Complex roles for a conserved two-component system in a honey bee symbiosis

Abstract

Elucidating how microbes associate with their hosts and respond to different environments is fundamental to our understanding of symbiosis. Here, we investigate the molecular and genetic mechanisms enabling the honey bee symbiont Bombella apis to colonize and persist in harsh honey bee microenvironments, like royal jelly and the larval gut. By using evolved B. apis strains, we demonstrate that the broadly conserved two-component system (TCS) ChvGI is integral for the bacterium’s ability to withstand royal jelly and the larval gut. Furthermore, we show that in B. apis ChvGI also regulates critical bacterial behaviors such as motility, flagellar production, and biofilm formation. In other Alphaproteobacteria, ChvGI is known as a master regulator that mediates the bacterial responses to stressors and is also found to be involved in symbiosis, often through the production of EPS and biofilm formation. Our work underscores the broader significance of ChvGI as an important TCS in Alphaproteobacteria that regulates bacterial behavior in response to different types of stressors and uncovers a genetic mechanism that allows an important honey bee symbiont to survive in diverse host environments. Importance Bombella apis is an alphaproteobacterial honey bee symbiont that provides protection against Aspergillus species, fungal pathogens of honey bees, and acts as a larval dietary supplement in nutrient poor conditions. This organism is compelling for both its ability to grow in the presence of antimicrobial royal jelly and in its ability to thrive in various hive and insect-associated environments, including the developing larva. Here, we have implicated the two-component system ChvGI as important for the survival of B. apis in royal jelly and for regulating bacterial behaviors like biofilm formation, motility, and host association. ChvGI is a broadly conserved TCS in Alphaproteobacteria that is widely known to play an important role in mutualistic and pathogenic symbioses, as well as regulating multiple bacterial behaviors. We hypothesize that ChvGI may aid in transition of B. apis through the different host environments it occupies.