Bee breweries: The unusually fermentative, lactobacilli-dominated brood cell microbiomes of cellophane bees

Abstract

Pathogens and parasites of solitary bees have been studied for decades, but the microbiome as a whole is poorly understood for most taxa. Comparative analyses of microbiome features such as composition, abundance, and specificity, can shed light on bee ecology and the evolution of host–microbe interactions. Here we study microbiomes of ground-nesting cellophane bees (Colletidae: Diphaglossinae). From a microbial point of view, the diphaglossine genus Ptiloglossa is particularly remarkable: their larval provisions are liquid and smell consistently of fermentation. We sampled larval provisions and various life stages from wild nests of Ptiloglossa arizonensis and two species of closely related genera: Caupolicana yarrowi and Crawfordapis luctuosa. We also sampled nectar collected by P. arizonensis. Using 16S rRNA gene sequencing, we find that larval provisions of all three bee species are near-monocultures of lactobacilli. Nectar communities are more diverse, suggesting ecological filtering. Shotgun metagenomic and phylogenetic data indicate that Ptiloglossa culture multiple species and strains of Apilactobacillus, which circulate among bees and flowers. Larval lactobacilli disappear before pupation, and hence are likely not vertically transmitted, but rather reacquired from flowers as adults. Thus, brood cell microbiomes are qualitatively similar between diphaglossine bees and other solitary bees: lactobacilli-dominated, environmentally acquired, and non-species-specific. However, shotgun metagenomes provide evidence of a shift in bacterial abundance. As compared with several other bee species, Ptiloglossa have much higher ratios of bacterial to plant biomass in larval provisions, matching the unusually fermentative smell of their brood cells. Overall, Ptiloglossa illustrate a path by which hosts can evolve quantitatively novel symbioses: not by acquiring or domesticating novel symbionts, but by altering the microenvironment to favor growth of already widespread and generalist microbes.

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

“…Lactic acid bacteria are known for their importance to honey bee health (Vásquez et al, 2012; Killer et al, 2014; Iorizzo et al, 2022) and resemble an important part of the bumble bee microbiota. For some ground nesting bees they can be even the dominating taxon within their gut-microbiota (Hammer et al, 2023b).…”

Microbial Metamorphosis: Symbiotic bacteria and fungi proliferate during diapause and may enhance overwintering survival in a solitary bee

“…In previous work on solitary bees, brood cell bacterial microbiomes are highly variable among individuals or composed of more limited taxa (18,19,40,(44)(45)(46). Most commonly in brood cells with consistent microbial communities, lactic acid bacteria are dominant in the provisions, but disappear before pupation (18,19). The loss or extreme reduction of bacteria upon pupation and emergence as adults, combined with evidence suggesting strain sharing between flowers and hosts points to annual environmental acquisition (18,38,47).…”

“…Secondly, the microbiome described here is complex and nearly all brood cells are dominated by 6 core bacterial genera and a single fungus. In previous work on solitary bees, brood cell bacterial microbiomes are highly variable among individuals or composed of more limited taxa (18,19,40,(44)(45)(46). Most commonly in brood cells with consistent microbial communities, lactic acid bacteria are dominant in the provisions, but disappear before pupation (18,19).…”

“…Most commonly in brood cells with consistent microbial communities, lactic acid bacteria are dominant in the provisions, but disappear before pupation (18,19). The loss or extreme reduction of bacteria upon pupation and emergence as adults, combined with evidence suggesting strain sharing between flowers and hosts points to annual environmental acquisition (18,38,47). This acquisition can lead to divergence in microbiomes depending on habitat, as seen in Megachile gut bacteria as it invades new areas and shares microbes with co-foraging bee species (48).…”

“…Moreover, the solitary bee species studied to date generally lack consistent species-specific microbiomes (15,16) in stark contrast to the conserved gut microbial communities found social bee species. While in the brood cells of some bee species, stored nectar and pollen can be dominated by lactobacilli these bacteria do not persist or are detected in very low abundance in the bee gut after defecation and during larval diapause (17)(18)(19). The combination of an annual phenology, solitary nesting, holometabolous development (complete metamorphosis), and lack of direct brood care may impede the persistence and transmission of a specialized core microbiome (20,21).…”