Amanda D Melin1,2,3, James P Higham4,5, Mareike C Janiak6,7,8,9, Michael J Montague10, Catalina I Villamil11, Michala K Stock12, Amber E Trujillo4,5, Allegra N DePasquale1, Joseph D Orkin13, Samuel E Bauman Surratt14, Olga Gonzalez15, Michael L Platt10, Melween I Martínez14, Susan C Antón4,5, Maria Gloria Dominguez-Bello16,17. 1. Department of Anthropology and Archaeology, University of Calgary, Alberta, Canada. 2. Alberta Children's Hospital Research Institute, Alberta, Canada. 3. Department of Medical Genetics, University of Calgary, Alberta, Canada. 4. Department of Anthropology, New York University, New York, USA. 5. New York Consortium in Evolutionary Primatology, New York, NY, USA. 6. Department of Anthropology and Archaeology, University of Calgary, Alberta, Canada. M.C.Janiak@salford.ac.uk. 7. Alberta Children's Hospital Research Institute, Alberta, Canada. M.C.Janiak@salford.ac.uk. 8. Department of Anthropology, New York University, New York, USA. M.C.Janiak@salford.ac.uk. 9. School of Science, Engineering and Environment, University of Salford, Salford, UK. M.C.Janiak@salford.ac.uk. 10. Department of Neuroscience, University of Pennsylvania, Philadelphia, PA, USA. 11. School of Chiropractic, Universidad Central del Caribe, Bayamón, Puerto Rico. 12. Department of Sociology and Anthropology, Metropolitan State University of Denver, Denver, CO, USA. 13. Institut de Biologia Evolutiva, Universitat Pompeu Fabra-CSIC, Barcelona, Spain. 14. Caribbean Primate Research Center, University of Puerto Rico, San Juan, Puerto Rico. 15. Disease Intervention and Prevention, Southwest National Primate Research Center, San Antonio, TX, USA. 16. Department of Biochemistry and Microbiology, Rutgers University, New Brunswick, NJ, USA. 17. Department of Anthropology, Rutgers University, New Brunswick, NJ, USA.
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. Video 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. Video abstract.
Entities:
Keywords:
Aging; Genital microbiome; Gut microbiome; Non-human primates; Oral microbiome; Sex differences
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