Changes in social environment impact primate gut microbiota composition

From BugSigDB
Needs review
Citation
PMID PubMed identifier for scientific articles.
DOI Digital object identifier for electronic documents.
URI
Authors
Pearce CS, Bukovsky D, Douchant K, Katoch A, Greenlaw J, Gale DJ, Nashed JY, Brien D, Kuhlmeier VA, Sabbagh MA, Blohm G, De Felice FG, Pare M, Cook DJ, Scott SH, Munoz DP, Sjaarda CP, Tusche A, Sheth PM, Winterborn A, Boehnke S, Gallivan JP
Journal
Animal microbiome
Year
2024
Keywords:
Gut microbiota, Metagenomics, Monkeys, Primates, Social environment, Social living
BACKGROUND: The gut microbiota (GM) has proven to be essential for both physical health and mental wellbeing, yet the forces that ultimately shape its composition remain opaque. One critical force known to affect the GM is the social environment. Prior work in humans and free-ranging non-human primates has shown that cohabitation and frequent social interaction can lead to changes in GM composition. However, it is difficult to assess the direction of causation in these studies, and interpretations are complicated by the influence of uncontrolled but correlated factors, such as shared diet. RESULTS: We performed a 15-month longitudinal investigation wherein we disentangled the impacts of diet and social living conditions on GM composition in a captive cohort of 13 male cynomolgus macaques. The animals were in single housing for the first 3 months of the study initially with a variable diet. After baseline data collection they were placed on a controlled diet for the remainder of the study. Following this diet shift the animals were moved to paired housing for 6 months, enabling enhanced social interaction, and then subsequently returned to single housing at the end of our study. This structured sequencing of diet and housing changes allowed us to assess their distinct impacts on GM composition. We found that the early dietary adjustments led to GM changes in both alpha and beta diversity, whereas changes in social living conditions only altered beta diversity. With respect to the latter, we found that two particular bacterial families - Lactobacillaceae and Clostridiaceae - demonstrated significant shifts in abundance during the transition from single housing to paired housing, which was distinct from the shifts we observed based on a change in diet. Conversely, we found that other bacteria previously associated with sociality were not altered based on changes in social living conditions but rather only by changes in diet. CONCLUSIONS: Together, these findings decouple the influences that diet and social living have on GM composition and reconcile previous observations in the human and animal literatures. Moreover, the results indicate biological alterations of the gut that may, in part, mediate the relationship between sociality and wellbeing.

Experiment 1


Needs review

Curated date: 2024/11/25

Curator: MyleeeA

Revision editor(s): MyleeeA

Subjects

Location of subjects
Canada
Host species Species from which microbiome was sampled. Contact us to have more species added.
Macaca fascicularis
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
Diet Dietary,Diets,Diet,diet
Group 0 name Corresponds to the control (unexposed) group for case-control studies
Uncontrolled diet (T1 single)
Group 1 name Corresponds to the case (exposed) group for case-control studies
Controlled diet (T2 single)
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Following T1Single data collection, at the beginning of the Single Living phase, the enrichment elements of NHP’s diet for the remainder of the study (referred to as “controlled” diet) was strictly controlled. This controlled diet approach directly help to investigate how diet alterations impact GM composition during a period of stable single living, i.e., comparing the transition from uncontrolled (T1Single) to controlled diet (T2Single) during the Single Living phase.
Group 0 sample size Number of subjects in the control (unexposed) group
13
Group 1 sample size Number of subjects in the case (exposed) group
13

Lab analysis

Sequencing type
16S
16S variable region One or more hypervariable region(s) of the bacterial 16S gene
V3-V4
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

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
decreased
Chao1 Abundance-based estimator of species richness
decreased
Richness Number of species
decreased
Faith Phylogenetic diversity, takes into account phylogenetic distance of all taxa identified in a sample
decreased

Signature 1

Needs review

Curated date: 2024/11/27

Curator: MyleeeA

Revision editor(s): MyleeeA

Source: Figure 2C and Figure S7A

Description: Differential relative abundance of bacterial families and genus exhibiting the diet effect. LEfSe analysis identified significantly different taxa between diet-uncontrolled (red, T1Single) and diet-controlled (light blue, T2Single) conditions.

