TY - JOUR
T1 - Age and sex-associated variation in the multi-site microbiome of an entire social group of free-ranging rhesus macaques
AU - Janiak, Mareike C.
AU - Montague, Michael J.
AU - Villamil, Catalina I.
AU - Stock, Michala K.
AU - Trujillo, Amber E.
AU - DePasquale, Allegra N.
AU - Orkin, Joseph D.
AU - Bauman Surratt, Samuel E.
AU - Gonzalez, Olga
AU - Platt, Michael L.
AU - Martínez, Melween I.
AU - Antón, Susan C.
AU - Dominguez-Bello, Maria Gloria
AU - Melin, Amanda D.
AU - Higham, James P.
N1 - Funding Information:
This work was supported by an AAPA Cobb Professional Development Award and a postdoctoral fellowship from the Alberta Children’s Hospital Research Institute to MCJ. MCJ was funded by a grant from the Natural Sciences and Engineering Research Council (NSERC) to ADM and by the Natural Environment Research Council (NERC, NE/T000341/1). Microbiome sampling was supported by NYU and a Leakey Foundation grant to JPH and SCA. Computational resources were provided by WestGrid and Compute Canada. The Caribbean Primate Research Center (CPRC) is supported by the National Institutes of Health. An Animal and Biological Material Resource Center Grant (P40OD012217) was awarded to UPR from the Office of Research Infrastructure Programs (ORIP), and a Research Facilities Construction Grant (C06OD026690) was awarded for the renovation of CPRC facilities after Hurricane Maria. MJM and MLP are supported by NIH NIMH R01MH96875 and R01MH118203. AET was supported by a Ford Foundation Fellowship. This work was partially supported by the Canadian Institute for Advanced Research (CIFAR), to MGDB.
Publisher Copyright:
© 2021, The Author(s).
PY - 2021/12
Y1 - 2021/12
N2 - 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. [MediaObject not available: see fulltext.]
AB - 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. [MediaObject not available: see fulltext.]
KW - Aging
KW - Genital microbiome
KW - Gut microbiome
KW - Non-human primates
KW - Oral microbiome
KW - Sex differences
KW - Puerto Rico
KW - RNA, Ribosomal, 16S/genetics
KW - Macaca mulatta
KW - Microbiota/genetics
KW - Animals
KW - Female
KW - Gastrointestinal Microbiome/genetics
KW - Mice
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UR - http://www.scopus.com/inward/citedby.url?scp=85103095366&partnerID=8YFLogxK
U2 - 10.1186/s40168-021-01009-w
DO - 10.1186/s40168-021-01009-w
M3 - Article
C2 - 33752735
AN - SCOPUS:85103095366
SN - 2049-2618
VL - 9
JO - Microbiome
JF - Microbiome
IS - 1
M1 - 68
ER -