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

Janiak, MC; Montague, MJ; Villamil, CI; Stock, MK; Trujillo, AE; DePasquale, AN; Orkin, JD; Bauman Surratt, SE; Gonzalez, O; Platt, ML; Martínez, MI; Antón, SC; Dominguez-Bello, MG; Melin, AD; Higham, JP

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. 4_dARqKdohA9mAZyu7q9YNVideo abstract

Citation

Janiak, M., Montague, M., Villamil, C., Stock, M., Trujillo, A., DePasquale, A., …Higham, J. (2021). Age and sex-associated variation in the multi-site microbiome of an entire social group of free-ranging rhesus macaques. Microbiome, 9(1), 68. https://doi.org/10.1186/s40168-021-01009-w

• Journal Article Type: Article
• Acceptance Date: Feb 2, 2021
• Publication Date: Mar 22, 2021
• Deposit Date: Mar 24, 2021
• Publicly Available Date: Mar 24, 2021
• Journal: Microbiome
• Publisher: Springer Verlag
• Volume: 9
• Issue: 1
• Pages: 68
• DOI: https://doi.org/10.1186/s40168-021-01009-w
• Publisher URL: https://doi.org/10.1186/s40168-021-01009-w
• Related Public URLs: http://www.microbiomejournal.com/
• Additional Information: Additional Information : ** From Springer Nature via Jisc Publications Router ** Licence for this article: http://creativecommons.org/licenses/by/4.0/ **Journal IDs: eissn 2049-2618 **Article IDs: publisher-id: s40168-021-01009-w; manuscript: 1009 **History: collection 12-2021; published 22-03-2021; online 22-03-2021; registration 02-02-2021; accepted 02-02-2021; submitted 03-09-2020; Funders : American Association of Physical Anthropologists;Alberta Children’s Hospital Research Institute;Natural Sciences and Engineering Research Council;Natural Environment Research Council (NERC);Leakey Foundation;Caribbean Primate Research Center (CPRC);National Institutes of Health;Animal and Biological Material Resource Center Grant/Office of Research Infrastructure Programs (ORIP);Research Facilities Construction Grant;Ford Foundation;Canadian Institute for Advanced Research (CIFAR);National Institute of Mental Health; Projects : R01MH96875;R01MH118203;unspecified;P40OD012217;C06OD026690; Grant Number: Cobb Professional Development Grant; Grant Number: NE/T000341/1; Grant Number: P40OD012217; Grant Number: C06OD026690; Grant Number: R01MH118203; Grant Number: R01MH96875