Core symbionts, age at inoculation, and diet affect colonization of the bumble bee gut by a common bacterial pathogen

<p dir="ltr">Microbes shape the health of bumble bees, an important group of pollinators including species of conservation concern. Most microbial research on bumble bees has focused on eukaryotic and viral pathogens or the core gut microbiome, a community of host-specialized bacterial symbionts that helps protect hosts against eukaryotic pathogens.</p><p dir="ltr">Bumble bees also harbor a third class of microbes: non-core gut bacteria, which are non-host-specific and vary among individuals. Understanding their functional role and how they interact with core symbionts is important for bumble bee ecology and management.</p><p dir="ltr">We surveyed non-core bacteria in wild bumble bee workers (<i>Bombus impatiens</i>) and conducted lab experiments with gnotobiotic <i>B. impatiens</i> to examine factors shaping colonization by a focal non-core bacterium (<i>Serratia marcescens</i>) and its consequences for bee health.</p><p dir="ltr">Non-core bacteria, including <i>Serratia</i>, frequently occur at high abundance in wild bumble bees, with roughly half of individuals harboring at least 10% non-core gut bacteria. Experiments showed that <i>Serratia marcescens</i> better colonizes the gut when bees are inoculated early (within one day of adult emergence) and the core gut microbiome is disrupted. A mixed wildflower pollen diet facilitated the highest level of infection compared to two monofloral pollen treatments. We also provide evidence that <i>Serratia</i><i> </i>is pathogenic: exposing bees with disrupted gut microbiomes to <i>Serratia</i> strongly reduced lifespan and, as a result, also reduced total reproduction.</p><p dir="ltr">These results have three important implications: first, non-core bacteria are widespread in wild bumble bees, and some species are opportunistic pathogens. Second, the core gut microbiome plays a crucial role in protecting against these pathogens. Third, the timing of inoculation relative to bee age, as well as diet, are key factors controlling bacterial pathogen colonization of the gut. Overall, these findings suggest that gut bacterial health could be an important target for monitoring and managing bumble bee health.</p><p dir="ltr">All data and R scripts are permanently archived in Dryad: https://doi.org/10.5061/dryad.qbzkh18t1</p>