Yearly variation coupled with social interactions shape the skin microbiome in free-ranging rhesus macaques

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Needs review
Citation
PMID PubMed identifier for scientific articles.
DOI Digital object identifier for electronic documents.
Authors
Roche CE, Montague MJ, Wang J, Dickey AN, Ruiz-Lambides A, Brent LJN, Platt ML, Horvath JE
Journal
Microbiology spectrum
Year
2023
Keywords:
16S rRNA, Cayo Santiago, microbial diversity, primates, rhesus macaques, skin microbiome, social behavior, year-to-year environment
While skin microbes are known to mediate human health and disease, there has been minimal research on the interactions between skin microbiota, social behavior, and year-to-year effects in non-human primates-important animal models for translational biomedical research. To examine these relationships, we analyzed skin microbes from 78 rhesus macaques living on Cayo Santiago Island, Puerto Rico. We considered age, sex, and social group membership, and characterized social behavior by assessing dominance rank and patterns of grooming as compared to nonsocial behaviors. To measure the effects of a shifting environment, we sampled skin microbiota (based on sequence analysis of the 16S rRNA V4 region) and assessed weather across sampling periods between 2013 and 2015. We hypothesized that, first, monkeys with similar social behavior and/or in the same social group would possess similar skin microbial composition due, in part, to physical contact, and, second, microbial diversity would differ across sampling periods. We found significant phylum-level differences between social groups in the core microbiome as well as an association between total grooming rates and alpha diversity in the complete microbiome, but no association between microbial diversity and measures of rank or other nonsocial behaviors. We also identified alpha and beta diversity differences in microbiota and differential taxa abundance across two sampling periods. Our findings indicate that social dynamics interact with yearly environmental changes to shape the skin microbiota in rhesus macaques, with potential implications for understanding the factors affecting the microbiome in humans, which share many biological and social characteristics with these animals. IMPORTANCE Primate studies are valuable for translational and evolutionary insights into the human microbiome. The majority of primate microbiome studies focus on the gut, so less is known about the factors impacting the microbes on skin and how their links affect health and behavior. Here, we probe the impact of social interactions and the yearly environmental changes on food-provisioned, free-ranging monkeys living on a small island. We expected animals that lived together and groomed each other would have more similar microbes on their skin, but surprisingly found that the external environment was a stronger influence on skin microbiome composition. These findings have implications for our understanding of the human skin microbiome, including potential manipulations to improve health and treat disease.

Experiment 1


Needs review

Curated date: 2024/04/01

Curator: Mercyajayi21

Revision editor(s): Mercyajayi21, Fiddyhamma

Subjects

Location of subjects
United States of America
Host species Species from which microbiome was sampled. Contact us to have more species added.
Macaca mulatta
Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
Axilla skin Axillary skin,Skin of axilla,Axilla skin,axilla skin
Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
Microbiome measurement Microbiome measurement,microbiome measurement
Group 0 name Corresponds to the control (unexposed) group for case-control studies
2013 sampling period
Group 1 name Corresponds to the case (exposed) group for case-control studies
2015 sampling period
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
The 2015 sampling period occurred from October 2015 through December 2015
Group 0 sample size Number of subjects in the control (unexposed) group
42
Group 1 sample size Number of subjects in the case (exposed) group
33

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
Mann-Whitney (Wilcoxon)
Welch's T-Test
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: "sampling period" 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.sampling period

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
increased
Faith Phylogenetic diversity, takes into account phylogenetic distance of all taxa identified in a sample
increased

Signature 1

Needs review

Curated date: 2024/04/02

Curator: Fiddyhamma

Revision editor(s): Fiddyhamma

Source: Fig 6, Text

Description: The volcano plot (center) depicts the differences between the 2013 and 2015 sampling periods for each detected ASV (red and black points). Taxa depicted in red are the most highly significant (P < 0.015). Overabundant ASVs from 2013 are located on the negative (left) side of the volcano plot, while overabundant ASVs from 2015 are located on the positive (right) side. The violin plots surrounding the volcano plot depict the CLR values of the most significant taxa from the volcano plot; left: overabundant taxa in 2013; right: overabundant taxa in 2015

Abundance in Group 1: increased abundance in 2015 sampling period

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Rhodococcus sp. (in: high G+C Gram-positive bacteria)
Acinetobacter sp.
Sarcina ventriculi
Altererythrobacter sp.
Stenotrophomonas koreensis
Ruminococcaceae UCG-002 spRuminococcaceae UCG-002 sp

