Dynamic Changes of Gut Microbial Communities of Bumble Bee Queens through Important Life Stages

Bumble bees are important pollinators in natural and agricultural ecosystems. Their social colonies are founded by individual queens, which, as the predominant reproductive females of colonies, contribute to colony function through worker production and fitness through male and new queen production. Therefore, queen health is paramount, but even though there has been an increasing emphasis on the role of gut microbiota for animal health, there is limited information on the gut microbial dynamics of bumble bee queens. Employing 16S rRNA amplicon sequencing and quantitative PCR, we investigate how the adult life stage and physiological state influence a queen’s gut bacterial community diversity and composition in unmated, mated, and ovipositing queens of Bombus lantschouensis. We found significant shifts in total gut microbe abundance and microbiota composition across queen states. There are specific compositional signatures associated with different stages, with unmated and ovipositing queens showing the greatest similarity in composition and mated queens being distinct. The bacterial genera Gilliamella, Snodgrassella, and Lactobacillus were relatively dominant in unmated and ovipositing queens, with Bifidobacterium dominant in ovipositing queens only. Bacillus, Lactococcus, and Pseudomonas increased following queen mating. Intriguingly, however, further analysis of unmated queens matching the mated queens in age showed that changes are independent of the act of mating. Our study is the first to explore the gut microbiome of bumble bee queens across key life stages from adult eclosion to egg laying and provides useful information for future studies of the function of gut bacteria in queen development and colony performance. IMPORTANCE Bumble bee queens undergo a number of biological changes as they transition through adult emergence, mating, overwintering, foraging, and colony initiation including egg laying. Therefore, they represent an important system to understand the link between physiological, behavioral, and environmental changes and host-associated microbiota. It is plausible that the bumble bee queen gut bacteria play a role in shaping the ability of the queen to survive environmental extremes and reproduce, due to long-established coevolutionary relationships between the host and microbiome members.