Abstract
BackgroundAn individual’s microbiome changes over the course of its lifetime, especially during infancy, and again in old age. Confounding factors such as diet and healthcare make it difficult to disentangle the interactions between age, health, and microbial changes in humans. Animal models present an excellent opportunity to study age- and sex-linked variation in the microbiome, but captivity is known to influence animal microbial abundance and composition, while studies of free-ranging animals are typically limited to studies of the fecal microbiome using samples collected non-invasively. Here, we analyze a large dataset of oral, rectal, and genital swabs collected from 105 free-ranging rhesus macaques (Macaca mulatta, aged 1 month-26 years), comprising one entire social group, from the island of Cayo Santiago, Puerto Rico. We sequenced 16S V4 rRNA amplicons for all samples.ResultsInfant gut microbial communities had significantly higher relative abundances of Bifidobacterium and Bacteroides and lower abundances of Ruminococcus, Fibrobacter, and Treponema compared to older age groups, consistent with a diet high in milk rather than solid foods. The genital microbiome varied widely between males and females in beta-diversity, taxonomic composition, and predicted functional profiles. Interestingly, only penile, but not vaginal, microbiomes exhibited distinct age-related changes in microbial beta-diversity, taxonomic composition, and predicted functions. Oral microbiome composition was associated with age, and was most distinctive between infants and other age classes.ConclusionsAcross all three body regions, with notable exceptions in the penile microbiome, while infants were distinctly different from other age groups, microbiomes of adults were relatively invariant, even in advanced age. While vaginal microbiomes were exceptionally stable, penile microbiomes were quite variable, especially at the onset of reproductive age. Relative invariance among adults, including elderly individuals, is contrary to findings in humans and mice. We discuss potential explanations for this observation, including that age-related microbiome variation seen in humans may be related to changes in diet and lifestyle.4_dARqKdohA9mAZyu7q9YNVideo abstract
Highlights
A major goal of the biomedical sciences is to understand how life transitions and aging impact human biological processes, health, and wellness
For body sites showing evidence of age or sex differences, we further identified KEGG pathways that explain the observed differences between predicted functional profiles with the linear discriminant analysis effect size (LEfSe) method [119], using an LDA effect size cut-off of ≥ 2 and an alpha of 0.01 for both the initial Kruskal-Wallis sum-rank test and the subsequent Wilcoxon rank-sum test
Pairwise comparisons of beta diversity by age group revealed that these differences are driven by the infant (
Summary
A major goal of the biomedical sciences is to understand how life transitions and aging impact human biological processes, health, and wellness. Large cohort studies of multi-site microbiome data with deep associated metadata and appropriate controls are valuable, especially from whole study populations of all ages and both sexes. Such datasets are hard to come by for humans, and are complicated by multiple factors, including our long lifespans, heterogeneity in consent and other sample access issues, and because of socioeconomic confounds. An individual’s microbiome changes over the course of its lifetime, especially during infancy, and again in old age Confounding factors such as diet and healthcare make it difficult to disentangle the interactions between age, health, and microbial changes in humans.
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