Microbial Thermal Response Strategies Impact Environmental Fitness of Horizontally Transmitted Symbiont Strains

Microbial symbionts in insect-microbe mutualisms are critical for host survival and fitness. However, symbioses are sensitive to external stressors. Understanding how a warming climate will impact these associations, therefore, is critical. Previous work on horizontally transmitted bug- Caballeronia bacterial symbionts has shown that different symbiont strains confer variable host outcomes under thermal stress, suggesting that environmental symbiont acquisition could be advantageous under shifting temperature regimes. However, it is unknown what specific bacterial thermal responses could impact microbial survival in the environment, which would be key to host acquisition. We evaluated in vitro thermal response mechanisms of heat-vulnerable and heat-resistant strains of Caballeronia using microbial transcripts, to identify pathways that may impact the symbionts’ respective thermal optima. We found that a heat-resistant strain prioritizes induction of thermally stable outer membrane components, motility structures, and molecular chaperones, allowing it to increase growth through induction of central metabolism and protein synthesis. Meanwhile, a heat-vulnerable strain arrests growth, favoring induction of genes related to alternative metabolism and biofilm formation. These results are indicative of variable bacterial thermal response strategies for elevated temperature survival. Ultimately these responses may alter which symbionts are more available to insect hosts as temperatures continue to rise. Importance Many eukaryotes host beneficial microbes that synthesize essential nutrients or can break down harmful compounds. While important, if these microbes are acquired from the local environment ( i.e., soils or plant surfaces), external stressors can destabilize the associations by impacting microbial growth, limiting the pool of available microbes. Using the bug- Caballeronia model system, we analyzed the in vitro thermal stress response of two Caballeronia symbiont strains that have different thermal optima. We found that stress responses involving increased motility, thermally stable membrane synthesis, and molecular chaperones may increase growth under thermal stress in symbionts. These results indicate that different thermal stress coping strategies may be favored in bug- Caballeronia system under increasing global temperatures. More broadly, these results provide insight into how microbial stress responses could shape adaptation of symbioses to a warming climate.