Revision editor(s): Fiddyhamma

Signature 2

Needs review

Curated date: 2024/04/02

Curator: Fiddyhamma

Revision editor(s): Fiddyhamma

Source: Fig 6, Text

Description: The volcano plot (center) depicts the differences between the 2013 and 2015 sampling periods for each detected ASV (red and black points). Taxa depicted in red are the most highly significant (P < 0.015). Overabundant ASVs from 2013 are located on the negative (left) side of the volcano plot, while overabundant ASVs from 2015 are located on the positive (right) side. The violin plots surrounding the volcano plot depict the CLR values of the most significant taxa from the volcano plot; left: overabundant taxa in 2013; right: overabundant taxa in 2015

Abundance in Group 1: decreased abundance in 2015 sampling period

NCBI Quality ControlLinks
Cecembia
Nocardioides aestuarii
Paracoccus sp. (in: a-proteobacteria)
Rickettsiella sp.
Thauera aromatica

Revision editor(s): Fiddyhamma

Experiment 2


Needs review

Curated date: 2024/04/03

Curator: Fiddyhamma

Revision editor(s): Fiddyhamma, Victoria

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
Non-Core microbiome social group (R)
Group 1 name Corresponds to the case (exposed) group for case-control studies
Non-Core microbiome social group (F)
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
The core features 1.0 list (e.g., features present in 100% of samples) was used to filter the complete microbiome table and output a “core” microbiome feature table, via q2-filter-features. The same core features were then removed from the complete microbiome table to output a “non-core” microbiome feature table. Core and non-core feature tables were then exported to biom format
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

Statistical test
Mann-Whitney (Wilcoxon)

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
increased

Experiment 3


Needs review

Curated date: 2024/04/03

Curator: Fiddyhamma

Revision editor(s): Fiddyhamma, Victoria

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
Core microbiome social groups (V)
Group 1 name Corresponds to the case (exposed) group for case-control studies
Core microbiome social groups (F)
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
The core features 1.0 list (e.g., features present in 100% of samples) was used to filter the complete microbiome table and output a “core” microbiome feature table, via q2-filter-features.

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
increased

Experiment 4


Needs review

Curated date: 2024/04/04

Curator: Fiddyhamma

Revision editor(s): Fiddyhamma, Victoria

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
Non-Core microbiome 2013 sampling period
Group 1 name Corresponds to the case (exposed) group for case-control studies
Non-Core microbiome 2015 sampling period
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
The core features 1.0 list (e.g., features present in 100% of samples) was used to filter the complete microbiome table and output a “core” microbiome feature table, via q2-filter-features. The same core features were then removed from the complete microbiome table to output a “non-core” microbiome feature table. Core and non-core feature tables were then exported to biom format

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
increased

Experiment 5


Needs review

Curated date: 2024/04/04

Curator: Fiddyhamma

Revision editor(s): Fiddyhamma

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
Core microbiome 2013 sampling period
Group 1 name Corresponds to the case (exposed) group for case-control studies
Core microbiome 2015 sampling period
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
The core features 1.0 list (e.g., features present in 100% of samples) was used to filter the complete microbiome table and output a “core” microbiome feature table, via q2-filter-features.

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
increased

Experiment 6


Needs review

Curated date: 2024/04/04

Curator: Fiddyhamma

Revision editor(s): Fiddyhamma

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
Complete microbiome social group R
Group 1 name Corresponds to the case (exposed) group for case-control studies
Complete microbiome social group F
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Colony members self-organize into social groups, demonstrate various forms of social behaviors, most notably grooming
Group 0 sample size Number of subjects in the control (unexposed) group
11
Group 1 sample size Number of subjects in the case (exposed) group
43

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Faith Phylogenetic diversity, takes into account phylogenetic distance of all taxa identified in a sample
unchanged

Signature 1

Needs review

Curated date: 2024/04/04

Curator: Fiddyhamma

Revision editor(s): Fiddyhamma

Source: Fig 2B, text

Description: Box plots representing the taxonomic differences for specific phyla among social groups, with significance assessed using a KW test on CLR transformed relative abundance values: Actinobacteria (KW P = 0.00013), Cyanobacteria (KW P = 0.12), Firmicutes (KW P = 0.044), and Proteobacteria (KW P = 0.0096). Pairwise comparisons between groups were assessed using t-tests; the symbolic number coding of P-values is as follows: *, P ≤ 0.05; **, P ≤ 0.01; ***, P ≤ 0.001; ****, P ≤ 0.0001.

