The Tick Microbiome: Why Non-pathogenic Microorganisms Matter in Tick Biology and Pathogen Transmission

Bonnet, Sarah; Binetruy, Florian; Hernández-Jarguín, Angélica; Duron, Olivier

doi:10.3389/fcimb.2017.00236

Cited by 301 publications

(384 citation statements)

References 133 publications

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“…Ticks are important vectors of many human and animal pathogens. In addition, they carry numerous endosymbionts and commensals, which may provide nutrient supplements to the tick and also affect vector competence (reviewed in (Narasimhan & Fikrig, ; Bonnet et al., ; Clay & Fuqua, )). Studies have reported that the tick microbial community is variable depending on several factors such as source of host blood meal (Rynkiewicz, Hemmerich, Rusch, Fuqua, & Clay, ), feeding status (Menchaca et al., ; Swei & Kwan, ; Zhang et al., ), tick species, life stage, gender, and geographical origin (Carpi et al., ; Van Treuren et al., ; Williams‐Newkirk, Rowe, Mixson‐Hayden, & Dasch, ).…”

Section: Discussionmentioning

confidence: 99%

“…The tick is also a vector for a number of other human pathogens, including Anaplasma phagocytophilum , Babesia microti , and Powassan virus (CDC, 2017a; Ebel, ; Piesman & Eisen, ). In addition, these ticks carry a variety of commensal and endosymbiotic bacteria of unknown pathogenicity (Bonnet, Binetruy, Hernández‐Jarguín, & Duron, ; Narasimhan & Fikrig, ).…”

Section: Introductionmentioning

confidence: 99%

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Effects of temperature on bacterial microbiome composition in Ixodes scapularis ticks

2018

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Ixodes scapularis , the blacklegged deer tick, is the principal vector of Lyme disease in North America. Environmental factors are known to influence regional and seasonal incidence of Lyme disease and possibly the endemicity of the disease to the northeastern and upper mid‐western regions of the United States. With a goal to understand the impact of environmental temperature on microbial communities within the tick, we investigated the bacterial microbiome of colony‐reared I. scapularis ticks statically incubated at different temperatures (4, 20, 30, and 37°C) at a constant humidity in a controlled laboratory setting by comparison of sequenced amplicons of the bacterial 16S V4 rRNA gene to that of the untreated baseline controls. The microbiomes of colony‐reared I. scapularis males were distinct than that of females, which were entirely dominated by Rickettsia . In silico removal of Rickettsia sequences from female data revealed the underlying bacterial community, which is consistent in complexity with those seen among male ticks. The bacterial community composition of these ticks changes upon incubation at 30°C for a week and 37°C for more than 5 days. Moreover, the male ticks incubated at 30 and 37°C exhibited significantly different bacterial diversity compared to the initial baseline microbiome, and the change in bacterial diversity was dependent upon duration of exposure. Rickettsia ‐free data revealed a significantly different bacterial diversity in female ticks incubated at 37°C compared to that of 4 and 20°C treatments. These results provide experimental evidence that environmental temperature can impact the tick bacterial microbiome in a laboratory setting.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Effects of temperature on bacterial microbiome composition in Ixodes scapularis ticks

2018

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“…It is evident that tick microbes can be maternally inherited (vertical transmission), environmentally acquired through the tick spiracles, mouth, or anal pore (environmental transmission), or obtained from host‐blood feeding (horizontal transmission) (Narasimhan & Fikrig, ). The microbial community resulting from these processes consists largely of tick symbionts and guest commensals (Clay & Fuqua, ; Greay et al, ), which can affect vector fitness (reviewed in Bonnet et al, ) and have been associated with variation in vector competence (Budachetri et al, ; Civitello, Rynkiewicz, & Clay, ; Gall et al, ; Narasimhan et al, ; Telford, ). The latter observation motivated an increased number of studies of the role of ecological and environmental factors in shaping the microbiome and the relationship between microbial symbionts and pathogens (Fryxell & DeBruyn, ; Gall, Scoles, Magori, Mason, & Brayton, ; Kwan, Griggs, Chicana, Miller, & Swei, ; Narasimhan et al, ; Swei & Kwan, ; Van Treuren et al, ; Zolnik, Prill, Falco, Daniels, & Kolokotronis, ).…”

