Abstract
BackgroundIn social insects, identical genotypes can show extreme lifespan variation providing a unique perspective on age-associated microbial succession. In honey bees, short- and long-lived host phenotypes are polarized by a suite of age-associated factors including hormones, nutrition, immune senescence, and oxidative stress. Similar to other model organisms, the aging gut microbiota of short-lived (worker) honey bees accrue Proteobacteria and are depleted of Lactobacillus and Bifidobacterium, consistent with a suite of host senescence markers. In contrast, long-lived (queen) honey bees maintain youthful cellular function with much lower expression of oxidative stress genes, suggesting a very different host environment for age-associated microbial succession.ResultsWe sequenced the microbiota of 63 honey bee queens exploring two chronological ages and four alimentary tract niches. To control for genetic and environmental variation, we quantified carbonyl accumulation in queen fat body tissue as a proxy for biological aging. We compared our results to the age-specific microbial succession of worker guts. Accounting for queen source variation, two or more bacterial species per niche differed significantly by queen age. Biological aging in queens was correlated with microbiota composition highlighting the relationship of microbiota with oxidative stress. Queens and workers shared many major gut bacterial species, but differ markedly in community structure and age succession. In stark contrast to aging workers, carbonyl accumulation in queens was significantly associated with increased Lactobacillus and Bifidobacterium and depletion of various Proteobacteria.ConclusionsWe present a model system linking changes in gut microbiota to diet and longevity, two of the most confounding variables in human microbiota research. The pattern of age-associated succession in the queen microbiota is largely the reverse of that demonstrated for workers. The guts of short-lived worker phenotypes are progressively dominated by three major Proteobacteria, but these same species were sparse or significantly depleted in long-lived queen phenotypes. More broadly, age-related changes in the honey bee microbiota reflect the regulatory anatomy of reproductive host metabolism. Our synthesis suggests that the evolution of colony-level reproductive physiology formed the context for host-microbial interactions and age-related succession of honey bee microbiota.
Highlights
In social insects, identical genotypes can show extreme lifespan variation providing a unique perspective on age-associated microbial succession
We examined the relationship between biological aging and the microbiota in various ways: (1) we performed distance-based linear model (DistLM) on the top 37 Operational taxonomic unit (OTU) to test whether the microbiota from each of four distinct tissues is significantly associated with carbonyl accumulation in queens, (2) we examined carbonyl accumulation as a covariate in three separate multivariate analysis of covariance (MANCOVA) models, (3) we calculated independent Pearson’s correlations between species-specific centered log ratio (CLR) scores and log transformed carbonyl data, and (4) we performed principle component analysis (PCA) on CLR scores from OTUs 1–9, plotting the relationship of bacterial community composition and age-associated succession relative to carbonyl accumulation by niche
Subtracting the rare biosphere (1.2%), these nine OTUs are the focus of most analyses and are what we present in figures
Summary
Identical genotypes can show extreme lifespan variation providing a unique perspective on age-associated microbial succession. Long-lived (queen) honey bees maintain youthful cellular function with much lower expression of oxidative stress genes, suggesting a very different host environment for age-associated microbial succession. Attributed to caste-specific diets, the phospholipid profile of aging workers becomes increasingly susceptible to oxidative stress, but the queen profile remains stable with age [8] Consistent with these results, antioxidant gene expression increases in aging workers but not queens [9, 10]. Workers live longer when fed the queen diet (royal jelly) as compared to a pollen diet [11] These results suggest that the drastically different lifespans and diets associated with division of labor in honey bees provide a model for mechanisms of diet, aging, and microbiota [12, 13]
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