Microbiome assembly and maintenance across the lifespan of bumble bee workers

How a host’s microbiome changes over its lifespan can influence
development and aging. As these temporal patterns have only been described
in detail for humans and a handful of other hosts, an important next step
is to compare microbiome dynamics across a broader array of host-microbe
symbioses, and to investigate how and why they vary. Here we characterize
the temporal dynamics and stability of the bumblebee worker gut
microbiome. Bumblebees are a useful symbiosis model given their relatively
well-understood life history and simple, host-specific gut bacterial
communities. Furthermore, microbial dynamics may influence bumblebee
health and pollination services. We combined high-temporal-resolution
sampling with 16S rRNA gene sequencing, quantitative PCR, and shotgun
metagenomics to characterize gut microbiomes over the adult lifespan of
Bombus impatiens workers. To understand how hosts may control (or lose
control of) the gut microbiome as they age, we also sequenced hindgut
transcriptomes. We found that, at the community level, microbiome assembly
is highly predictable and similar to patterns of primary succession
observed in the human gut. At the same time, partitioning of strain-level
bacterial variants among colonies suggests stochastic colonization events
similar to those observed in flies and nematodes. We also find strong
differences in temporal dynamics among symbiont species, suggesting
ecological differences among microbiome members in colonization and
persistence. Finally, we show that both the gut microbiome and host
transcriptome—including expression of key immunity genes—stabilize, as
opposed to senesce, with age. We suggest that in highly social groups such
as bumblebees, maintenance of both microbiomes and immunity contribute to
the inclusive fitness of workers, and thus remain under selection even in
old age. Our findings provide a foundation for exploring the mechanisms
and functional outcomes of bee microbiome succession, and for comparative
analyses with other host-microbe symbioses.