Bactericidal activity of avian complement: a contribution to understand avian-host tropism of Lyme borreliae

Abstract

Complement has been considered as an important factor impacting the host–pathogen association of spirochetes belonging to the Borrelia burgdorferi sensu lato complex, and may play a role in the spirochete’s ecology. Birds are known to be important hosts for ticks and in the maintenance of borreliae. Recent field surveys and laboratory transmission studies indicated that certain avian species act as reservoir hosts for different Borrelia species. Nevertheless, our current understanding of the molecular mechanisms determining host tropism of Borrelia is still in its fledgling stage. Concerning the role of complement in avian-host tropism, only a few bird species and Borrelia species have been analysed so far. Here, we performed in vitro serum bactericidal assays with serum samples collected from four bird species including the European robin Erithacus rubecula, the great tit Parus major, the Eurasian blackbird Turdus merula, and the racing pigeon Columba livia, as well as four Borrelia species (B. afzelii, B. garinii, B. valaisiana, and B. burgdorferi sensu stricto). From July to September 2019, juvenile wild birds were caught using mist nets in Portugal. Racing pigeons were sampled in a loft in October 2019. Independent of the bird species analysed, all Borrelia species displayed an intermediate serum-resistant or serum-resistant phenotype except for B. afzelii challenged with serum from blackbirds. This genospecies was efficiently killed by avian complement, suggesting that blackbirds served as dead-end hosts for B. afzelii. In summary, these findings suggest that complement contributes in the avian–spirochete–tick infection cycle and in Borrelia-host tropism.

The Infection Rate of Bird-Feeding Ixodes ricinus Ticks with Borrelia garinii and B. valaisiana Varies with Host Haemosporidian Infection Status

“…Another assumption of the immune polarization hypothesis is that avian hosts should be able to mount immune responses to Borrelia spirochetes associated with such hosts. Indeed, contrary to earlier expectations based on the absence of clinical signs of Borrelia infection in avian hosts [ 69 ], the ability to mount host defenses against Borrelia spirochetes was confirmed for the key avian reservoir of bird-associated Borrelia spirochetes, the Eurasian blackbird [ 10 , 70 , 71 ].…”

“…Importantly, the lower rates of Borrelia -infected bird-feeding ticks in haemosporidian-positive birds may not only be due to reduced host-to-tick spirochete transmission, but also due to spirochete killing within bird-feeding ticks by ingested avian anti- Borrelia antibodies. In fact, such antibodies have recently been detected in the sera of Eurasian blackbirds [ 71 ], though an avian serum complement is thought to play the key role in Borrelia killing in ticks [ 71 , 79 ]. Further experimental research is needed to confirm our results and address the complexity of avian immunological mechanisms responsible for Borrelia suppression in hosts but also in feeding ticks.…”

The evolving story of Borrelia burgdorferi sensu lato transmission in Europe

“…Noteworthy, species of the B. burgdorferi s.l. complex largely vary in their ability to survive in the presence of complement obtained from different vertebrates (Kurtenbach et al 1998 , 2002a ; Kraiczy 2016a , b ; Tufts et al 2019 ; Lin et al 2020 ; Sürth et al 2021 ). Apparently, the ability of a Borrelia species to resist complement-mediated killing by a particular host’s serum almost always correlated with the capability of this specific Borrelia species to successfully infect and survive in that host and utilize it as reservoir (Kurtenbach et al 2002a ; Lin et al 2020 ).…”

Unprecedented genetic variability of PFam54 paralogs among Eurasian Lyme borreliosis‐causing spirochetes

“…Differences in susceptibility to complement in vitro therefore could be one of the possibilities to determine infection capacity of B. garinii isolates. Recent data has demonstrated variation in the susceptibility of B. garinii to avian complement from different terrestrial European bird species (Sürth et al., 2021 ), suggesting that host adaptation toward specific bird species could exist.…”

“…If true, one could hypothesize that the variability in architecture types within B. garinii isolates could correspond to the capacity to infect specific bird species. Borrelia garinii selectively binds complement regulator Factor H of avian origin to protect itself from complement-mediated killing and, thus facilitate infection of avian hosts (Hart et al, 2018(Hart et al, , 2021Sürth et al, 2021). Differences in susceptibility to complement in vitro therefore could be one of the possibilities to determine infection capacity of B. garinii isolates.…”