High temperatures augment inhibition of parasites by a honey bee gut symbiont

Abstract

ABSTRACTTemperature affects growth, metabolism, and interspecific interactions in microbial communities. Within animal hosts, gut bacterial symbionts can provide resistance to parasitic infections. Infection can also be shaped by host body temperature. However, the effects of temperature on the antiparasitic activities of gut symbionts have seldom been explored. TheLactobacillus-rich gut microbiota of facultatively endothermic honey bees is subject to seasonal and ontogenetic changes in host temperature that could alter the effects of symbionts against parasites. We used cell cultures of aLactobacillussymbiont and an important trypanosomatid gut parasite of honey bees to test the potential for temperature to shape parasite-symbiont interactions.We found that symbionts showed greater heat tolerance than parasites and chemically inhibited parasite growth via production of acids. Acceleration of symbiont growth and acid production at high temperatures resulted in progressively stronger antiparasitic effects across a temperature range typical of bee colonies. Consequently, the presence of symbionts reduced both peak growth rate and heat tolerance of parasites. Results suggest that the endothermic behavior of honey bees could potentiate the effectiveness of gut symbionts that limit parasites’ ability to withstand high temperature, implicating thermoregulation as a reinforcer of core symbioses and possibly microbiome-mediated antiparasitic defense.IMPORTANCETwo factors that shape the resistance of animals to infection are body temperature and gut microbiota. However, temperature can also alter interactions among microbes, raising the question of whether and how temperature changes the antiparasitic effects of gut microbiota. Honey bees are agriculturally important hosts of diverse parasites and infection-mitigating gut microbes. They can also socially regulate their body temperatures to an extent unusual for an insect. We show that high temperatures found in honey bee colonies augment the ability of a gut bacterial symbiont to inhibit growth of a common bee parasite and reduce the parasite’s ability to grow at high temperatures. This suggests that fluctuations in colony and body temperatures across life stages and seasons could alter the protective value of bees’ gut microbiota against parasites, and that temperature-driven changes in gut microbiota could be an underappreciated mechanism by which temperature— including endothermy and fever— alters animal infection.