Complex Population Structure of Lyme Borreliosis Group Spirochete Borrelia garinii in Subarctic Eurasia

Abstract

Borrelia garinii, a causative agent of Lyme borreliosis in Europe and Asia, is naturally maintained in marine and terrestrial enzootic cycles, which primarily involve birds, including seabirds and migratory passerines. These bird groups associate with, correspondingly, Ixodes uriae and Ixodes ricinus ticks, of which the latter species may bite and transmit the infection to humans. Studies of the overlap between these two natural cycles of B. garinii have been limited, in part due to the absence of representative collections of this spirochete's samples, as well as of the lack of reliable measure of the genetic heterogeneity of its strains. As a prerequisite for understanding the epidemiological correlates of the complex maintenance of B. garinii, the present study sought to assess the diversity and phylogenetic relationships of this species' strains from its natural hosts and patients with Lyme borreliosis from subarctic Eurasia. We used sequence typing of the partial rrs-rrl intergenic spacer (IGS) of archived and prospective samples of B. garinii from I. uriae ticks collected predominantly on Commander Islands in North Pacific, as well as on the islands in northern Sweden and arctic Norway. We also typed B. garinii samples from patients with Lyme borreliosis and I. ricinus ticks infesting migratory birds in southern Sweden, or found questing in selected sites on the islands in the Baltic Sea and Lithuania. Fifty-two (68%) of 77 B. garinii samples representing wide geographical range and associated with I. ricinus and infection of humans contributed 12 (60%) of total 20 identified IGS variants. In contrast, the remaining 25 (32%) samples recovered from I. uriae ticks from a few islands accounted for as many as 10 (50%) IGS types, suggesting greater local diversity of B. garinii maintained by seabirds and their ticks. Two IGS variants of the spirochete in common for both tick species were found in I. ricinus larvae from migratory birds, an indication that B. garinii strains are exchanged between different ecological niches. Notably, B. garinii variants associated with I. uriae ticks were found in each of the six clusters, representing two phylogenetic lineages of this species identified among the studied samples. Our findings suggest that B. garinii in subarctic Eurasia comprises two partially overlapping populations with different levels of genetic heterogeneity, presumably, due to distinctive selective pressures on the spirochete in its marine and terrestrial enzootic cycles.

Seabirds and the Circulation of Lyme Borreliosis Bacteria in the North Pacific

“…Anti-Borrelia Ab prevalence in birds was highest in the Commander Islands; this is consistent with a high spirochete prevalence reported in I. uriae ticks collected from the vegetation on these islands (Comstedt et al 2009). The global and local prevalence of anti-Borrelia antibodies we observed in the North Pacific is, nevertheless, much lower than that observed in the North Atlantic for black-legged kittiwakes (global prevalence of 18.6%) and common murres (global prevalence of 77.1%) (Staszewski et al 2008).…”

“…Seabirds may be particularly important in the global circulation of LB spirochetes (Olsen et al 1995); these birds are widely distributed and breed in large groups that often include a diverse range of interacting species (Schreiber and Burger 2001). The tick Ixodes uriae parasitises several of these seabird species in polar areas (Choe andKim 1987, Dietrich et al 2011) and has been shown to be infected with Bbsl in colonies of both Hemispheres (Olsen et al 1993, 1995, Gylfe et al 1999, Smith et al 2006, Duneau et al 2008, Comstedt et al 2009). However, host-dependent population structure has been found for I. uriae ticks (McCoy et al , 2005a and different local tick-seabird species combinations show variation in Bbsl infection prevalence and intensity (Gó mezDíaz et al 2010), which may influence the circulation of the pathogens within the marine system (Duneau et al 2008, McCoy 2008.…”

“…In the North Atlantic, significant spatial and interspecific variability in exposure to spirochetes has been reported (Staszewski et al 2008), and the anti-Borrelia Ab levels of individual birds was shown to be highly stable between years in one wide-spread species, the black-legged kittiwake Rissa tridactyla (Staszewski et al 2007). In the North Pacific, the presence of Borrelia in ticks has been reported (Olsen et al 1995, Comstedt et al 2009, but little is known about variability in Bbsl exposure within and among seabird communities. North Pacific seabird communities are composed of a rich array of colonial species, and share with the North Atlantic communities both the tick vector I. uriae and some seabird host species (black-legged kittiwake, common murre Uria aalge, and thick-billed murre Uria lomvia).…”

Zoonotic Peculiarities of Borrelia burgdorferi s.l.: Vectors Competence and Vertebrate Host Specificity

“…The involvement of seabirds and I. uriae (in the marine environment) in the transport of infected Borrelia garinii between the northern and the southern hemispheres was described. (Comstedt et al, 2009;Gern et al, 1998;Kurtenbach et al, 2006). In this context, it is interesting to mention that in a laboratory study, reactivation of latent Borrelia-infection could be induced in passerines experimentally submitted to stressful conditions simulating migration.…”

Evidence for Borrelia bavariensis Infections of Ixodes uriae within Seabird Colonies of the North Atlantic Ocean

“…The species was eventually identified as B. garinii, which has subsequently been found in seabird colonies throughout Europe and Antarctica, as well as in two colonies in North America (16)(17)(18)(19)(20). Since this discovery, B. burgdorferi sensu stricto and B. lusitaniae have also been reported in a few seabird colonies in the eastern North Atlantic (17).…”