Temperature dependent, pH-mediated inhibition of parasite growth and infection by gut microbiota of bumble bees

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

Submitted to: Ecological Society of America Abstracts
Publication Type: Abstract Only
Publication Acceptance Date: 6/14/2020
Publication Date: N/A
Citation: N/A

Interpretive Summary: Both gut microbiota and host body temperature, including fever, can influence resistance to infection in animals. However, the effects of temperature on gut microbiota, and the consequences of these effects for host resistance to infection, remain unexplored. Bumble bees can maintain high body and nest temperatures during flight and in their nests, and have a gut symbiont community that enhances host resistance to gut parasites. Using a widespread bumble bee parasite and co-occurring gut bacterial symbiont, we tested the hypothesis that high temperatures reduce infection by favoring growth of non-pathogenic bacteria that inhibit parasites. Our results demonstrated that (1) Compared to parasites, bacterial symbionts grew more rapidly at higher temperatures, and tolerated higher maximum temperatures (2) Symbiont metabolites inhibited parasite growth via production of acids that was both necessary and sufficient for inhibition. Inhibition occurred within the pH range previously observed in honey bee guts. (3) Inhibitory effects of symbionts increased with temperature, reflecting accelerated production of acids, and reduced the optimal growth temperature for parasites in vitro. (4) In live bees, infection intensity decreased by over 80% between 21 and 37 °C. Temperatures of peak infection were lower than predicted based on growth of isolated parasites, consistent with the hypothesis that high temperatures provide a competitive advantage to non-pathogenic bacteria, and potentiate the ability of these bacteria to reduce infection by parasites. Results indicate that a temperature increase over the range measured in bumble bee colonies would favor non-pathogenic bacterial symbionts over parasites, potentiate the pH-dependent inhibition of parasites by symbiont metabolites, and reduce infection intensity without disrupting the core gut microbiota. High temperatures, whether due to host endothermy or environmental factors, could reduce parasitic infection by inhibiting parasites while sparing or promoting growth of beneficial symbionts. These experiments highlight a relatively unexplored, symbiont-mediated mechanism by which fever could counteract infection in animals.

Technical Abstract: Background/Question/Methods Both gut microbiota and host body temperature, including fever, can influence resistance to infection in host-parasite systems. Metabolic theory equations have been used to predict the temperature dependence of infection outcome based on differences in the thermal performance curves of parasite performance and host immune function. However, the effects of temperature on gut microbiota, and the consequences of these effects for host resistance to infection, remain unexplored. Bumble bees can maintain high body and nest temperatures during flight and incubation, and harbor a consistent core gut symbiont community that enhances host resistance to gut parasites. Using a widespread bumble bee trypanosomatid parasite (Crithidia bombi) and co-occurring gut bacterial symbiont (Lactobacillus bombicola), we tested the hypothesis that high temperatures reduce infection by selectively promoting growth of non-pathogenic symbionts that inhibit parasites. Specifically, we (1) Used metabolic theory equations to characterize differential responses of growth to temperature in parasite and symbiont cell cultures (2) Demonstrated chemically mediated inhibition of parasite growth by symbiont metabolic products (3) Assessed the temperature dependence of symbiont-mediated inhibition in parasite/symbiont co-cultures, and (4) Tested the temperature dependence of infection and gut microbial composition in bumble bees Results/Conclusions (1) Compared to parasites, bacterial symbionts had higher temperatures of peak growth and upper limits of thermotolerance. (2) Symbiont metabolites inhibited parasite growth via a reduction in pH that was both necessary and sufficient for inhibition. Inhibition occurred within the pH range previously observed in honey bee guts. (3) Inhibitory effects of symbionts increased with temperature, reflecting accelerated production of acids, and reduced the optimal growth temperature for parasites in vitro. (4) In live bees, 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. Results indicate that a temperature increase over the range measured in bumble bee colonies would favor non-pathogenic bacterial symbionts over parasites, potentiate the pH-dependent inhibition of parasites by symbiont metabolites, and reduce infection intensity without disrupting the core gut microbiota. High temperatures, whether due to host endothermy or environmental factors, could reduce parasitic infection by inhibiting parasites while sparing or promoting growth of beneficial symbionts. These experiments highlight a relatively unexplored, symbiont-mediated mechanism by which febrile temperatures could ameliorate disease in animals.