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

Larson, Peter J.; Zhou, Wei; Santiago, Alba; Driscoll, Sarah; Fleming, Elizabeth; Voigt, Anita Y.; Chun, Ock K.; Grady, James J.; Kuchel, George A.; Robison, Julie; Oh, Julia

doi:10.1038/s43587-022-00287-9

Cited by 39 publications

(69 citation statements)

References 97 publications

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“…However, this species was proven to be an essential member of the human skin commensals [52,53] and emerged as the second most abundant species on the skin of Han Chinese [27]. Here, we con rmed the association of M. osloensis with premature-aging traits and further validated its capability of promoting skin cell senescence, which explained the premature aging phenotype in Chinese and other elderly populations [54].…”

Section: Discussionsupporting

confidence: 58%

Integration of skin phenome and microbiome reveals the key role of bacteria in human skin aging

Xia

Zhong

et al. 2023

Preprint

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Background: Despite the complexity, distinct ecological niches are believed to primarily drive the skin microbiome composition. Meanwhile, skin aging is a dynamic process with a spectrum of phenotypical changes, making it an attractive model for studying microbiome-phenotype interactions. Although a large number of studies confirmed the impact of chronological age in skin bacterial communities, the understanding of cross-kingdom microbiome variation with skin aging remains minimal. And this is not trivial because one’s skin condition or perceived age may deviate largely from their actual age as skin aging is a complex process combining chronological and extrinsic aging. Results: To this end, 822 facial microbial samples and skin phenotypes from the corresponding area were assessed in a Chinese cohort, the largest population size to date for skin shotgun metagenomic profiling. Our data revealed that among 14 measured variables, porphyrin and chronological age explained the most significant microbial variability. Consistent with previous studies based on 16S rRNA gene sequencing, we revealed increased biodiversity with aging and further specified age-associated species across kingdoms. While the abundance of most bacteria increased with age, two species, Cutibacterium acnes and Aeromicrobium choanae, declined. Microbiome undergoes active function selection from energy demands/growth to stress adaptation along aging. In addition, we characterized microbial changes in skin aging, asa combined consequence of both intrinsic and extrinsic reasons and reflecting the actual dynamic of niche conditions rather than chronological age. Using the multiple linear regression model, we predicted premature-aging/delayed-aging-related microbial species, mainly localizing to Moraxella osloensis and C. acnes. Furthermore, we validated the biological functions in vitro of some host-microbe interactions predicted by the microbiome-skin phenome association network. M. osloensis regulated collagen metabolism, extracellular matrix assembly and promoted cell senescence in human keratinocyte and fibroblast cells. Conclusions: We presume that application of both culture-independent and culture-dependent approaches can advance a good understanding of microbiome-phenotype interactions. Our study is of significance for designing interventions against aging-related skin conditions.

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Section: Discussionsupporting

confidence: 58%

Integration of skin phenome and microbiome reveals the key role of bacteria in human skin aging

Xia

Zhong

et al. 2023

Preprint

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“…On the contrary, CDC was the only variable associated with the abundance of any S. epidermidis clade (L, p=0.0066, q=0.21; M, p=0.001, q=0.068) at q=0.25 (Figure 3D). S. epidermidis clade L contains strains found in nosocomial infections and was previously shown to be enriched in older adults living in skilled nursing facilities 7 . Thus, the negative association between CDC and S. epidermidis clade L suggests a possible link between the falling collagen quantity and quality in older adults and the susceptibility to nosocomial infections.…”

Section: Changes In Strain-level Population Structure During Skin Agingmentioning

confidence: 99%

“…While these physiologic changes undoubtedly result in corresponding changes in skin microbiome composition [11][12][13][14][15][16][17] , a well-controlled, high-resolution characterization taken together with detailed biophysical skin measurements is lacking. On one hand, confounding factors such as sex, ethnicity, geography, and health condition can all affect skin microbiome 18 , which increase data dimensionality and decrease statistical power 7 . On the other hand, while previous investigations revealed aging-related skin microbiome changes at phylum-to genus-resolution 11,[14][15][16][17][18] , studies by our group and others have shown that the aging-related diversity of the skin microbiome is often manifested at species-, strain-, or genelevel 7 .…”

Section: Introductionmentioning

confidence: 99%

“…On one hand, confounding factors such as sex, ethnicity, geography, and health condition can all affect skin microbiome 18 , which increase data dimensionality and decrease statistical power 7 . On the other hand, while previous investigations revealed aging-related skin microbiome changes at phylum-to genus-resolution 11,[14][15][16][17][18] , studies by our group and others have shown that the aging-related diversity of the skin microbiome is often manifested at species-, strain-, or genelevel 7 . Moreover, such high-resolution diversity has potential health implications.…”

Section: Introductionmentioning

confidence: 99%

“…Moreover, such high-resolution diversity has potential health implications. For example, we found that a phylogenetic clade of Staphylococcus (S.) epidermidis, which contains strains associated with nosocomial infections, was significantly enriched in adults living in skilled nursing facilities, compared to younger adults 7 . We hypothesize that these high-resolution changes in the skin microbiome are not only a biomarker of aging but also associated with aging-induced biophysical changes in the skin.…”

Section: Introductionmentioning

confidence: 99%

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Skin microbiome attributes associate with biophysical skin aging

Zhou

Fleming

Legendre³

et al. 2023

Preprint

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Two major arms of skin aging are changes in the biophysical conditions of the skin and alterations in the skin microbiome. This work partitioned both arms to study their interaction in detail. Leveraging the resolution provided by shotgun metagenomics, we explored how skin microbial species, strains, and gene content interact with the biophysical traits of the skin during aging. With a dataset well-controlled for confounding factors, we found that skin biophysical traits, especially the collagen diffusion coefficient, are associated with the composition and the functional potential of the skin microbiome, including the abundance of bacterial strains found in nosocomial infections and the abundance of antibiotic resistance genes. Our findings reveal important associations between skin biophysical features and aging-related changes in the skin microbiome and generate testable hypotheses for the mechanisms of such associations.

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Wound Healing in the Geriatric Population

Gorenstein,

Droz,

Gillette

2023

Acute Care Surgery in Geriatric Patients

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

Cited by 39 publications

References 97 publications

Integration of skin phenome and microbiome reveals the key role of bacteria in human skin aging

Integration of skin phenome and microbiome reveals the key role of bacteria in human skin aging

Skin microbiome attributes associate with biophysical skin aging

Wound Healing in the Geriatric Population

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

Cited by 39 publications

References 97 publications

Integration of skin phenome and microbiome reveals the ­key role of bacteria in human skin aging

Integration of skin phenome and microbiome reveals the ­key role of bacteria in human skin aging

Skin microbiome attributes associate with biophysical skin aging

Wound Healing in the Geriatric Population

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Product

Resources

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Integration of skin phenome and microbiome reveals the key role of bacteria in human skin aging

Integration of skin phenome and microbiome reveals the key role of bacteria in human skin aging