The genome of Borrelia burgdorferi encodes a large number of lipoproteins,
many of which are expressed only at certain stages of the spirochete's life
cycle. In the current study we describe the B, burgdorferi population stru
cture with respect to the production of two lipoproteins [outer surface pro
tein A (OspA) and outer surface protein C (OspC)] during transmission from
the tick vector to the mammalian host. Before the blood meal, the bacteria
in the tick were a homogeneous population that mainly produced OspA only, D
uring the blood meal, the population became more heterogeneous; many bacter
ia produced both OspA and OspC whereas others produced only a single Osp an
d a few produced neither Osp. From the heterogeneous spirochetal population
in the gut, a subset depleted of OspA entered the salivary glands and stab
ly infected the host at time points >53 hr into the blood meal. We also exa
mined genetic heterogeneity at the B. burgdorferi vlsE locus before and dur
ing the blood meal. In unfed ticks, the vlsE locus was stable and one predo
minant and two minor alleles were detected, During the blood meal, multiple
vlsE alleles were observed in the tick. Tick feeding may increase recombin
ation at the vlsE locus or selectively amplify rare vlsE alleles present in
unfed ticks, On the basis of our data we propose a model, which is differe
nt from the established model for B. burgdorferi transmission, Implicit in
our model is the concept that tick transmission converts a homogeneous spir
ochete population into a heterogeneous population that is poised to infect
the mammalian host.