Membership robustness but structural change of the native gut microbiota of bumble bees upon systemic immune induction

Authors: SAUERS, LOGAN - Illinois State University; BASSINGTHWAITE, TOBY - Illinois State University; SIERRA-RIVERA, BRYAN - Illinois State University; Hampton, Kylie; Duffield, Kristin; Gore, Haley; Ramirez, Jose; SADD, BEN - Illinois State University

Submitted to: Microbiology Spectrum
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/26/2024
Publication Date: 10/7/2024
Citation: Sauers, L.A., Bassingthwaite, T., Sierra-Rivera, B., Hampton, K.J., Duffield, K.R., Gore, H., Ramirez, J.L., Sadd, B.M. 2024. Membership robustness but structural change of the native gut microbiota of bumble bees upon systemic immune induction. Microbiology Spectrum. https://doi.org/10.1128/spectrum.00861-24.
DOI: https://doi.org/10.1128/spectrum.00861-24

Interpretive Summary: The microorganisms that comprise an insect’s gut (i.e., its microbiome) are critically important to its health and ability to resist harmful environmental conditions (e.g., disease and pesticides). Importantly, the immune system may play an integral role in shaping the community of microbial species within the microbiome. While pollinating insects, such as bumblebees, play an important role in food production, they are highly susceptible to disease and chemical insecticides. Here, we assessed how the immune system of the common eastern bumble bee, Bombus impatiens, an important pollinator native to eastern North America, shapes its core gut microbiome. Specifically, we investigated how the beneficial microbes in the gut of B. impatiens respond to nonpathogenic stimulation of B. impatiens immune system with heat-killed bacteria. We found that immune stimulation altered the colonization of, and associations between, the core microbes in bumblebees. Specifically, we found that changes in microbial community structure due to an immune challenge resulted in an imbalance of microbial species. Our results highlight the importance of the immune system in determining the microbiome structure and has important implications for developing strategies to protect native pollinators.

Technical Abstract: Understanding factors influencing the composition and maintenance of beneficial host-associated microbial communities is central to understanding their ecological, evolutionary, and health consequences for hosts. Host immunity is often implicated as a regulator of these microbiota, but immunity may also play a disruptive role, with responses to infection perturbing beneficial communities. Such effects may be more prominent from innate immune responses, with more rapid-acting and often non-specific components, compared to adaptive responses. We investigated how upregulation of antibacterial immunity in the bumble bee Bombus impatiens affects its core gut microbiota, testing the hypothesis that immunity-induced perturbation impacts the microbiota structure. Freshly emerged adult bees were fed a microbiota inoculum before receiving a non-pathogenic immune stimulation injection. We quantified microbial communities using 16S rRNA amplicon sequencing and targeted quantitative PCR. Coarse community membership shows apparent robustness, but we find that immune stimulation alters the abundance of two core community members, Gilliamella and Snodgrassella. Moreover, a positive association in communities between these bacteria is perturbed following a Gram-negative challenge. The observed changes in the gut microbial community are suggestive of immune response-induced dysbiosis, linking ecological interactions across levels between hosts, their pathogens, and their beneficial gut microbiota. The potential for collateral perturbation of the natural gut microbiota following an innate immune response may contribute to immune costs, shaping the evolutionary optimization of immune investment depending on the ecological context.