Dominance of Fructose-Associated Fructobacillus in the Gut Microbiome of Bumblebees (Bombus terrestris) Inhabiting Natural Forest Meadows

SIMPLE SUMMARY: A vast array of microorganisms colonize invertebrates and vertebrates. Most of these microbes reside in the digestive tract, where they constitute the intestinal (gut) microbiome. Some microbes are commensal, coexisting with their host without causing harm, while others can be mutualistic or pathogenic. Mutualistic microorganisms perform many health-related functions such as promoting digestion and acquisition of nutrients; hormone regulation; maintenance and control of the immune system; regulation of homeostasis and stress physiology of the body; insecticide resistance; production of certain vitamins; and providing protection against pathogenic microorganisms, parasites, and diseases. Bee-specific bacterial genera such as Lactobacillus, Snodgrassella, and Gilliamella dominate the gut communities of many bumblebees. This study confirmed Lactobacillus, Snodgrassella, and Gilliamella as dominant gut bacteria of the buff-tailed bumblebee Bombus terrestris in the agricultural landscape. However, we show that the guts of B. terrestris from natural forest habitats can be dominated by fructose-associated Fructobacillus spp. Our findings may have important implications for understanding the ecological role of bumblebees and the reasons for the decline of key pollinators. ABSTRACT: Bumblebees are key pollinators in agricultural landscapes. However, little is known about how gut microbial communities respond to anthropogenic changes. We used commercially produced colonies of buff-tailed bumblebees (Bombus terrestris) placed in three habitats. Whole guts (midgut, hindgut, and rectum) of B. terrestris specimens were dissected from the body and analyzed using 16S phylogenetic community analysis. We observed significantly different bacterial community composition between the agricultural landscapes (apple orchards and oilseed rape (Brassica napus) fields) and forest meadows, whereas differences in gut communities between the orchards and oilseed rape fields were nonsignificant. Bee-specific bacterial genera such as Lactobacillus, Snodgrassella, and Gilliamella dominated gut communities of B. terrestris specimens. In contrast, the guts of B. terrestris from forest meadows were dominated by fructose-associated Fructobacillus spp. Bacterial communities of workers were the most diverse. At the same time, those of males and young queens were less diverse, possibly reflecting greater exposure to the colony’s inner environment compared to the environment outside the colony, as well as bumblebee age. Our results suggest that habitat quality, exposure to environmental microbes, nectar quality and accessibility, and land use significantly affect gut bacterial composition in B. terrestris.