Palmer-Young, E. C. | Search bioRxiv

bioRxiv2018

Temperature-mediated inhibition of a bumble bee parasite by an intestinal symbiont

Competition between organisms is often mediated by environmental factors including temperature. In animal intestines, nonpathogenic symbionts compete physically and chemically against pathogens, with consequences for host infection. We used metabolic theory-based models to characterize differential responses to temperature of a bacterial symbiont and a co-occurring trypanosomatid parasite of bumble bees, which regulate body temperature during flight and incubation. We hypothesized that inhibition of parasites by bacterial symbionts would increase with temperature, due to symbionts having higher optimal growth temperatures than parasites.\n\nWe found that a temperature increase over the range measured in bumble bee colonies would favor symbionts over parasites. As predicted by our hypothesis, symbionts reduced the optimal growth temperature for parasites, both in direct competition and when parasites were exposed to symbiont spent medium. Inhibitory effects of the symbiont increased with temperature, reflecting accelerated growth and acid production by symbionts. Our results indicate that high temperatures, whether due to host endothermy or environmental factors, can enhance the inhibitory effects of symbionts on parasites. Temperature-modulated manipulation of microbiota could be one explanation for fever- and heat-induced reductions of infection in animals, with consequences for diseases of medical and conservation concern.

ecology↗

bioRxiv2018

pH-mediated inhibition of a bumble bee parasite by an intestinal symbiont

Non-pathogenic microbes can provide multiple benefits to their hosts, including pathogen inhibition. Gut symbionts can augment resistance to pathogens by stimulating host immune responses, competing for space and nutrients, or producing antimicrobial metabolites. The gut microbiota of social bees, which pollinate many crops and wildflowers, has demonstrated benefits against diverse infections and might help protect against pathogen-related declines. The bumble bee gut microbiota, consisting chiefly of five taxa common to corbiculate bees, has been shown to enhance resistance to the trypanosomatid parasite Crithidia bombi. Specifically, infection intensity was negatively correlated with abundance of Lactobacillus \"Firm-5\" bacteria. However, the mechanism underlying this relationship remains unknown. We tested the hypothesis that the Firm-5 bacterium Lactobacillus bombicola, which produces lactic acid, inhibits C. bombi via a pH-mediated effect.\n\nConsistent with our hypothesis, Lactobacillus bombicola spent medium inhibited C. bombi growth via a reduction in pH that was both necessary and sufficient for inhibition. Inhibition of all parasite strains occurred within the pH range previously observed in honey bee guts, though sensitivity to acidity varied among parasite strains. Spent medium was slightly more potent than HCl, D-, and L-lactic acids for a given pH, suggesting that other metabolites also contribute to inhibitory effects. Our results implicate symbiont-mediated reduction in gut pH as a key determinant of trypanosomatid infection in bees. Future investigation into in vivo effects of gut microbial composition on pH and infection intensity would help determine the relevance of these findings for bees threatened by trypanosomatids.\n\nImportancePollinators such as honey and bumble bees provide services to plants in agricultural and wild ecosystems, but both wild and managed bees are threatened by infection-related declines. The symbiotic gut microbiota of bees provides a naturally occurring defense against infection. For example, the bumble bee microbiota reduces infection with trypanosomatid parasites, but how inhibition occurs remains unknown. We show that the acidic spent medium from a common bumble bee gut symbiont, Lactobacillus bombicola, inhibits in vitro growth of the trypanosomatid gut parasite, Crithidia bombi. The acidity of the spent medium was both necessary and sufficient for parasite inhibition. Inhibitory pH values were within the range documented in honey bee guts, suggesting that pH-mediated parasite inhibition is plausible in live bees. Results suggest that production of acids by sugar-fermenting symbionts confers pH-mediated resistance to infection in bees, whereas depletion of core microbiota could result in low-acid conditions that favor parasite growth.

ecology↗