The microbiome of blood-sucking arthropods can shape their competence to acquire and maintain infections with vector-borne pathogens. We used a controlled study to investigate the interactions between
Borrelia afzelii
, which causes Lyme disease in Europe, and the bacterial microbiome of
Ixodes ricinus
, its primary tick vector. We applied a surface sterilization treatment to
I. ricinus
eggs to produce dysbiosed tick larvae that had a much lower bacterial abundance and a changed bacterial microbiome compared to the control larvae. Dysbiosed and control larvae were fed on
B. afzelii
-infected mice and uninfected control mice and the engorged larvae were left to molt into nymphs, which were tested for
B. afzelii
infection and their bacterial microbiome by
16S rRNA
amplicon sequencing. Surprisingly, larval dysbiosis had no effect on the vector competence of
I. ricinus
for
B. afzelii
, as the nymphal infection prevalence and the nymphal spirochete load were the same between the dysbiosed group and the control group. The strong effect of egg surface sterilization on the tick bacterial microbiome largely disappeared once the larvae molted into nymphs. The most important determinant of the bacterial microbiome of
I. ricinus
nymphs was the
B. afzelii
infection status of the mouse on which the nymphs had fed as larvae. Nymphs that had taken their larval blood meal from an infected mouse had a less abundant but more diverse bacterial microbiome compared to control nymphs. Our study demonstrates that vector-borne infections in the vertebrate host shape the microbiome of the arthropod vector.
IMPORTANCE
Many blood-sucking arthropods transmit pathogens that cause infectious disease. For example,
Ixodes ricinus
ticks transmit the bacterium
Borrelia afzelii
, which causes Lyme disease in humans. Ticks also have a microbiome, which can influence their ability to acquire and transmit tick-borne pathogens like
B. afzelii
. We sterilized
I. ricinus
eggs with bleach, and the tick larvae that hatched from these eggs had a dramatically reduced and changed bacterial microbiome compared to control larvae. These larvae were fed on
B. afzelii
-infected mice and the resultant nymphs were tested for
B. afzelii
and their bacterial microbiome. We found that our manipulation of the bacterial microbiome had no effect on the ability of the tick larvae to acquire and maintain populations of
B. afzelii
. In contrast, we found that
B. afzelii
infection had dramatic effects on the bacterial microbiome of
I. ricinus
nymphs. Our study demonstrates that infections in the vertebrate host can shape the tick microbiome.
The abundance of the Lyme disease pathogen Borrelia afzelii declines over time in the tick vector Ixodes ricinus