauii   
Ruthenibacterium lactatiformans   
Subdoligranulum variabile   
[Clostridium] methylpentosum   
[Clostridium] nexile   
[Clostridium] symbiosum   
Clostridium ASF536Clostridium ASF536
Candidatus Stoquefichus sp. SB1   
Lachnospiraceae bacterium 10-1   
Lachnospiraceae bacterium MA2020   
Lachnospiraceae bacterium M18-1   
Lachnospiraceae bacterium 28-4   

Revision editor(s): PreciousChijioke

Experiment 4


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Reviewed Marked as Reviewed by KateRasheed on 2025-4-30

Curated date: 2025/04/17

Curator: PreciousChijioke

Revision editor(s): PreciousChijioke, KateRasheed

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
Control mice on day 10
Group 1 name Corresponds to the case (exposed) group for case-control studies
TH+ (Tyrosine hydroxylase) -activated mice on day 10
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
TH+ (Tyrosine hydroxylase) -activated mice were treated with C21 ( compound 21) (3 mg/kg) administered daily for 10 consecutive days.

Lab analysis

Statistical Analysis

Alpha Diversity

Faith Phylogenetic diversity, takes into account phylogenetic distance of all taxa identified in a sample
unchanged

Signature 1

EditHistoryDelete
Flag for review
Your review change was submitted
Reviewed Marked as Reviewed by KateRasheed on 2025-4-30

Curated date: 2025/04/18

Curator: PreciousChijioke

Revision editor(s): PreciousChijioke

Source: Fig S6

Description: Annotated changes in gut bacteria

Abundance in Group 1: increased abundance in TH+ (Tyrosine hydroxylase) -activated mice on day 10

NCBI Quality ControlLinks
Desulfovibrio piger   
Thomasclavelia spiroformis   
Oscillibacter sp. KLE 1745   
Mediterraneibacter gnavus   
Intestinimonas butyriciproducens   
Parabacteroides goldsteinii   
Odoribacter laneus   
Alistipes communis   
Alistipes timonensis   
Alistipes senegalensis   
Bacteroides uniformis   
Phocaeicola vulgatus   
Bacteroides stercoris   
Bacteroides salyersiae   
Bacteroides pyogenes   
Bacteroides thetaiotaomicron   
Prevotella dentalis   
Hoylesella enoeca   

Revision editor(s): PreciousChijioke

Signature 2

EditHistoryDelete
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Your review change was submitted
Reviewed Marked as Reviewed by KateRasheed on 2025-4-30

Curated date: 2025/04/18

Curator: PreciousChijioke

Revision editor(s): PreciousChijioke

Source: Fig S6

Description: Annotated changes in gut bacteria

Abundance in Group 1: decreased abundance in TH+ (Tyrosine hydroxylase) -activated mice on day 10

NCBI Quality ControlLinks
Adlercreutzia caecimuris   
Adlercreutzia mucosicola   
Lachnospiraceae bacterium A2   
Lachnospiraceae bacterium MD335   
Mediterraneibacter massiliensis   
Lachnospiraceae bacterium 28-4   
Lachnospiraceae bacterium 2_1_46FAA   

Revision editor(s): PreciousChijioke

Experiment 5


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Reviewed Marked as Reviewed by KateRasheed on 2025-4-30

Curated date: 2025/04/18

Curator: PreciousChijioke

Revision editor(s): PreciousChijioke, KateRasheed

Differences from previous experiment shown

Subjects

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
Group 1 name Corresponds to the case (exposed) group for case-control studies
ChAT+ (Choline acetyltransferase) -activated mice on day 10
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
ChAT+ (Choline acetyltransferase) -activated mice were treated with C21 ( compound 21) (3 mg/kg) administered daily for 10 consecutive days.

