Rickettsia helvetica infection is associated with microbiome modulation in Ixodes ricinus collected from humans in Serbia
Résumé
Rickettsia helvetica is an emerging pathogen in various European countries, and it is one of the agents causing spotted fever diseases. This tick-borne pathogen replicates in the tick organs, but its potential interactions with the vector microbiota are poorly understood. The vector microbiome plays a pivotal role in tick-pathogen interactions, and some microbiota member facilitates or competes with tick-borne pathogen colonization in tick tissues. Manipulations of the tick microbiome have led to reduced pathogen colonization in the tick vector. However, translating these findings into disease control applications requires a thorough characterization of vector microbiota response to different pathogen infections. In this study, we analyzed and compared the microbiota of Ixodes ricinus ticks collected on humans in Serbia. Ticks were either positive for R. helvetica, or negative (referred hereafter as ‘pathogen-free’) for 34 major tick-borne pathogens. Richness and evenness in samples of the two datasets were compared using alpha-diversity indexes. Microbial community structure and interaction patterns in response to pathogen infection were characterized using co-occurrence networks. The Network Construction and comparison for Microbiome (Net CoMi) method was used to compare the connectivity of R. helvetica-infected and ‘pathogen-free’ networks. The hierarchical organization, based on keystone taxa, and the functional profiles of R. helvetica-positive and ‘pathogen-free’ samples were also compared. Our results show that R. helvetica infection has a significant impact on tick microbiota. The presence of the pathogen was associated withdecreased richness and variability. The networks comparison demonstrated a significant change in the hierarchical organization of I. ricinus microbiota and some taxa were identified as positively associated with R. helvetica. The reconstruction of microbial metabolic pathways shows that the presence of R. helvetica might have major impact on the metabolic functions of the tick microbiome. The characterization of the tick microbiome in ticks collected from humans can reveal novel targets to prevent tick-borne pathogen infection, as the tick microbiome has a critical role on vector competence. This study highlighted a potential target for an anti-microbiota vaccine. These results can inform novel interventions for the prevention of R. helvetica infection in humans.