Factors affecting the microbiome of Ixodes scapularis and Amblyomma americanum.

R Jory Brinkerhoff,Kelly Ocasio,David T Gauthier,Wayne L Hynes,Chris Clark,Ulrike Gertrud Munderloh

doi:10.1371/journal.pone.0232398

R Jory Brinkerhoff, Kelly Ocasio + Show 4 more

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https://doi.org/10.1371/journal.pone.0232398

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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 human-biting 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 environmentally-related 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.

Highlights

Microbial communities associated with arthropod disease vectors have been a focus of study for over a decade
While the majority of metagenomic studies of disease vectors focus on bacterial communities, rather than eukaryotic microbes or viruses, there is still much to learn about the factors that affect bacterial community composition in arthropod vectors and how these microbial communities might impact pathogen transmission [7]
Microbiota of individual ticks from the same population may vary substantially [39] so our goal was to collect ten adult male, ten adult female, and ten nymphal Ixodes scapularis and the same number of Amblyomma americanum from each site and we visited each site on several occasions to maximize our chances of meeting this objective

Summary

Introduction

Microbial communities associated with arthropod disease vectors have been a focus of study for over a decade (eg [1, 2, 3, 4, 5, 6]). While the majority of metagenomic studies of disease vectors focus on bacterial communities, rather than eukaryotic microbes or viruses, there is still much to learn about the factors that affect bacterial community composition in arthropod vectors and how these microbial communities might impact pathogen transmission [7]. In addition to the obvious importance of pathogen occurrence, abundance, and genotypic diversity in disease vectors, there is increasing recognition that non-pathogenic microbes might affect acquisition and transmission of vector-borne pathogens [8, 9]. The presence of specific bacterial genera may inhibit the growth of pathogens, and some non-pathogenic bacteria may facilitate colonization by pathogens or affect vector behavior in ways that impact transmission dynamics [10, 11]. Pathogen occurrence may enhance vector survival [12, 13] and affect range expansion and abundance of such vectors in the environment [9, 14, 15]

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