Factors affecting the microbiome of Ixodes scapularis and Amblyomma americanum

Abstract

The microbial community composition of disease vectors can impact pathogen establishment and transmission as well as on vector behavior and fitness. While data on vector microbiota are accumulating quickly, determinants of the variation in disease vector microbial communities are incompletely understood. We explored the microbiome of two humanbiting tick species abundant in eastern North America (Amblyomma americanum and Ixodes scapularis) to identify the relative contribution of tick species, tick life stage, tick sex, environmental context and vertical transmission to the richness, diversity, and species composition of the tick microbiome. We sampled 89 adult and nymphal Ixodes scapularis (N = 49) and Amblyomma americanum (N = 40) from two field sites and characterized the microbiome of each individual using the v3-v4 hypervariable region of the 16S rRNA gene. We identified significant variation in microbial community composition due to tick species and life stage with lesser impact of sampling site. Compared to unfed nymphs and males, the microbiome of engorged adult female I. scapularis, as well as the egg masses they produced, were low in bacterial richness and diversity and were dominated by Rickettsia, suggesting strong vertical transmission of this genus. Likewise, microbiota of A. americanum nymphs and males were more diverse than those of adult females. Among bacteria of public health importance, we detected several different Rickettsia sequence types, several of which were distinct from known species. Borrelia was relatively common in I. scapularis but did not show the same level of sequence variation as Rickettsia. Several bacterial genera were significantly over-represented in Borrelia-infected I. scapularis, suggesting a potential interaction of facilitative relationship between these taxa; no OTUs were under-represented in Borrelia-infected ticks. The systematic sampling we conducted for this study allowed us to partition the variation in tick microbial composition as a function of tick-and environmentallyrelated factors. Upon more complete understanding of the forces that shape the tick microbiome it will be possible to design targeted experimental studies to test the impacts of individual taxa and suites of microbes on vector-borne pathogen transmission and on vector biology.

Microbiome Composition and Borrelia Detection in Ixodes scapularis Ticks at the Northwestern Edge of Their Range

“…In contrast to our results, three recent studies have shown no significant difference in bacterial diversity associated with Borrelia infection status [ 58 , 73 , 74 ], and a fourth study was ambiguous [ 28 ]. However, one of these studies reported results for a mix of females and males [ 73 ], which would have increased the variance in an already noisy system [ 17 ].…”

“…The microbiome of Ixodes scapularis ticks in Alberta is dominated by Rickettsia endosymbionts, with Pseudomonas more common in some individuals, making it similar to the microbiome composition reported for these ticks in established areas of their range [ 28 , 29 , 51 ]. Alberta ticks that carried Borrelia had significantly greater microbiome diversity than ticks that had no Borrelia , a finding that suggests an altered microbiome ecology in Borrelia -positive ticks, as well as the potential to use microbiome diversity as an indicator of elevated risk of infection by Borrelia .…”

“…A third study [ 58 ] distinguished males from females and found no significant differences in bacterial community composition between B+ and B− ticks, on the basis of unweighted UniFrac distance; however, they did not address differences in numbers of bacterial taxa for B+ and B− ticks. Finally, the fourth study [ 28 ] gave mixed results. Richness in B+ ticks was significantly higher when all life stages were considered; however, there was no difference in diversity between B+ and B− nymphal ticks alone [ 28 ].…”

“…Ixodes ticks have recently expanded their range in Canada [ 24 , 25 ], which is a serious concern because they transmit Borrelia species that cause Lyme disease, the most common arthropod-vectored disease in North America [ 24 , 26 , 27 ]. The main vector of Lyme disease in North America is the blacklegged tick, Ixodes scapularis , the microbiome of which is dominated by Rickettsia in established populations, while more than 50% of ticks may also be infected with Borrelia in some areas [ 28 , 29 ]. Few microbiome studies of I. scapularis are available from areas where the tick is expanding its range or is adventitious, such as Alberta [ 30 , 31 ].…”

Mechanisms Affecting the Acquisition, Persistence and Transmission of Francisella tularensis in Ticks

“…Rickettsia endosymbionts are common in Ixodes and some Ornithodoros tick species, while FLEs have been found in Amblyomma , Dermacentor , and Hyalomma ticks [ 31 ]. However, the number of different endosymbionts and prevalence of endosymbionts in each tick are known to vary by geographic location, time of year collected, life stage, sex, tick species, and lab-reared vs. wild-caught ticks [ 31 , 101 , 102 , 103 , 104 ]. A comprehensive study of over 80 tick species from around the world, including lab-reared and wild-caught ticks, identified the most prevalent tick endosymbiont to be a Coxiella -like endosymbiont (CLE) [ 31 ].…”