Age and sex-associated variation in the multi-site microbiome of an entire social group of free-ranging rhesus macaques

Abstract

Background 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. 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. Results Infant 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. Conclusions Across 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.

Maternal effects on early-life gut microbiome maturation in a wild nonhuman primate

“…The broad dynamic of microbial colonization in geladas presents many similarities with previous reports on humans [2,5,8] and other mammals ( [10,37,73], but see [74]). We observed a low initial number of microbes and a rapid increase in microbial diversity in the first seven months of life, followed by more gradual changes in microbial composition until weaning (~17 months).…”

“…Although studies on host-associated microbial communities in wild primates are emerging, many remain limited in scope, hampered by cross-sectional samples and small sample sizes of unweaned infants (particularly in the first few weeks of life), which together prevent longitudinal characterization of gut microbial colonization processes [72][73][74][75]. Here, we used dense crosssectional and longitudinal monitoring to characterize gut microbial colonization during the first three years of life and assess the role of maternal effects in shaping offspring maturation trajectories in wild gelada monkeys (Theropithecus gelada).…”

Ecology impacts the decrease of Spirochaetes and Prevotella in the fecal gut microbiota of urban humans

“…We could not observe any bacterial clades that were location-specific and prevalent, most probably due to the central role of host phylogeny for bacterial prevalence patterns as well as the well-defined and shared diet and dietary information throughout German zoos, which may have a homogenizing effect. As most samples from zoos were collected collectively from zoo compounds, it was not feasible to include information on sex or reproductive status of the animals, which limits the interpretation of our study results regarding this known confounder in microbiome studies [ 40 ].…”

Neonatal Immune System Ontogeny: The Role of Maternal Microbiota and Associated Factors. How Might the Non-Human Primate Model Enlighten the Path?

“…Such questions may include the impact of antibiotic use in neonate colonization and immune system maturation and their link to infectious or non-infectious diseases in early life and later life [125]. The NHP model allows the monitoring of the microbiota's early colonization in neonate, concomitantly with the bacterial metabolites produced and their respective role in shaping the immune system [126]. Indeed, as illustrated in Figure 4 below, the NHP model harbors several advantages for biomedical research.…”