Abundance in Group 1: increased abundance in Complete microbiome social group F

NCBI Quality ControlLinks
Cyanobacteriota

Revision editor(s): Fiddyhamma

Signature 2

Needs review

Curated date: 2024/04/04

Curator: Fiddyhamma

Revision editor(s): Fiddyhamma

Source: Fig 2B, text

Description: Box plots representing the taxonomic differences for specific phyla among social groups, with significance assessed using a KW test on CLR transformed relative abundance values: Actinobacteria (KW P = 0.00013), Cyanobacteria (KW P = 0.12), Firmicutes (KW P = 0.044), and Proteobacteria (KW P = 0.0096). Pairwise comparisons between groups were assessed using t-tests; the symbolic number coding of P-values is as follows: *, P ≤ 0.05; **, P ≤ 0.01; ***, P ≤ 0.001; ****, P ≤ 0.0001.

Abundance in Group 1: decreased abundance in Complete microbiome social group F

NCBI Quality ControlLinks
Actinomycetota
Bacillota
Pseudomonadota

Revision editor(s): Fiddyhamma

Experiment 7


Needs review

Curated date: 2024/04/04

Curator: Fiddyhamma

Revision editor(s): Fiddyhamma

Differences from previous experiment shown

Subjects

Group 1 name Corresponds to the case (exposed) group for case-control studies
Complete microbiome social group V
Group 1 sample size Number of subjects in the case (exposed) group
12

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Faith Phylogenetic diversity, takes into account phylogenetic distance of all taxa identified in a sample
unchanged

Signature 1

Needs review

Curated date: 2024/04/04

Curator: Fiddyhamma

Revision editor(s): Fiddyhamma

Source: Fig 2B, text

Description: Box plots representing the taxonomic differences for specific phyla among social groups, with significance assessed using a KW test on CLR transformed relative abundance values: Actinobacteria (KW P = 0.00013), Cyanobacteria (KW P = 0.12), Firmicutes (KW P = 0.044), and Proteobacteria (KW P = 0.0096). Pairwise comparisons between groups were assessed using t-tests; the symbolic number coding of P-values is as follows: *, P ≤ 0.05; **, P ≤ 0.01; ***, P ≤ 0.001; ****, P ≤ 0.0001.

Abundance in Group 1: decreased abundance in Complete microbiome social group V

NCBI Quality ControlLinks
Actinomycetota

Revision editor(s): Fiddyhamma

Experiment 8


Needs review

Curated date: 2024/04/04

Curator: Fiddyhamma

Revision editor(s): Fiddyhamma

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
Complete microbiome social group F
Group 1 name Corresponds to the case (exposed) group for case-control studies
Complete microbiome social group KK
Group 0 sample size Number of subjects in the control (unexposed) group
43
Group 1 sample size Number of subjects in the case (exposed) group
8

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Faith Phylogenetic diversity, takes into account phylogenetic distance of all taxa identified in a sample
unchanged

Signature 1

Needs review

Curated date: 2024/04/04

Curator: Fiddyhamma

Revision editor(s): Fiddyhamma

Source: Fig 2B, text

Description: Box plots representing the taxonomic differences for specific phyla among social groups, with significance assessed using a KW test on CLR transformed relative abundance values: Actinobacteria (KW P = 0.00013), Cyanobacteria (KW P = 0.12), Firmicutes (KW P = 0.044), and Proteobacteria (KW P = 0.0096). Pairwise comparisons between groups were assessed using t-tests; the symbolic number coding of P-values is as follows: *, P ≤ 0.05; **, P ≤ 0.01; ***, P ≤ 0.001; ****, P ≤ 0.0001.

Abundance in Group 1: increased abundance in Complete microbiome social group KK

NCBI Quality ControlLinks
Actinomycetota
Pseudomonadota

Revision editor(s): Fiddyhamma

Experiment 9


Needs review

Curated date: 2024/04/04

Curator: Fiddyhamma

Revision editor(s): Fiddyhamma

Differences from previous experiment shown

Subjects

Group 1 name Corresponds to the case (exposed) group for case-control studies
Complete microbiome social group V
Group 1 sample size Number of subjects in the case (exposed) group
12

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Faith Phylogenetic diversity, takes into account phylogenetic distance of all taxa identified in a sample
unchanged

Signature 1

Needs review

Curated date: 2024/04/04

Curator: Fiddyhamma

Revision editor(s): Fiddyhamma

Source: Fig 2B, text

Description: Box plots representing the taxonomic differences for specific phyla among social groups, with significance assessed using a KW test on CLR transformed relative abundance values: Actinobacteria (KW P = 0.00013), Cyanobacteria (KW P = 0.12), Firmicutes (KW P = 0.044), and Proteobacteria (KW P = 0.0096). Pairwise comparisons between groups were assessed using t-tests; the symbolic number coding of P-values is as follows: *, P ≤ 0.05; **, P ≤ 0.01; ***, P ≤ 0.001; ****, P ≤ 0.0001.

