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Associations of the skin, oral and gut microbiome with aging, frailty and infection risk reservoirs in older adults

Nature Aging volume 2, pages 941–955 (2022)Cite this article

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Abstract

Older adults represent a vulnerable population with elevated risk for numerous morbidities. To explore the association of the microbiome with aging and age-related susceptibilities, including frailty and infectious disease risk, we conducted a longitudinal study of the skin, oral, and gut microbiota in 47 community- or skilled nursing facility-dwelling older adults versus younger adults. We found that microbiome changes were not associated with chronological age so much as frailty; we identified prominent changes in microbiome features associated with susceptibility to pathogen colonization and disease risk, including diversity, stability, heterogeneity and biogeographic determinism, which were moreover associated with a loss of Cutibacterium acnes in the skin microbiome. Strikingly, the skin microbiota were also the primary reservoir for antimicrobial resistance, clinically important pathobionts and nosocomial strains, suggesting a potential role particularly for the skin microbiome in disease risk and dissemination of multidrug resistant pathogens.

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Fig. 1: Study design.
Fig. 2: Instability, hyperdiversification, heterogeneity and biogeographic divergence in the aging microbiome.
Fig. 3: Compositional differences in the microbiota of older adults.
Fig. 4: Associations among age, frailty and the skin microbiome.
Fig. 5: Strain-level diversity, heterogeneity, and differential abundance of clades.
Fig. 6: The skin is a major reservoir of pathobionts and plasmid-borne antimicrobial resistance in older adults.

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Data availability

Metagenomic sequence files from participants who consented to making their deidentified metagenomic data available in public access data can be accessed in National Center for Biotechnology Information BioProject PRJNA699281. HMP data can be accessed from https://www.hmpdacc.org/hmp/; SRS IDs of the samples used in this study are detailed in Supplementary Table 2. Oh et al.29,30 data can be accessed via National Center for Biotechnology Information BioProject PRJNA46333.

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Acknowledgements

Funding for this project were provided by internal UConn support via the UConn Research Excellence Program and the UConn Microbiome Research Seed Grant. Investigator salaries were additionally supported by the National Institute on Aging (R56 AG060746 and P30 AG067988) and Claude D. Pepper Older Americans Independence Center at UConn. JO is additionally supported by the National Institutes of Health (DP2 GM126893-01, K22 AI119231-01, 1U54NS105539, 1 U19 AI142733 and 1 R21 AR075174), the National Science Foundation (1853071), the American Cancer Society, the Leo Foundation and the Mackenzie Foundation.

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Author notes

  1. These authors contributed equally: Peter J. Larson, Wei Zhou, George A. Kuchel, Julie T. Robison, and Julia Oh.

Authors and Affiliations

  1. UCONN Health (University of Connecticut), Farmington, CT, US

    Peter J. Larson, Alba Santiago, Sarah Driscoll, James J. Grady, George A. Kuchel & Julie T. Robison

  2. The Jackson Laboratory, Farmington, CT, US

    Peter J. Larson, Wei Zhou, Elizabeth Fleming, Anita Y. Voigt & Julia Oh

  3. The University of Connecticut, Storrs, CT, US

    Ock K. Chun

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Contributions

Conceptualization: P.J.L., G.A.K., J.T.R. and J.O. Methodology: J.O., J.T.R. and G.A.K. Software: P.J.L., W.Z. and J.O. Validation: P.J.L., W.Z. and J.O. Formal analysis: P.J.L. and W.Z. Investigation: P.J.L., A.S., S.D., A.Y.V., E.F. and W.Z. Resources: G.A.K., J.T.R., J.O. Data Curation: J.T.R., A.S., S.D., W.Z. and J.O. Writing – Original Draft: P.J.L. and W.Z. Writing – Review & Editing: J.O., GK, J.T.R., A.S., S.D., A.Y.V. and W.Z. Visualization: P.J.L. and W.Z. Supervision: G.A.K., J.T.R. and J.O. Project Administration: J.T.R. and J.O. Funding acquisition: G.A.K., J.T.R., JG, O.K.C. and J.O.

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Correspondence to Julia Oh.

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Larson, P.J., Zhou, W., Santiago, A. et al. Associations of the skin, oral and gut microbiome with aging, frailty and infection risk reservoirs in older adults. Nat Aging 2, 941–955 (2022). https://doi.org/10.1038/s43587-022-00287-9

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