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. 2020 May 21;17(10):3607.
doi: 10.3390/ijerph17103607.

Local Population Structure and Seasonal Variability of Borrelia garinii Genotypes in Ixodes ricinus Ticks, Slovakia

Zuzana Mtierová  1 , Markéta Derdáková  1 , Michal Chvostáč  1 , Yuliya M Didyk  1   2 , Barbara Mangová  1 , Veronika Rusňáková Tarageľová  1 , Diana Selyemová  1 , Alžbeta Šujanová  1 , Radovan Václav  1
Affiliations

Local Population Structure and Seasonal Variability of Borrelia garinii Genotypes in Ixodes ricinus Ticks, Slovakia

Zuzana Mtierová et al. Int J Environ Res Public Health. .

Abstract

Lyme disease (LD) is the most common tick-borne human disease in Europe, and Borrelia garinii, which is associated with avian reservoirs, is one of the most genetically diverse and widespread human pathogenic genospecies from the B. burgdorferi sensu lato (s.l.) complex. The clinical manifestations of LD are known to vary between regions and depend on the genetic strain even within Borrelia genospecies. It is thus of importance to explore the genetic diversity of such pathogenic borreliae for the wide range of host and ecological contexts. In this study, multilocus sequence typing (MLST) was employed to investigate the local population structure of B. garinii in Ixodes ricinus ticks. The study took place in a natural wetland in Slovakia, temporally encompassing spring and autumn bird migration periods as well as the breeding period of resident birds. In total, we examined 369 and 255 ticks collected from 78 birds and local vegetation, respectively. B. burgdorferi s.l. was detected in 43.4% (160/369) of ticks recovered from birds and in 26.3% (67/255) of questing ticks, respectively. Considering the ticks from bird hosts, the highest prevalence was found for single infections with B. garinii (22.5%). Infection intensity of B. garinii in bird-feeding ticks was significantly higher than that in questing ticks. We identified ten B. garinii sequence types (STs) occurring exclusively in bird-feeding ticks, two STs occurring exclusively in questing ticks, and one ST (ST 244) occurring in both ticks from birds and questing ticks. Four B. garinii STs were detected for the first time herein. With the exception of ST 93, we detected different STs in spring and summer for bird-feeding ticks. Our results are consistent with previous studies of the low geographic structuring of B. garinii genotypes. However, our study reveals some consistency in local ST occurrence and a geographic signal for one of the clonal complexes.

Keywords: Lyme disease; Turdus merula; clonal complexes; ecological niche; geographic structuring; host ecology.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Study site location in south-east Slovakia. Map was plotted using SimpleMappr.
Figure 2
Figure 2
Infection intensity of Borrelia garinii in Ixodes ricinus ticks with respect to tick source (two bars in left) and time of season (two bars in right) in Slovakia. Infection intensities (number of copies/µL) refer to back-transformed estimates from the negative-binomial generalized linear model. Birds (n = 21 ticks) and vegetation (n = 11 ticks) denote bird-feeding and questing ticks, respectively. Bird-feeding ticks comprised 5 larvae and 16 nymphs, whereas questing ticks comprised 10 nymphs and 1 adult. The data for June and July were pooled. Errors are 95% confidence limits.
Figure 3
Figure 3
Seasonal occurrence of multi-locus sequence types (STs) of Borrelia garinii detected in bird-feeding and questing Ixodes ricinus ticks in Slovakia. Birds and vegetation denote bird-feeding and questing ticks, respectively. Each ST is denoted by a unique bar colour. ST labels with a red margin indicate novel STs detected for the first time in this study. Note that no ST was resolved for questing ticks in July.
Figure 4
Figure 4
Population structure of Borrelia garinii multi-locus sequence types (STs) involving STs from Slovakia. Population structure for 147 STs deposited in the PubMLST database was constructed by the goeBURST algorithm with PhyloViz 2. Clonal complexes (CCs) were constructed at the level of single-locus variants (SLVs). ST 903 was not assigned into any CC and was classified as a singleton. ST nodes representing inferred CC founders are outlined in light-green color. Node size reflects the number of isolates for the ST. Black lines between nodes refer to links drawn without recourse to tiebreak rules, whereas blue lines show links based on tiebreak rule 1 (number of SLVs). Different colors and their areas within nodes reflect country and the number of isolates for the given ST and country. Red color denotes Slovakia; for country legend please see Figure 5.
Figure 5
Figure 5
Minimum-spanning tree of Borrelia garinii multi-locus sequence types (STs). The tree was constructed for 147 STs deposited in the PubMLST database by the goeBURST Full MST algorithm with PhyloViz 2. The tree was constructed at the maximum level of locus variants (level 8). ST nodes representing inferred CC founders are outlined in light-green color. Node size reflects the number of isolates for the ST. The links having less differences between nodes are shown by darker grey color compared to links between more different nodes. Different colors and their area within nodes reflect country and the number of isolates for the given ST and country. The tree miniature highlights STs detected in Slovakia (red colour).
Figure 6
Figure 6
Unrooted ML tree of Borrelia garinii based on concatenated sequences of eight MLST genes. The tree involves sequences for 147 B. garinii sequence types (STs) deposited in the PubMLST database. Even though the tree is unrooted, B. burgdorferi s.s. (ST 1) was used as outgroup and was drawn at root. Branch length for B. burgdorferi s.s. is not scaled as indicated by the slashes. ML tree was constructed using IQ-TREE, based on the best-fit substitution model (GTR-F-R5) selected according to ModelFinder. The branch support was assessed using the aBayes test and is shown for branches with >70% support. Taxon labels are isolate and ST IDs according to the PubMLST database. STs detected for the first time in this study are marked in red.
Figure 7
Figure 7
Minimum-spanning tree of Borrelia garinii multi-locus sequence types (STs). The tree highlights STs detected in samples from Lyme disease human patients (blue colour). Blue area within nodes reflects the number of isolates for the given ST.
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