Borreliainfection in rodent host has dramatic effects on the microbiome of ticks

Abstract

Background: Vector-borne diseases remain major causes of human morbidity and mortality. It is increasingly recognized that the community of microbes inhabiting arthropods can strongly affect their vector competence, but the role of the tick microbiome in Borrelia transmission - the cause of Lyme disease - remains unclear. Results: Here, we use a large-scale experiment to clarify the reciprocal interactions between Borrelia afzelii and the microbiome of Ixodes ricinus, its primary vector. In contrast to other reports, we find that depletion of the bacterial microbiome in larval ticks has no effect on their subsequent acquisition of B. afzelii during blood feeding on infected mice. Rather, exposure to B. afzelii-infected hosts drives pervasive changes to the tick microbiome, decreasing overall bacterial abundance, shifting bacterial community composition, and increasing bacterial diversity. These effects appear to be independent of the acquisition of B. afzelii by ticks, suggesting they are mediated by physiological or immunological aspects of B. afzelii infection in the rodent host. Conclusions: Manipulation of the microbiome of I. ricinus larvae had no effect on their ability to acquire B. afzelii. In contrast, B. afzelii infection in the mouse had dramatic effects on the composition of the gut microbiome in I. ricinus nymphs. Our study demonstrates that vector-borne infections in the vertebrate host shape the microbiome of the arthropod vector.

Ecological and evolutionary perspectives on tick-borne pathogen co-infections

“…The contributions of the tick microbiota to tick-pathogen interactions are highly relevant for vectorial capacity, with the relationship between microbiota and pathogens being bidirectional ( Wu-Chuang et al., 2021a ). For example, tick colonization by A. phagocytophilum or B. afzelii has been reported to modulate the tick microbiome ( Abraham et al, 2017 ; Hamilton et al, 2021 ). Ticks bred in a sterile environment without microbiota have altered gut integrity which reduced the ability of B. burgdorferi to colonize this niche ( Narasimhan et al., 2014 ).…”