Tick-Bacteria Mutualism Depends on B Vitamin Synthesis Pathways

Mutualistic interactions with microbes have facilitated the radiation of major eukaryotic lineages [1, 2]. Microbes can notably provide biochemical abilities, allowing eukaryotes to adapt to novel habitats or to specialize on particular feeding niches [2–4]. To investigate the importance of mutualisms for the exclusive blood feeding habits of ticks, we focused on a bacterial genus of medical interest, Francisella, which is known to include both virulent intracellular pathogens of vertebrates [5, 6] and maternally inherited symbionts of ticks [7–9]. Through a series of physiological experiments, we identified a Francisella type, F-Om, as an obligate nutritional mutualist in the life cycle of the African soft tick Ornithodoros moubata. Francisella F-Om mutualism synthesizes B vitamins that are deficient in the blood meal of ticks. Indeed, experimental elimination of Francisella F-Om resulted in alteration of tick life history traits and physical abnormalities, deficiencies which were fully restored with an oral supplement of B vitamins. We also show that Francisella F-Om is maternally transmitted to all maturing tick oocytes, suggesting that this heritable symbiont is an essential adaptive element in the life cycle of O. moubata. The Francisella F-Om genome further revealed a recent origin from a Francisella pathogenic life style, as observed in other Francisella symbionts [6, 7, 10]. Though half of its protein-coding sequences are now pseudogenized or lost, Francisella F-Om has kept several B vitamin synthesis pathways intact, confirming the importance of these genes in evolution of its nutritional mutualism with ticks. •Ticks are dependent on mutualistic interactions with intracellular bacteria•Elimination of a Francisella symbiont hampers ticks’ growth and molting to adulthood•These deficiencies were rescued by oral supplementation of B vitamins•B vitamin supplementation by symbionts is critical for ticks’ blood feeding lifestyle Ticks rely on vertebrate blood as their only food, and this diet is limited in B vitamins. Duron et al. show that use of this unbalanced diet is possible because an intracellular bacterial symbiont supplies missing nutrients; this nutritional symbiont is essential for ticks’ growth and survival to adulthood.