Lab analysis

Statistical Analysis

Alpha Diversity

Faith Phylogenetic diversity, takes into account phylogenetic distance of all taxa identified in a sample
decreased

Signature 1

EditHistoryDelete
Flag for review
Your review change was submitted
Reviewed Marked as Reviewed by KateRasheed on 2025-4-30

Curated date: 2025/04/18

Curator: PreciousChijioke

Revision editor(s): PreciousChijioke

Source: Fig S7

Description: Gut-Associated Activation-Meditated Changes in the Fecal Microbiome

Abundance in Group 1: increased abundance in ChAT+ (Choline acetyltransferase) -activated mice on day 10

NCBI Quality ControlLinks
Akkermansia   
Akkermansiaceae   
Verrucomicrobiales   

Revision editor(s): PreciousChijioke

Signature 2

EditHistoryDelete
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Your review change was submitted
Reviewed Marked as Reviewed by KateRasheed on 2025-4-30

Curated date: 2025/04/19

Curator: PreciousChijioke

Revision editor(s): PreciousChijioke

Source: Fig S7

Description: Gut-Associated Activation-Meditated Changes in the Fecal Microbiome

Abundance in Group 1: decreased abundance in ChAT+ (Choline acetyltransferase) -activated mice on day 10

NCBI Quality ControlLinks
Adlercreutzia   
Alistipes   
Anaerofustis   
Anaerotruncus   
Barnesiella   
Barnesiellaceae   
Bifidobacteriaceae   
Bifidobacteriales   
Bifidobacterium   
Blautia   
Burkholderiales   
Candidatus Stoquefichus   
Cellulomonadaceae   
Cellulomonas   
Clostridiaceae   
Clostridium   
Coprobacter   
Coprococcus   
Dorea   
Eisenbergiella   
Enterococcaceae   
Enterococcus   
Erysipelotrichaceae   
Erysipelotrichales   
Eubacteriaceae   
Eubacteriales   
Eubacterium   
Faecalicatena   
Faecalitalea   
Flavobacteriales   
Intestinimonas   
Lachnoclostridium   
Lachnospiraceae   
Lawsonia   
Marinilabiliales   
Marvinbryantia   
Micrococcales   
Oscillibacter   
Oscillospiraceae   
Parabacteroides   
Parasutterella   
Prevotella   
Prevotellaceae   
Pseudoflavonifractor   
Rikenella   
Rikenellaceae   
Ruminiclostridium   
Ruminococcus   
Ruthenibacterium   
Sellimonas   
Spirochaetaceae   
Spirochaetales   
Sutterellaceae   
Tannerellaceae   
Treponema   
Tyzzerella   
Varicellovirus   

Revision editor(s): PreciousChijioke

Experiment 6


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Reviewed Marked as Reviewed by KateRasheed on 2025-4-30

Curated date: 2025/04/18

Curator: PreciousChijioke

Revision editor(s): PreciousChijioke, KateRasheed

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
Control mice on day 6
Group 1 name Corresponds to the case (exposed) group for case-control studies
TH+ (Tyrosine hydroxylase) -activated mice on day 6
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
TH+ (Tyrosine hydroxylase) -activated mice were treated with C21 ( compound 21) (3 mg/kg) administered daily for 10 consecutive days.

Lab analysis

Statistical Analysis

Alpha Diversity

Faith Phylogenetic diversity, takes into account phylogenetic distance of all taxa identified in a sample
unchanged

Signature 1

EditHistoryDelete
Flag for review
Your review change was submitted
Reviewed Marked as Reviewed by KateRasheed on 2025-4-30

Curated date: 2025/04/18

Curator: PreciousChijioke

Revision editor(s): PreciousChijioke

Source: Fig S7

Description: Gut-Associated Activation-Meditated Changes in the Fecal Microbiome

Abundance in Group 1: increased abundance in TH+ (Tyrosine hydroxylase) -activated mice on day 6

NCBI Quality ControlLinks
Parabacteroides   
Tannerellaceae   

Revision editor(s): PreciousChijioke

Signature 2

EditHistoryDelete
Flag for review
Your review change was submitted
Reviewed Marked as Reviewed by KateRasheed on 2025-4-30

