Seasonal shifts in the gut microbiome indicate plastic responses to diet in wild geladas
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Study information
-
Quality control
- Retracted paper
- Contamination issues suspected
- Batch effect issues suspected
- Uncontrolled confounding suspected
- Results are suspect (various reasons)
- Tags applied
study design
Citation
PMID PubMed identifier for scientific articles.
DOI Digital object identifier for electronic documents.
URI
Authors
Baniel A, Amato KR, Beehner JC, Bergman TJ, Mercer A, Perlman RF, Petrullo L, Reitsema L, Sams S, Lu A, Snyder-Mackler N
Journal
Microbiome
Year
2021
Keywords:
Graminivory, Gut microbiome, Primates, Seasonality, Thermoregulation, Theropithecus gelada
BACKGROUND: Adaptive shifts in gut microbiome composition are one route by which animals adapt to seasonal changes in food availability and diet. However, outside of dietary shifts, other potential environmental drivers of gut microbial composition have rarely been investigated, particularly in organisms living in their natural environments. RESULTS: Here, we generated the largest wild nonhuman primate gut microbiome dataset to date to identify the environmental drivers of gut microbial diversity and function in 758 samples collected from wild Ethiopian geladas (Theropithecus gelada). Because geladas live in a cold, high-altitude environment and have a low-quality grass-based diet, they face extreme thermoregulatory and energetic constraints. We tested how proxies of food availability (rainfall) and thermoregulatory stress (temperature) predicted gut microbiome composition of geladas. The gelada gut microbiome composition covaried with rainfall and temperature in a pattern that suggests distinct responses to dietary and thermoregulatory challenges. Microbial changes were driven by differences in the main components of the diet across seasons: in rainier periods, the gut was dominated by cellulolytic/fermentative bacteria that specialized in digesting grass, while during dry periods the gut was dominated by bacteria that break down starches found in underground plant parts. Temperature had a comparatively smaller, but detectable, effect on the gut microbiome. During cold and dry periods, bacterial genes involved in energy, amino acid, and lipid metabolism increased, suggesting a stimulation of fermentation activity in the gut when thermoregulatory and nutritional stress co-occurred, and potentially helping geladas to maintain energy balance during challenging periods. CONCLUSION: Together, these results shed light on the extent to which gut microbiota plasticity provides dietary and metabolic flexibility to the host, and might be a key factor to thriving in changing environments. On a longer evolutionary timescale, such metabolic flexibility provided by the gut microbiome may have also allowed members of Theropithecus to adopt a specialized diet, and colonize new high-altitude grassland habitats in East Africa. Video abstract.
Experiment 1
Needs review
Subjects
- Location of subjects
- Ethiopia
- Host species Species from which microbiome was sampled. Contact us to have more species added.
- Theropithecus gelada
- 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
- Seasonality measurement Seasonality measurement,seasonality measurement
- Group 0 name Corresponds to the control (unexposed) group for case-control studies
- Dry season (< 100 mm of rain in the past month)
- Group 1 name Corresponds to the case (exposed) group for case-control studies
- Wet season (> 200 mm of rain in the past month)
- Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
- Wet season (> 200 mm of rain in the past month) refers to the period of rainfall in the previous month.
- Group 0 sample size Number of subjects in the control (unexposed) group
- 362
- Group 1 sample size Number of subjects in the case (exposed) group
- 282
Lab analysis
- Sequencing type
- 16S
- 16S variable region One or more hypervariable region(s) of the bacterial 16S gene
- 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).
- centered log-ratio
- Statistical test
- Mixed-Effects Regression
- 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
- Confounders controlled for Confounding factors that have been accounted for by stratification or model adjustment
- Confounders controlled for: "individual membership" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.individual membership, Confounders controlled for: "unit membership" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.unit membership
Alpha Diversity
- Shannon Estimator of species richness and species evenness: more weight on species richness
- increased
- Richness Number of species
- unchanged
- Faith Phylogenetic diversity, takes into account phylogenetic distance of all taxa identified in a sample
- unchanged
Signature 1
Needs review
Source: Table S6-S7, Figure 4
Description: Differentially abundant taxa between wet and dry season
Abundance in Group 1: increased abundance in Wet season (> 200 mm of rain in the past month)
Revision editor(s): KateRasheed
Signature 2
Needs review
Source: Table S6-S7, Fig. 4
Description: Differentially abundant taxa between wet and dry season
Abundance in Group 1: decreased abundance in Wet season (> 200 mm of rain in the past month)
Revision editor(s): KateRasheed
Experiment 2
Needs review
Differences from previous experiment shown
Subjects
- Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
- Mixed sex population Mixed sex population,mixed sex population
- Group 0 name Corresponds to the control (unexposed) group for case-control studies
- Male samples
- Group 1 name Corresponds to the case (exposed) group for case-control studies
- Female samples
- Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
- Female samples refers to the Ethiopian female geladas whose fecal samples were collected for analysis
- Group 0 sample size Number of subjects in the control (unexposed) group
- 138
- Group 1 sample size Number of subjects in the case (exposed) group
- 620
Lab analysis
Statistical Analysis
Alpha Diversity
- Shannon Estimator of species richness and species evenness: more weight on species richness
- increased
- Richness Number of species
- increased
- Faith Phylogenetic diversity, takes into account phylogenetic distance of all taxa identified in a sample
- increased
Signature 1
Needs review
Source: Table S7
Description: Differential abundance of taxa between male and female geladas
Abundance in Group 1: increased abundance in Female samples
Revision editor(s): KateRasheed
Signature 2
Needs review
Source: Table S7
Description: Differential abundance of taxa between male and female geladas
Abundance in Group 1: decreased abundance in Female samples
| NCBI | Quality Control | Links |
|---|---|---|
| Alphaproteobacteria bacterium canine oral taxon 081 | ||
| Pirellulales | ||
| Planctomycetia |
Revision editor(s): KateRasheed
Experiment 3
Needs review
Differences from previous experiment shown
Subjects
- Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
- Reproductive behaviour measurement Reproductive behaviour measurement,reproductive behaviour measurement
- Group 0 name Corresponds to the control (unexposed) group for case-control studies
- Cycling females
- Group 1 name Corresponds to the case (exposed) group for case-control studies
- Pregnant females
- Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
- Pregnant females refers to female at their pregnancy reproductive state. It started on the date of conception and ended the day before parturition.
