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

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.

Microbiome assembly and maintenance across the lifespan of bumble bee workers

“…Despite exposure to microbes present in the diet and rearing environment, gut microbiomes of workers from both commercial Bombus impatiens and wild-queen-derived B. impatiens and B. ternarius colonies are almost entirely dominated by the core, hostspecialized bacterial taxa known to be prevalent in bumble bees (Hammer, Le, Martin, & Moran, 2021; Figure 2a; Figure S3). Bacteria previously observed in microbiome-disrupted bumble bees, such as Enterobacteriaceae (Li, Powell, et al, 2015;Meeus et al, 2015;Parmentier et al, 2016) and Fructobacillus (Koch et al, 2012;Krams et al, 2022), are virtually absent from the 16S rRNA gene amplicon data sets, including commercial bee midguts (Figure S4) and hindguts (Figure 2a) and wild-queen-derived colonies (Figure S5). The single exception is a male bee from one of the latter colonies, which has a large proportion of Klebsiella (Enterobacteriaceae) and fungal sequences (Figure S5).…”

Microbiome assembly and maintenance across the lifespan of bumble bee workers

“…2C). Microbes previously observed in microbiome-disrupted bumblebees, such as Enterobacteriaceae (54, 69, 70), Fructobacillus (55, 71), and fungi (72), are virtually absent in the 16S amplicon datasets, including commercial bee midguts (Fig. S8) and hindguts (Fig.…”

Bumble bee microbiota shows temporal succession and increase of lactic acid bacteria when exposed to outdoor environments

“…In general, mainly Enterobacteriaceae , Apibacter ( Weeksellaceae ) and Fructobacillus ( Lactobacillaceae ) are considered as environmentally acquired strains, as these groups usually lack in laboratory environments (Newbold et al, 2015; Hammer et al, 2021a). Environmental influences can be shown by location or habitat dependence, as colonies of B. terrestris near forest environments were dominated by Fructobacillus compared to colonies in agricultural or horticultural landscapes (Krams et al, 2022). An investigation of 28 Chinese bumble bee species revealed two distinct enterotypes either dominated by core-members of the microbiota ( Snodgrassella and Gilliamella ) or by externally acquired microbes mainly belonging to Enterobacteriaceae (Li et al, 2015).…”

“…Besides these hive-maintained core-set of microbes, bumble bees can acquire several strains from the environment, which are considered non-core members, as they are usually lacking in laboratory rearing (Hammer et al, 2021a). Environmental acquisition can have a dominant influence on the microbiota of B. terrestris (Bosmans et al, 2018; Krams et al, 2022). A shift in the bumble bee microbiota composition when moved outdoors suggests that particularly enterobacteria are acquired from outdoor environments.…”