Factors affecting the microbiome of Ixodes scapularis and Amblyomma americanum.

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 unders...

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Main Authors: R Jory Brinkerhoff, Chris Clark, Kelly Ocasio, David T Gauthier, Wayne L Hynes
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2020-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0232398
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spelling doaj-1689053648244e429f9fc6d615a2619d2021-03-03T21:46:14ZengPublic Library of Science (PLoS)PLoS ONE1932-62032020-01-01155e023239810.1371/journal.pone.0232398Factors affecting the microbiome of Ixodes scapularis and Amblyomma americanum.R Jory BrinkerhoffChris ClarkKelly OcasioDavid T GauthierWayne L HynesThe 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.https://doi.org/10.1371/journal.pone.0232398
collection DOAJ
language English
format Article
sources DOAJ
author R Jory Brinkerhoff
Chris Clark
Kelly Ocasio
David T Gauthier
Wayne L Hynes
spellingShingle R Jory Brinkerhoff
Chris Clark
Kelly Ocasio
David T Gauthier
Wayne L Hynes
Factors affecting the microbiome of Ixodes scapularis and Amblyomma americanum.
PLoS ONE
author_facet R Jory Brinkerhoff
Chris Clark
Kelly Ocasio
David T Gauthier
Wayne L Hynes
author_sort R Jory Brinkerhoff
title Factors affecting the microbiome of Ixodes scapularis and Amblyomma americanum.
title_short Factors affecting the microbiome of Ixodes scapularis and Amblyomma americanum.
title_full Factors affecting the microbiome of Ixodes scapularis and Amblyomma americanum.
title_fullStr Factors affecting the microbiome of Ixodes scapularis and Amblyomma americanum.
title_full_unstemmed Factors affecting the microbiome of Ixodes scapularis and Amblyomma americanum.
title_sort factors affecting the microbiome of ixodes scapularis and amblyomma americanum.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2020-01-01
description 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.
url https://doi.org/10.1371/journal.pone.0232398
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