Instability, Heterogeneity, and Pathogenicity Reservoirs in the Skin, Oral, and Gut Microbiota of Older Adults

Background: The microbiota – communities of bacteria, viruses, fungi, archaea, and protozoa that inhabit nearly every surface of the human body – are an emerging risk factor for aging-related diseases. Microbiota influence local and systemic health through metabolic and immunomodulatory processes, and can harbor, or protect against, pathogens. Despite this, older adults have often been excluded from systematic metagenome studies. We investigated the skin, oral, and gut microbiota of older adults living in both community and skilled nursing facility (SNF) settings, focusing on potential relationships with frailty and place of residence.

Methods: We conducted a longitudinal microbiome survey of 47 subjects age 65+ years of age; 22 SNF dwelling (SNFD) and 25 community dwelling (CD). We performed metagenomic whole genome shotgun sequencing on stool, oral, and skin samples from 8 sites, 1360 total. To correlate clinical and behavioral variables, we measured frailty, collected medical records, and interviewed subjects on diet and lifestyle. We also drew comparisons with our and others’ previous younger cohorts.

Results: We observed prominent differences between the microbiomes of younger and older adults, particularly for SNFDs, at all body sites. Subject frailty was negatively correlated with the relative abundance of Cutibacterium acnes in skin communities, which itself was highly correlated with microbial community stability, diversity, heterogeneity, and biogeography, factors that may modulate pathogen colonization and disease risk. The skin was the primary reservoir for plasmid-borne antimicrobial resistance and clinically important pathobionts. Strain composition of important commensals such as C. acnes and Staphylococcus epidermidis in SNFDs further indicated a shift from healthy to pro-inflammatory or nosocomial pathogen strains.

Conclusions: Our results constitute the first holistic assessment of the older adult microbiome, raising new hypotheses about the relationship between the microbiota and aging, as well as how they could be leveraged to improve the health of older adults. These findings suggest skin aging may predispose resident microflora to perturbation and highlight the skin as a perhaps the major reservoir for pathogens and antibiotic resistance in older adults.