Curated date: 2025/04/18

Curator: PreciousChijioke

Revision editor(s): PreciousChijioke

Source: Fig S7

Description: Gut-Associated Activation-Meditated Changes in the Fecal Microbiome

Abundance in Group 1: decreased abundance in TH+ (Tyrosine hydroxylase) -activated mice on day 6

NCBI Quality ControlLinks
Blautia   
Clostridioides   
Clostridium   
Eisenbergiella   
Flavobacteriales   
Pseudoflavonifractor   
Streptococcaceae   
Streptococcus   
Fluvicola   

Revision editor(s): PreciousChijioke

Experiment 7


EditHistoryDelete
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Reviewed Marked as Reviewed by KateRasheed on 2025-4-30

Curated date: 2025/04/30

Curator: PreciousChijioke

Revision editor(s): PreciousChijioke, KateRasheed

Differences from previous experiment shown

Subjects

Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
Cecum mucosa Caecum mucosa,Caecum mucosa of organ,Caecum mucous membrane,Caecum organ mucosa,Cecal mucosa,Cecum mucosa of organ,Cecum mucous membrane,Cecum organ mucosa,Intestinum crassum caecum mucosa,Intestinum crassum caecum mucosa of organ,Intestinum crassum caecum mucous membrane,Intestinum crassum caecum organ mucosa,Mucosa of caecum,Mucosa of cecum,Mucosa of intestinum crassum caecum,Mucosa of organ of caecum,Mucosa of organ of cecum,Mucosa of organ of intestinum crassum caecum,Mucous membrane of caecum,Mucous membrane of cecum,Mucous membrane of intestinum crassum caecum,Organ mucosa of caecum,Organ mucosa of cecum,Organ mucosa of intestinum crassum caecum,Cecum mucosa,cecum mucosa
Group 0 name Corresponds to the control (unexposed) group for case-control studies
Control mice on day 10
Group 1 name Corresponds to the case (exposed) group for case-control studies
ChAT+ (Choline acetyltransferase) -activated mice on day 10
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
ChAT+ (Choline acetyltransferase) -activated mice were treated with C21 ( compound 21) (3 mg/kg) administered daily for 10 consecutive days.

Lab analysis

Statistical Analysis

Statistical test
T-Test
LDA Score above Threshold for the linear discriminant analysis (LDA) score for studies using the popular LEfSe tool
Not specified

Alpha Diversity

Faith Phylogenetic diversity, takes into account phylogenetic distance of all taxa identified in a sample
decreased

Signature 1

EditHistoryDelete
Flag for review
Your review change was submitted
Reviewed Marked as Reviewed by KateRasheed on 2025-4-30

Curated date: 2025/04/30

Curator: PreciousChijioke

Revision editor(s): PreciousChijioke

Source: Fig 2N

Description: Gut-associated ChAT+ and TH+ neuronal activation alters the gut microbiome

Abundance in Group 1: increased abundance in ChAT+ (Choline acetyltransferase) -activated mice on day 10

NCBI Quality ControlLinks
Akkermansia   

Revision editor(s): PreciousChijioke

Experiment 8


EditHistoryDelete
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Reviewed Marked as Reviewed by KateRasheed on 2025-4-30

Curated date: 2025/04/30

Curator: PreciousChijioke

Revision editor(s): PreciousChijioke, KateRasheed

Differences from previous experiment shown

Subjects

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


Lab analysis

Statistical Analysis

Alpha Diversity

Faith Phylogenetic diversity, takes into account phylogenetic distance of all taxa identified in a sample
decreased

Signature 1

EditHistoryDelete
Flag for review
Your review change was submitted
Reviewed Marked as Reviewed by KateRasheed on 2025-4-30

Curated date: 2025/04/30

Curator: PreciousChijioke

Revision editor(s): PreciousChijioke

Source: Fig 2N

Description: Gut-associated ChAT+ and TH+ neuronal activation alters the gut microbiome

Abundance in Group 1: increased abundance in ChAT+ (Choline acetyltransferase) -activated mice on day 10

NCBI Quality ControlLinks
Akkermansia   

Revision editor(s): PreciousChijioke

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