Temperature-mediated inhibition of a bumblebee parasite by an intestinal symbiont

Abstract

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 bumblebees, 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. We found that a temperature increase over the range measured in bumblebee colonies would favour 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.

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

“…Although the reduction in C. bombi infection at high temperature corresponded with higher populations of Lactobacillaceae (Fig. ), which produced parasite‐inhibiting organic acids in vitro (Palmer‐Young et al ., ), our findings indicate that an abundance of acid‐producing bacteria does not necessarily confer resistance to parasites. In models controlling for temperature, there was no significant correlation between Lactobacillaceae abundance and C. bombi infection (Fig.…”

“…In agreement with predictions from in vitro experiments and temperature‐dependent changes in performance of parasites, bees, and bacterial symbionts, we found reductions in trypanosomatid infection intensity as temperature increased over the typical range of bee body temperatures (Heinrich, ). Parasites in cell culture had optimal growth temperatures of 27–32°C (Palmer‐Young et al ., ). Hence, reductions in infection above 32°C could be due to direct inhibition of growth, but reductions between 21 and 32°C likely reflect relative, rather than absolute, disadvantage of parasites in comparison to the bee immune system and gut bacterial symbionts.…”

“…The core bee gut bacterial symbionts also have relatively high temperatures of peak performance (35–37°C (Engel et al ., )). In the case of L. bombicola , growth and production of C. bombi ‐inhibiting acids increased exponentially across the 21–37°C range (Palmer‐Young et al ., b). Thus, reductions in infection with increasing temperature could reflect increases in metabolic rates of acid‐producing, parasite‐inhibiting bacteria.…”

“…Populations of Lactobacillaceae were the most responsive to temperature, with mean abundances increasing twofold between the lowest and highest temperatures. Experiments in vitro with the widespread symbiont L. bombicola – the most abundant member of this family among our samples – indicate that growth rate of this species increases throughout the experimental temperature range (Palmer‐Young et al ., b). Whether the Lactobacillaceae are more thermophilic than other major symbionts, or their maximum population size is simply less constrained by host surface area than those of the biofilm‐forming Neisseriaceae and Orbaceae (Martinson et al ., ), remains to be determined.…”

“…Because bumble and honey bee muscle performance (Gilmour and Ellington, ; Harrison and Fewell, ), bumble bee respiration rate (Kammer and Heinrich, ) and bacterial gut symbiont performance all have higher temperatures of peak performance than does the parasite C . bombi (Palmer‐Young et al ., ), we predicted that infection would decrease across the temperature range previously recorded in wild bees (Heinrich, ). Based on metabolic theory and the concept of thermal mismatches (Cohen et al ., ) – which predict that high temperatures improve performance of the host immune system and antiparasitic bacterial symbionts relative to performance of parasites – we also predicted that the temperature of peak infection in bees would be lower than the temperature of peak growth rate for parasite cell cultures.…”