The pathogen Borrelia burgdorferi sensu lato (s.l.) influences the desiccation resistance of Ixodes ricinus nymphs potentially enhancing its vector role

Abstract Borrelia burgdorferi sensu lato (s.l.), the causative agent of Lyme borreliosis, has been associated with increased mobility, questing height and survival under desiccating conditions in its tick vector Ixodes ricinus . However, the underlying physiological mechanisms remain poorly understood. Here, we tested whether B. burgdorferi s.l. infection enhances desiccation stress tolerance by modifying the tick’s cuticular lipid composition. In a behavioural bioassay, we showed that infected ticks were significantly more likely to reach higher positions than uninfected ones (64.3% vs. 37.4%; p-value = 0.012). These elevated positions expose nymphs to harsher desiccating conditions, but survival experiments at different relative humidity levels (100%, 80%, and 53% relative humidity) revealed that infected ticks survived longer under desiccation stress. To investigate the basis of enhanced survival under desiccating conditions, we investigated the lipid layer on the ticks’ cuticle through solvent-washing experiments that confirmed the importance of cuticle integrity for desiccation resistance. Gas chromatography-mass spectrometry analysis revealed that infected ticks had a higher proportion of saturated fatty acids and a lower proportion of unsaturated ones compared to Borrelia free ticks. This shift in lipid composition is consistent with improved cuticle waterproofing and reduced water loss, which may explain the observed tolerance. Our results indicate that infection with B. burgdorferi s.l. is associated with a distinct cuticular lipid profile in I. ricinus , which may allow infected ticks to quest higher and longer under challenging environmental conditions. These behavioural and physiological modifications appear beneficial for both partners.