Section: Introductionmentioning

confidence: 99%

Drivers and patterns of microbial community assembly in a Lyme disease vector

Couper

Kwan

et al. 2019

Ecology and Evolution

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Vector‐borne diseases constitute a major global health burden and are increasing in geographic range and prevalence. Mounting evidence has demonstrated that the vector microbiome can impact pathogen dynamics, making the microbiome a focal point in vector‐borne disease ecology. However, efforts to generalize preliminary findings across studies and systems and translate these findings into disease control strategies are hindered by a lack of fundamental understanding of the processes shaping the vector microbiome and the interactions therein. Here, we use 16S rRNA sequencing and apply a community ecology framework to analyze microbiome community assembly and interactions in Ixodes pacificus , the Lyme disease vector in the western United States. We find that vertical transmission routes drive population‐level patterns in I. pacificus microbial diversity and composition, but that microbial function and overall abundance do not vary over time or between clutches. Further, we find that the I. pacificus microbiome is not strongly structured based on competition but assembles nonrandomly, potentially due to vector‐specific filtering processes which largely eliminate all but the dominant endosymbiont, Rickettsia . At the scale of the individual I. pacificus , we find support for a highly limited internal microbial community, and hypothesize that the tick endosymbiont may be the most important component of the vector microbiome in influencing pathogen dynamics.

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“…In the tick gut, endosymbionts and other non-pathogenic microbes significantly outnumber pathogenic organisms [10]. The nature of the relationship between ticks and their symbionts remains understudied and, therefore, poorly understood.…”

Section: Introductionmentioning

confidence: 99%

Range-wide genetic analysis of Dermacentor variabilis and its Francisella-like endosymbionts demonstrates phylogeographic concordance between both taxa

et al. 2018

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BackgroundThe American dog tick, Dermacentor variabilis, is an important vector of pathogens to humans, wildlife and domestic animals in North America. Although this tick species is widely distributed in the USA and Canada, knowledge of its range-wide phylogeographic patterns remains incomplete.MethodsWe carried out a phylogenetic analysis of D. variabilis using samples collected from 26 USA states and five Canadian provinces. Tick samples (n = 1053 in total) originated from two main sources: existing archives (2000–2011), and new collections made from 2012 to 2013. We sequenced a 691 bp fragment of the cox1 gene from a subset (n = 332) of geographically diverse D. variabilis. DNA extracted from individual ticks (n = 1053) was also screened for a Francisella-like endosymbiont, using a targeted 16S rRNA sequencing approach, and important pathogens (Rickettsia spp. and Coxiella burnetii), using species-specific quantitative PCR assays.ResultsMaximum parsimony analysis of cox1 sequences revealed two major groups within D. variabilis with distinct geographical distributions: one from the eastern USA/Canada (Group 1) and one from the west coast states of the USA (California and Washington; Group 2). However, genetic subdivisions within both of these two major groups were weak to moderate and not tightly correlated with geography. We found molecular signatures consistent with Francisella-like endosymbionts in 257 of the DNA extracts from the 1053 individual ticks, as well as Rickettsia spp. and Coxiella burnetii in a small number of ticks (n = 29 and 2, respectively). Phylogenetic patterns for Francisella-like endosymbionts, constructed using sequence data from the bacterial 16S rRNA locus, were similar to those for D. variabilis, with two major groups that had a nearly perfect one-to-one correlation with the two major groups within D. variabilis.ConclusionsOur findings reveal a distinct phylogenetic split between the two major D. variabilis populations. However, high levels of genetic mixture among widely separated geographical localities occur within each of these two major groups. Furthermore, our phylogenetic analyses provide evidence of long-term tick-symbiont co-evolution. This work has implications for understanding the dispersal and evolutionary ecology of D. variabilis and associated vector-borne diseases.Electronic supplementary materialThe online version of this article (10.1186/s13071-018-2886-5) contains supplementary material, which is available to authorized users.

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The Tick Microbiome: Why Non-pathogenic Microorganisms Matter in Tick Biology and Pathogen Transmission

Cited by 301 publications

References 133 publications

Effects of temperature on bacterial microbiome composition in Ixodes scapularis ticks

Effects of temperature on bacterial microbiome composition in Ixodes scapularis ticks

Drivers and patterns of microbial community assembly in a Lyme disease vector

Range-wide genetic analysis of Dermacentor variabilis and its Francisella-like endosymbionts demonstrates phylogeographic concordance between both taxa

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