Temperature dependence of parasitic infection and gut bacterial communities in bumble bees

Authors: Palmer-Young, Evan; NGOR, LYNA - University Of California; NEVAREZ, RODRIGO - University Of California; ROTHMAN, JASON - University Of California; RAFFEL, THOMAS - Oakland University; MCFREDERICK, QUINN - University Of California

Submitted to: Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/13/2019
Publication Date: 10/1/2019
Citation: Palmer-Young, E.C., Ngor, L., Nevarez, R.B., Rothman, J.A., Raffel, T.R., Mcfrederick, Q.S. 2019. Temperature dependence of parasitic infection and gut bacterial communities in bumble bees. Environmental Microbiology. 21(12):4706-4723. https://doi.org/10.1111/1462-2920.14805.
DOI: https://doi.org/10.1111/1462-2920.14805

Interpretive Summary: Both gut microbiota and host body temperature, including fever, can influence resistance to infection. However, the effects of temperature on gut microbiota, and the consequences of these effects for resistance to infection, remain unexplored. Our experiments with bumble bees and an intestinal parasite show dramatic reductions in infection intensity at high temperatures, along with subtle changes in the size and community composition of the gut bacterial microbiota that contribute to host resistance. These results indicate that high body temperatures may reduce parasitic infection by clearing pathogens while sparing or encouraging growth of beneficial bacteria, highlighting an unexplored mechanism by which febrile temperatures could ameliorate disease. Our findings have implications for both bumble bee conservation and, more generally, our understanding of how febrile temperatures and climate affect host-parasite interactions in humans and wildlife.

Technical Abstract: High temperatures (e.g. fever) and gut microbiota can both influence host resistance to infection. However, effects of temperature-driven changes in gut microbiota on resistance to parasites remain unexplored. We examined the temperature dependence of infection and gut bacterial communities in bumble bees infected with the trypanosomatid parasite Crithidia bombi. Infection intensity decreased by over 80% between 21 and 37 °C. Temperatures of peak infection were lower than predicted based on parasite growth in vitro, consistent with mismatches in thermal performance curves of hosts, parasites, and gut symbionts. Gut bacterial community size and composition exhibited slight but significant, non-linear, and taxon-specific responses to temperature. Abundance of total gut bacteria and of Orbaceae, both negatively correlated with infection in previous studies, were positively correlated with infection here. Prevalence of the bee pathogen-containing family Enterobacteriaceae declined with temperature, suggesting that high temperature may confer protection against diverse gut pathogens. Our results indicate that resistance to infection reflects not only the temperature dependence of host and parasite performance, but also temperature-dependent activity of gut bacteria. The thermal ecology of gut parasite-symbiont interactions may be broadly relevant to infectious disease, both in ectothermic organisms that inhabit changing climates, and in endotherms that exhibit fever-based immunity.