Trypanosome Infection Disturbs the Gut Microbiota of Bumble Bee Hosts

Host-microbe interactions are ubiquitous with both positive and negative outcomes for host health and fitness. While pathogens abound, there has been an increased focus beneficial host-microbial community associations, such as native gut microbiota that can aid in disease resistance, nutrient sequestration, and detoxification. However, while beneficial microbes can protect against infection, there is a limited appreciation for how pathogen infection may disrupt healthy gut microbiota structure and function. Crithidia bombi is a common trypanosomatid gut parasite of bumble bees with fitness-relevant effects on individuals and colonies. The native bumble bee gut microbiota has been shown to increase protection against Crithidia, and an association has been found between infection occurrence and host gut microbiota structure in nature. However, we hypothesize that the association between gut microbiota structure and infection could also emerge if infection disrupts the healthy gut community, especially early during the gut community establishment. Using experimental inoculations, we investigate if Crithidia infection alters the bumble bee gut microbiota community. Bombus impatiens workers were exposed early in microbiota colonization or post-establishment to one of three C. bombi strains or left naïve. Subsequently, guts were dissected to quantify total bacterial load, numbers of key bumble bee gut bacterial symbionts, and C. bombi. We find that infection by Crithidia leads to a reduction in total gut bacteria, and when it occurs early during microbiota colonization, Lactobacillus spp. and Gilliamella spp. numbers are reduced and increased, respectively. This provides evidence for an infection-mediated disruption of the gut microbiota balance, which could explain microbiota structure and infection associations in the field. Furthermore, healthy microbiota perturbation is another way that pathogens may detrimentally affect hosts, and may underlie some previously described infection effects. This adds to our understanding of the multi-dimensional and directionality of effects between host organisms and their parasitic and beneficial microbes