Early Signs of Gut Microbiome Aging: Biomarkers of Inflammation, Metabolism, and Macromolecular Damage in Young Adulthood

Citation

Renson, Audrey; Harris, Kathleen Mullan; Dowd, Jennifer Beam; Gaydosh, Lauren; McQueen, Matthew B.; Krauter, Kenneth S.; Shanahan, Michael J.; & Aiello, Allison E. (2020). Early Signs of Gut Microbiome Aging: Biomarkers of Inflammation, Metabolism, and Macromolecular Damage in Young Adulthood. Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 75(7), 1258-1266. PMCID: PMC7302166

Abstract

Emerging links between gut microbiota and diseases of aging point to possible shared immune, metabolic, and cellular damage mechanisms, operating long before diseases manifest. We conducted 16S rRNA sequencing of fecal samples collected from a subsample (n=668) of Add Health Wave V, a nationally representative longitudinal study of adults aged 32-42. An overlapping subsample (n=345) included whole blood RNA-seq. We examined associations between fecal taxonomic abundances and dried blood spot-based markers of lipid and glucose homeostasis and C-reactive protein (measured in Wave IV), as well as gene expression markers of inflammation, cellular damage, immune cell composition, and transcriptomic age (measured in Wave V), using Bayesian hierarchical models adjusted for potential confounders. We additionally estimated a co-abundance network between inflammation-related genes and bacterial taxa using penalized Gaussian graphical models. Strong and consistent microbiota associations emerged for HbA1c, glucose, C-reactive protein, and principal components of genes upregulated in inflammation, DNA repair, and reactive oxygen species, with Streptococcus infantis, Pseudomonas spp., and Peptoniphilus as major players for each. This pattern was largely echoed (though attenuated) for immunologic cell composition gene sets, and only Serratia varied meaningfully by transcriptomic age. Network co-abundance indicated relationships between Prevotella sp., Bacteroides sp., and Ruminococcus sp. and gut immune/metabolic regulatory activity, and Ruminococcussp, Dialister, and Butyrivibriocrossotus with balance between Th1 and Th2 inflammation. In conclusion, many common associations between microbiota and major physiologic aging mechanisms are evident in early-mid adulthood, and suggest avenues for early detection and prevention of accelerated aging.

URL

http://dx.doi.org/10.1093/gerona/glaa122

Reference Type

Journal Article

Year Published

2020

Journal Title

Journals of Gerontology Series A: Biological Sciences and Medical Sciences

Author(s)

Renson, Audrey
Harris, Kathleen Mullan
Dowd, Jennifer Beam
Gaydosh, Lauren
McQueen, Matthew B.
Krauter, Kenneth S.
Shanahan, Michael J.
Aiello, Allison E.

Article Type

Regular

PMCID

PMC7302166

Data Set/Study

National Longitudinal Study of Adolescent to Adult Health (Add Health)

Continent/Country

United States of America

State

Nonspecific

ORCiD

Aiello - 0000-0001-7029-2537
Renson - 0000-0003-1603-2587