Wolbachiagenomics reveals a potential for a nutrition-based symbiosis in blood-sucking Triatomine bugs

SummaryThe 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 bugRhodnius prolixus, one of the main vectors of the Chagas disease in humans, is known to maintain a nutritional symbiosis with the gut symbiontsRhodococcus rhodnii.In this study, we show thatWolbachiasymbionts are also widely distributed in theRhodniusgenus. We have screened a large set ofRhodniusblood-sucking bugs samples belonging to 17 different species and to the three phylogenetic groups,prolixus, pallescensandpictipes. We assembled 13 genomes ofWolbachiainfecting eightRhodniusspecies fromprolixusandpictipesgroups. We demonstrate that theseWolbachiabelong to supergroup F and are closely related toWolbachiainfecting the bedbugCimex lectularius(wCle). Although bedbugs and triatomines are very distantly related hemipteran bugs, the genomes of their respectiveWolbachiawere highly similar, suggesting recent horizontal host switches. We also show thatRhodnius Wolbachiagenomes infecting theprolixusgroup encode intact biotin operon, the hallmark of nutritional symbiosis in bedbugs. This operon is lacking from all the otherWolbachiainfectingR. pictipes. Finally, host genome analyses provide evidence of massiveWolbachia-to-Rhodniusgene transfers in almost samples, providing footprints of past infections that support a widespread and probably ancient symbiotic association betweenWolbachiaand triatomine bugs.Our results suggest that bothWolbachiaandR. rhodniigut symbionts and theirRhodniushost maintain a highly prevalent symbiotic relationship, in which the vertically-inheritedWolbachiahas the metabolic potantial to ensure or complement, the nutritional mutualism provided by the gut symbionts. Specific loss of the biotin operon in some symbiont genomes suggests that the boundaries between obligatory mutualism, facultative mutualism and parasitism inWolbachiaare transient and fluid, supporting a dynamic process of transition and reversion from one state to another.