The Queen Gut Refines with Age: Longevity Phenotypes in a Social Insect Model

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 without expressing oxidative stress genes, suggesting a very different host environment for age-associated microbial succession.\n\nResultsWe sequenced the microbiota of 63 honey bee queens exploring two chronological ages and four alimentary tract niches. To control for individual 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.\n\nConclusionsWe present a model system linking changes in gut microbiota to diet and longevity, two of the most confounding variables in human microbiota research. As described for other model systems, metabolic changes associated with diet and host longevity correspond to the changing microbiota. 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, our results suggest that lifespan evolution formed the context for host-microbial interactions and age-related succession of honey bee microbiota.