Abundance in Group 1: increased abundance in Complete microbiome social group V

NCBI Quality ControlLinks
Bacillota

Revision editor(s): Fiddyhamma

Experiment 10


Needs review

Curated date: 2024/04/04

Curator: Fiddyhamma

Revision editor(s): Fiddyhamma

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
Complete microbiome social group HH
Group 1 name Corresponds to the case (exposed) group for case-control studies
Complete microbiome social group KK
Group 0 sample size Number of subjects in the control (unexposed) group
4
Group 1 sample size Number of subjects in the case (exposed) group
8

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Faith Phylogenetic diversity, takes into account phylogenetic distance of all taxa identified in a sample
unchanged

Signature 1

Needs review

Curated date: 2024/04/04

Curator: Fiddyhamma

Revision editor(s): Fiddyhamma

Source: Fig 2B, text

Description: Box plots representing the taxonomic differences for specific phyla among social groups, with significance assessed using a KW test on CLR transformed relative abundance values: Actinobacteria (KW P = 0.00013), Cyanobacteria (KW P = 0.12), Firmicutes (KW P = 0.044), and Proteobacteria (KW P = 0.0096). Pairwise comparisons between groups were assessed using t-tests; the symbolic number coding of P-values is as follows: *, P ≤ 0.05; **, P ≤ 0.01; ***, P ≤ 0.001; ****, P ≤ 0.0001.

Abundance in Group 1: increased abundance in Complete microbiome social group KK

NCBI Quality ControlLinks
Pseudomonadota

Revision editor(s): Fiddyhamma

Experiment 11


Needs review

Curated date: 2024/04/04

Curator: Fiddyhamma

Revision editor(s): Fiddyhamma

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
Complete microbiome social group V
Group 0 sample size Number of subjects in the control (unexposed) group
12

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Faith Phylogenetic diversity, takes into account phylogenetic distance of all taxa identified in a sample
unchanged

Signature 1

Needs review

Curated date: 2024/04/04

Curator: Fiddyhamma

Revision editor(s): Fiddyhamma

Source: Fig 2B, text

Description: Box plots representing the taxonomic differences for specific phyla among social groups, with significance assessed using a KW test on CLR transformed relative abundance values: Actinobacteria (KW P = 0.00013), Cyanobacteria (KW P = 0.12), Firmicutes (KW P = 0.044), and Proteobacteria (KW P = 0.0096). Pairwise comparisons between groups were assessed using t-tests; the symbolic number coding of P-values is as follows: *, P ≤ 0.05; **, P ≤ 0.01; ***, P ≤ 0.001; ****, P ≤ 0.0001.

Abundance in Group 1: increased abundance in Complete microbiome social group KK

NCBI Quality ControlLinks
Actinomycetota

Revision editor(s): Fiddyhamma

Experiment 12


Needs review

Curated date: 2024/04/06

Curator: Fiddyhamma

Revision editor(s): Fiddyhamma

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
2013 sampling period (Complete microbiome)
Group 1 name Corresponds to the case (exposed) group for case-control studies
2015 sampling period (Complete microbiome)
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
The 2015 sampling period occurred from October 2015 through December 2015
Group 0 sample size Number of subjects in the control (unexposed) group
42
Group 1 sample size Number of subjects in the case (exposed) group
33

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
increased
Faith Phylogenetic diversity, takes into account phylogenetic distance of all taxa identified in a sample
increased

Signature 1

Needs review

Curated date: 2024/04/06

Curator: Fiddyhamma

Revision editor(s): Fiddyhamma

Source: Figure 4B, text

Description: Box plots representing the significant pairwise taxa using Wilcoxon tests on CLR transformed relative abundance values on phyla: Actinobacteria, Firmicutes, Deinococcus-Thermus, Fusobacteria, and Proteobacteria.

Abundance in Group 1: decreased abundance in 2015 sampling period (Complete microbiome)

NCBI Quality ControlLinks
Actinomycetota
Pseudomonadota
Bacillota
Deinococcus
Fusobacteriia

Revision editor(s): Fiddyhamma