Bacterial microbiota composition of Ixodes ricinus ticks: the role of environmental variation, tick characteristics and microbial interactions

Abstract

The factors shaping microbial communities within organisms are still poorly understood. Besides ecological factors and host characteristics, direct interactions among microbes may shape the occurrence of microbes and the structure of communities. In the past it has been difficult to disentangle if patterns of microbial co-occurrence are due to facilitation or competition effects, or shaped by shared ecological preferences (i.e., environmental filtering). Here we use a joint species distribution model to characterize the bacterial microbiota composition of an important human disease vector, the sheep tick Ixodes ricinus, along ecological gradients in the Swiss Alps, and to test for facilitation or competition effects among human pathogens and tick endosymbionts. We identify a number of ecological variables that significantly predicted the diversity of tick microbial community and the occurrence of specific tick endosymbionts and human pathogens. However, ecological associations were generally microbe-specific rather than universal. We also found evidence for significant microbe interactions, in particular widespread facilitation among pathogens, which promotes pathogen co-infection within ticks, as well as competition between the tick endosymbiont Spiroplasma and a number of human pathogens. These findings highlight that direct interactions among microbes can affect the vector competence of ticks and thereby tick-borne disease dynamics.