Life history strategies complement niche partitioning to support the coexistence of closely related Gilliamella species in the bee gut

The maintenance of bacterial diversity at both species- and strain-levels
is crucial for the sustainability of honey bee gut microbiota and host
health. Periodic or random fluctuation in diet typically alters the
metabolic niches available to gut microbes, thereby continuously reshaping
bacterial diversity and interspecific interactions. It remains unclear how
closely related bacteria adapt to these fluctuations and maintain
coexistence within the bee gut. Here, we demonstrate that the five
predominant Gilliamella species associated with Apis cerana, a widely
distributed Asiatic honey bee, have diverged in carbohydrate metabolism to
adapt to distinct nutrient niches driven by dietary fluctuation.
Specifically, the glycan-specialists gain improved growth on a pollen-rich
diet, but are overall inferior in competition to non-glycan-specialist on
either a simple sugar or sugar-pollen diet, when co-inoculated in the bee
host and transmitted across generations. Strikingly, despite of their
disadvantage in a high-sugar condition, the glycan-specialists are found
prevalent in natural A. cerana guts. We further reveal that these bacteria
have adopted a life history strategy characterized by high biomass yield
on a low-concentration sugar diet, allowing them to thrive under poor
nutritional conditions, such as when the bee hosts undergo periodical
starvation. Transcriptome analyses indicate that the divergence in life
history strategies is attributed to gene expression programming rather
than genetic variation. This study highlights the importance of
integrative metabolic strategies in carbohydrate utilization, which
facilitate the coexistence of closely related Gilliamella species in a
changing bee gut environment.