- Group 0 sample size Number of subjects in the control (unexposed) group
- 158
- Group 1 sample size Number of subjects in the case (exposed) group
- 61
Lab analysis
Statistical Analysis
Alpha Diversity
- Shannon Estimator of species richness and species evenness: more weight on species richness
- unchanged
- Richness Number of species
- unchanged
- Faith Phylogenetic diversity, takes into account phylogenetic distance of all taxa identified in a sample
- unchanged
Signature 1
Needs review
Source: Table S13
Description: Differential abundance of taxa between pregnant and cycling female geladas
Abundance in Group 1: increased abundance in Pregnant females
| NCBI | Quality Control | Links |
|---|---|---|
| Campylobacterales | ||
| Campylobacterota | ||
| Epsilonproteobacteria | ||
| Helicobacter | ||
| Helicobacteraceae | ||
| Thomasclavelia | ||
| Verrucomicrobiia | ||
| Verrucomicrobiota | ||
| [Ruminococcus] torques |
Revision editor(s): KateRasheed
Experiment 4
Needs review
Differences from previous experiment shown
Subjects
- Group 0 name Corresponds to the control (unexposed) group for case-control studies
- Lactating females
- Group 0 sample size Number of subjects in the control (unexposed) group
- 346
Lab analysis
Statistical Analysis
Alpha Diversity
- Shannon Estimator of species richness and species evenness: more weight on species richness
- increased
- Richness Number of species
- increased
- Faith Phylogenetic diversity, takes into account phylogenetic distance of all taxa identified in a sample
- increased
Signature 1
Needs review
Source: Table S13
Description: Differential abundance of taxa between pregnant and cycling female geladas
Abundance in Group 1: increased abundance in Pregnant females
| NCBI | Quality Control | Links |
|---|---|---|
| Verrucomicrobiota | ||
| Verrucomicrobiia | ||
| [Ruminococcus] torques | ||
| Epsilonproteobacteria | ||
| Campylobacterota | ||
| Thomasclavelia | ||
| Campylobacterales |
Revision editor(s): KateRasheed
Experiment 5
Needs review
Differences from previous experiment shown
Subjects
- Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
- Temperature Temperature,temperature
- Group 0 name Corresponds to the control (unexposed) group for case-control studies
- Average minimum temperature(Average Min Temp)
- Group 1 name Corresponds to the case (exposed) group for case-control studies
- Average maximum temperature(Average Max Temp)
- Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
- Average maximum temperature(Average Max Temp) refers to colder temperature (i.e. <8oC in the past month) in Ethiopia
- Group 0 sample size Number of subjects in the control (unexposed) group
- 567
- Group 1 sample size Number of subjects in the case (exposed) group
- 191
Lab analysis
Statistical Analysis
Alpha Diversity
- Shannon Estimator of species richness and species evenness: more weight on species richness
- unchanged
- Richness Number of species
- unchanged
- Faith Phylogenetic diversity, takes into account phylogenetic distance of all taxa identified in a sample
- unchanged
Signature 1
Needs review
Source: Table S7
Description: Differential abundance of taxa between average minimum temperature and average maximum temperature
Abundance in Group 1: increased abundance in Average maximum temperature(Average Max Temp)
| NCBI | Quality Control | Links |
|---|---|---|
| Lactobacillus | ||
| Streptococcus | ||
| Lactobacillales | ||
| Hydrogenoanaerobacterium | ||
| Coprococcus | ||
| Marvinbryantia | ||
| Clostridium | ||
| Cyanobacteriota |
Revision editor(s): KateRasheed
Signature 2
Needs review
Source: Table S7
Description: Differential abundance of taxa between average minimum temperature and average maximum temperature
Abundance in Group 1: decreased abundance in Average maximum temperature(Average Max Temp)
Revision editor(s): KateRasheed
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