Strain-level analysis reveals the vertical microbial transmission during the life cycle of bumblebee

Abstract

Background Microbial acquisition and development of the gut microbiota impact the establishment of a healthy host-microbes symbiosis. Compared with other animals, the eusocial bumblebees and honeybees possess a simple, recurring, and similar set of gut microbiota. However, all bee gut phylotypes have high strain-level diversity. Gut communities of different bee species are composed of host-specific groups of strains. The variable genomic regions among strains of the same species often confer critical functional differences, such as carbon source utilization, essential for the natural selection of specific strains. The annual bumblebee colony founded by solitary queens enables tracking the transmission routes of gut bacteria during development stages. Results Here, we first showed the changes in the microbiome of individual bumblebees across their holometabolous life cycle. Some core gut bacteria persist throughout different stages of development. Gut microbiota of newly emerged workers always resembles those of their queens, suggesting a vertical transmission of strains from queens to the newborn workers. We then follow the dynamic changes in the gut community by comparing strain-level metagenomic profiles of queen-worker pairs longitudinally collected across different stages of the nest development. Species composition of both queen and worker shifts with the colony’s growth, and the queen-to-worker vertical inheritance of specific strains was identified. Finally, comparative metagenome analysis showed clear host-specificity for microbes across different bee hosts. Species from honeybees often possess a higher level of strain variation, and they also exhibited more complex gene repertoires linked to polysaccharide digestion. Our results demonstrate bacterial transmission events in bumblebee, highlighting the role of social interactions in driving the microbiota composition. Conclusions By the community-wide metagenomic analysis based on the custom genomic database of bee gut bacteria, we reveal strain transmission events at high resolution and the dynamic changes in community structure along with the colony development. The social annual life cycle of bumblebees is key for the acquisition and development of the gut microbiota. Further studies using the bumblebee model will advance our understanding of the microbiome transmission and the underlying mechanisms, such as strain competition and niche selection.

Microbiome assembly and maintenance across the lifespan of bumble bee workers

“…A final explanation is founder (or foundress) effects. Bumblebee colonies are initiated by a single foundress queen, who is the source of gut symbionts for her offspring (35, 56). A diverse pool of strains may be stochastically sorted into a single foundress queen’s gut, with the established population resistant to subsequent invasion [i.e., priority effects (2)].…”

“…Previous work has outlined the early stages of gut microbiome succession in bumblebees (56)(57)(58), but there is no information on what happens to the microbiome in old age. We also lack information on the temporal dynamics of endogenous processes (e.g., immunity) in the bee gut that control gut microbes, and may be controlled by them (59,60).…”

Bumblebees with the socially transmitted microbiome: A novel model organism for gut microbiota research

“…However, phylogenomic analysis shows that Snodgrassella from Bombus spp. harbor a high level of intra‐species diversity with 5 potential separate clades (Su et al ., 2021). In the honeybee gut, Gilliamella and Snodgrassella live side by side and dominate in the compartment of the ileum (Martinson et al ., 2012; Kwong & Moran, 2016b).…”

“…(Kwong et al ., 2017; Zhang et al ., 2021b). Four bifidobacterial species have been characterized from bumblebee guts ( B. actinocoloniiforme , B. bohemicum , B. commune , B. bombi ) (Killer et al ., 2009; Killer et al ., 2011; Praet et al ., 2015a), and they are phylogenetically clustered together and separated from the species associated with honeybees (Zheng et al ., 2019; Su et al ., 2021). Bombiscardovia is another member of the family Bifidobacteriaceae only found in bumblebees (Killer et al ., 2010).…”

Holobiont Evolution: Population Theory for the Hologenome

“…Experiments with new-born, microbiota-free honeybees showed that horizontal transmission from hive materials and social contact with nest-mates established a typical gut composition (Powell et al . 2014) whereas vertical transmission from queen to workers takes place in bumblebees (Su et al . 2021).…”