Abundance in Group 1: increased abundance in Controlled diet (T2 single)

NCBI Quality ControlLinks
Betaproteobacteria
Clostridiaceae
Coriobacteriaceae
Eubacteriales
Helicobacter
Helicobacteraceae
Intestinibacter
Intestinimonas
Lentisphaera
Paramuribaculum
Peptostreptococcaceae
Sarcina
Senegalimassilia
Aestuariispira

Revision editor(s): MyleeeA

Signature 2

Needs review

Curated date: 2024/11/27

Curator: MyleeeA

Revision editor(s): MyleeeA

Source: Figure 2C and Figure S7A

Description: Differential relative abundance of bacterial families and genus exhibiting the diet effect. LEfSe analysis identified significantly different taxa between diet-uncontrolled (red, T1Single) and diet-controlled (light blue, T2Single) conditions.

Abundance in Group 1: decreased abundance in Controlled diet (T2 single)

NCBI Quality ControlLinks
Veillonellaceae
Prevotellaceae
Lactobacillaceae
Prevotella
Limosilactobacillus
Lactobacillus
Fusicatenibacter
Faecalibacterium
Coprococcus
Clostridium
Blautia
Anaerobutyricum
Agathobacter
Agathobaculum
Oribacterium

Revision editor(s): MyleeeA

Experiment 2


Needs review

Curated date: 2024/11/28

Curator: MyleeeA

Revision editor(s): MyleeeA

Differences from previous experiment shown

Subjects

Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
Social interaction measurement Social interaction measurement,social interaction measurement
Group 0 name Corresponds to the control (unexposed) group for case-control studies
T2 single
Group 1 name Corresponds to the case (exposed) group for case-control studies
Combination of T3 social, T4 social and T5RSL
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
At the 3-month mark, the Protected Pairwise Social Living phase was implemented and lasted for 6 months, during which T3Social and T4Social data were collected. At the 9-month mark, the Return to Single Living phase was implemented, wherein the macaques were returned to their previous single housing conditions (as in Single Living). The final data collection session, referred to as T5RSL, took place 6 months into this phase.
Group 0 sample size Number of subjects in the control (unexposed) group
Not specified
Group 1 sample size Number of subjects in the case (exposed) group
Not specified

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
increased
Chao1 Abundance-based estimator of species richness
increased
Richness Number of species
increased
Faith Phylogenetic diversity, takes into account phylogenetic distance of all taxa identified in a sample
increased

Experiment 3


Needs review

Curated date: 2024/11/28

Curator: MyleeeA

Revision editor(s): MyleeeA

Differences from previous experiment shown

Subjects

Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
Diet measurement Diet measurement,diet measurement
Group 0 name Corresponds to the control (unexposed) group for case-control studies
T1 Single (Effect of Diet)
Group 1 name Corresponds to the case (exposed) group for case-control studies
T2 Single (Effect of Diet)
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Group with controlled diet (T2Single) during the Single Living phase.

Lab analysis

Statistical Analysis

Statistical test
Mann-Whitney (Wilcoxon)
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
Not specified


Experiment 4


incomplete

Curated date: 2024/11/28

Curator: MyleeeA

Revision editor(s): MyleeeA

Differences from previous experiment shown

Subjects

Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
Social environment measurement Social environment measurement,social environment measurement
Group 0 name Corresponds to the control (unexposed) group for case-control studies
T2Single (effect of moving from single to pairwise living)
Group 1 name Corresponds to the case (exposed) group for case-control studies
T3Social(effect of moving from single to pairwise living)
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
The Protected Pairwise Social Living phase was implemented and lasted for 6 months, during which T3Social and T4Social data were collected.

Lab analysis

Statistical Analysis

MHT correction Have statistical tests be corrected for multiple hypothesis testing (MHT)?
No


Experiment 5


incomplete

Curated date: 2024/11/28

Curator: MyleeeA

Revision editor(s): MyleeeA

Differences from previous experiment shown

Subjects

Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
Social interaction measurement Social interaction measurement,social interaction measurement
Group 1 name Corresponds to the case (exposed) group for case-control studies
T4Social(effect of moving from single to pairwise living)

Lab analysis

Statistical Analysis

Experiment 6


incomplete

Curated date: 2024/11/28

Curator: MyleeeA

Revision editor(s): MyleeeA

Differences from previous experiment shown

Subjects

Location of subjects
Not specified
Host species Species from which microbiome was sampled. Contact us to have more species added.
Not specified
Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
Not specified
Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
Not specified
Group 0 name Corresponds to the control (unexposed) group for case-control studies
Not specified
Group 1 name Corresponds to the case (exposed) group for case-control studies
Not specified
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Not specified
Sequencing type
Not specified
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
Not specified
Data transformation Data transformation applied to microbial abundance measurements prior to differential abundance testing (if any).
Not specified
Statistical test
Not specified
Significance threshold p-value or FDR threshold used for differential abundance testing (if any)
Not specified
MHT correction Have statistical tests be corrected for multiple hypothesis testing (MHT)?
Not specified