Abstract
The nutritional symbiosis promoted by bacteria is a key determinant for adaptation and evolution of many insect lineages. A complex form of nutritional mutualism that arose in blood-sucking insects critically depends on diverse bacterial symbionts that supplement the diet of their nutrient-poor hosts with B vitamins. For instance, the triatomine bug Rhodnius prolixus, one of the main vectors of the Chagas disease, is known to maintain a nutritional symbiosis with the gut symbionts Rhodococcus rhodnii.
In this study, we showed that Wolbachia symbionts were also widely distributed in the Rhodnius genus. We have screened a large set of Rhodnius blood-sucking bugs samples belonging to 17 different species and to the three phylogenetic groups, prolixus, pallescens and pictipes. We assembled 13 complete, or nearly complete, genomes of Wolbachia infecting eight Rhodnius species (wRho) from prolixus and pictipes groups. We demonstrated that these Wolbachia belonged to supergroup F and were closely related to Wolbachia infecting the bedbug Cimex lectularius (wCle). Although bedbugs and triatomines are very distantly related hemipteran bugs, the genomes of their respective Wolbachia were highly similar and highly syntenic, suggesting recent horizontal host switches. We also showed that wRho genomes infecting the prolixus group encode intact biotin operon, the hallmark of nutritional symbiosis in bedbugs. This operon was lacking from all the wRho infecting R. pictipes. Finally, host genomes analyses provided evidence of massive Wolbachia-to-Rhodnius gene transfers in almost samples, providing footprints of past infections that support a widespread and probably ancient symbiotic association between Wolbachia and triatomine bugs.
Our results suggest that both Wolbachia and R. rhodnii gut symbionts and their Rhodnius host maintain a highly prevalent tripartite symbiotic relationship, in which the vertically-inherited Wolbachia could compensate for the transitory absence of the horizontally-inherited nutritional gut symbionts. We speculate that the symbiotic relationship between Wolbachia and Rhodnius could subsequently returned to a parasitic relationship in some species harbouring a specific loss of the biotin operon. This suggests that the boundaries between obligatory mutualism, facultative mutualism and parasitism in Wolbachia are transient and fluid, supporting a dynamic process of transition and reversion from one state to another.
Competing Interest Statement
The authors have declared no competing interest.