How do host age and nutrition affect density regulation of obligate versus facultative bacterial symbionts? Insights from the tsetse fly.

Abstract

Host-symbiont relationships can vary tremendously in the extent to which hosts depend on and control their symbionts. Obligate symbionts that provide micronutrients to their host are often compartmentalised to specialised host organs and depend on their hosts for survival, whereas facultative symbionts retain the ability to survive outside of their hosts. Few studies compare the extent to which a host controls and adjusts the density of obligate and facultative symbionts directly. We used tsetse as a model for teasing apart the relationships between a host (Glossina morsitans morsitans) and obligate (Wigglesworthia glossinidia) and facultative (Sodalis glossinidius) symbionts. We hypothesised that tsetse actively regulate the density of Wigglesworthia according to the host's requirements, depending on their current nutritional state and developmental age. In contrast, we postulated that Sodalis retains some independence from host control and that the growth of this symbiont is dependent on the conditions of the immediate environment, such as nutrient availability. Using qPCR, we examined how symbiont densities change across host age and the hunger cycle. Additionally, we investigated how host nutrition influences symbiont density, by comparing tsetse that were fed nutrient-poor or vitamin enriched diets. We found that the density of Wigglesworthia was not influenced by the nutritional status of the host but reflected long-term host nutritional needs. In contrast, the density of facultative Sodalis depended on the nutrient availability. We propose that tsetse tightly regulate Wigglesworthia but exert only partial control over Sodalis growth due to the relatively recent transition of this symbiont to host-associated living.