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The characterization and manipulation of the bacterial microbiome of the Rocky Mountain wood tick, Dermacentor andersoni.

ABSTRACT: In North America, ticks are the most economically impactful vectors of human and animal pathogens. The Rocky Mountain wood tick, Dermacentor andersoni (Acari: Ixodidae), transmits Rickettsia rickettsii and Anaplasma marginale to humans and cattle, respectively. In recent years, studies have shown that symbiotic organisms are involved in a number of biochemical and physiological functions. Characterizing the bacterial microbiome of D. andersoni is a pivotal step towards understanding symbiont-host interactions.In this study, we have shown by high-throughput sequence analysis that the composition of endosymbionts in the midgut and salivary glands in adult ticks is dynamic over three generations. Four Proteobacteria genera, Rickettsia, Francisella, Arsenophonus, and Acinetobacter, were identified as predominant symbionts in these two tissues. Exposure to therapeutic doses of the broad-spectrum antibiotic, oxytetracycline, affected both proportions of predominant genera and significantly reduced reproductive fitness. Additionally, Acinetobacter, a free-living ubiquitous microbe, invaded the bacterial microbiome at different proportions based on antibiotic treatment status suggesting that microbiome composition may have a role in susceptibility to environmental contaminants.This study characterized the bacterial microbiome in D. andersoni and determined the generational variability within this tick. Furthermore, this study confirmed that microbiome manipulation is associated with tick fitness and may be a potential method for biocontrol.

SUBMITTER: Clayton KA

PROVIDER: S-EPMC4674957 | biostudies-literature | 2015 Dec

REPOSITORIES: biostudies-literature

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The characterization and manipulation of the bacterial microbiome of the Rocky Mountain wood tick, Dermacentor andersoni.

Clayton Katie A KA Gall Cory A CA Mason Katheen L KL Scoles Glen A GA Brayton Kelly A KA

Parasites & vectors 20151210

<h4>Background</h4>In North America, ticks are the most economically impactful vectors of human and animal pathogens. The Rocky Mountain wood tick, Dermacentor andersoni (Acari: Ixodidae), transmits Rickettsia rickettsii and Anaplasma marginale to humans and cattle, respectively. In recent years, studies have shown that symbiotic organisms are involved in a number of biochemical and physiological functions. Characterizing the bacterial microbiome of D. andersoni is a pivotal step towards underst ...[more]

PMID: 26653035

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Project description:Tick salivary glands produce complex cocktails of bioactive molecules that facilitate blood feeding and pathogen transmission by modulating host hemostasis, pain/itch responses, wound healing, and both innate and adaptive immunity. In this study, cutaneous responses at Dermacentor andersoni bite-sites were analyzed using Affymetrix mouse genome arrays and histopathology at 12, 48, 96 and 120 h post- infestation (hpi) during primary infestations and 120 hpi during secondary infestations. The microarray data suggests: (1) chemotaxis of neutrophils, monocytes, and other cell types; (2) production and scavenging of reactive oxygen species; and, (3) keratin- based wound healing responses. Histological analysis supported the microarray findings. At 12 hpi, a mild inflammatory infiltrate was present in the dermis, especially concentrated at the junction between dermal connective tissue and underlying adipose tissue. A small lesion was located immediately under the hypostome and likely represents the feeding "pool." Surprisingly, at 48 hpi, the number of inflammatory cells had not increased from 12 hpi, perhaps mirroring the reduction in gene expression seen at this time point. The feeding lesion is very well defined, and extravasated erythrocytes are readily evident around the hypostome. By 96 hpi, the inflammatory infiltrate has increased dramatically and the feeding lesion appears to have moved deeper into the dermis. At 120 hpi, most of the changes at 96 hpi are intensified. The infiltrate is very dense, the epidermis is markedly thickened, the feeding lesion is poorly defined and the dermal tissue near the hypostome appears to be loosing its normal architecture. In conclusion, during D. andersoni feeding infiltration of inflammatory cells increases across time concurrent with significant changes in the epidermal and dermal compartments near the feeding tick. The importance of changes in the epidermal layer in the host response to ticks is not known, however, it is possible the host attempts to "slough off" the tick by greatly increasing epithelial cell replication.

Project description:UnlabelledTick-borne transmission of bacterial pathogens in the order Rickettsiales is responsible for diverse infectious diseases, many of them severe, in humans and animals. Transmission dynamics differ among these pathogens and are reflected in the pathogen-vector interaction. Anaplasma marginale has been shown to establish and maintain infectivity within Dermacentor spp. for weeks to months while escaping the complex network of vacuolar peptidases that are responsible for digestion of the tick blood meal. How this prolonged maintenance of infectivity in a potentially hostile environment is achieved has been unknown. Using the natural vector Dermacentor andersoni, we demonstrated that A. marginale-infected tick vacuoles (AmVs) concurrently recruit markers of the early endosome (Rab5), recycling endosome (Rab4 and Rab11), and late endosome (Rab7), are maintained near neutral pH, do not fuse with lysosomes, exclude the protease cathepsin L, and engage the endoplasmic reticulum and Golgi apparatus for up to 21 days postinfection. Maintenance of this safe vacuolar niche requires active A. marginale protein synthesis; in its absence, the AmVs mature into acidic, protease-active phagolysosomes. Identification of this bacterially directed modeling of the tick midgut endosome provides a mechanistic basis for examination of the differences in transmission efficiency observed among A. marginale strains and among vector populations.ImportanceTicks transmit a variety of intracellular bacterial pathogens that cause significant diseases in humans and animals. For successful transmission, these bacterial pathogens must first gain entry into the tick midgut digestive cells, avoid digestion, and establish a replicative niche without harming the tick vector. Little is known about how this replicative niche is established and maintained. Using the ruminant pathogen A. marginale and its natural tick vector, D. andersoni, this study characterized the features of the A. marginale niche in the tick midgut and demonstrates that A. marginale protein synthesis is required for the maintenance of this niche. This work opens a new line of inquiry about the pathogen effectors and their targets within the tick that mediate tick-pathogen interactions and ultimately serve as the determinants of pathogen success.

Project description:BackgroundNearly a quarter of emerging infectious diseases identified in the last century are arthropod-borne. Although ticks and insects can carry pathogenic microorganisms, non-pathogenic microbes make up the majority of their microbial communities. The majority of tick microbiome research has had a focus on discovery and description; very few studies have analyzed the ecological context and functional responses of the bacterial microbiome of ticks. The goal of this analysis was to characterize the stability of the bacterial microbiome of Dermacentor andersoni ticks between generations and two populations within a species.MethodsThe bacterial microbiome of D. andersoni midguts and salivary glands was analyzed from populations collected at two different ecologically distinct sites by comparing field (F1) and lab-reared populations (F1-F3) over three generations. The microbiome composition of pooled and individual samples was analyzed by sequencing nearly full-length 16S rRNA gene amplicons using a Pacific Biosciences CCS platform that allows identification of bacteria to the species level.FindingsIn this study, we found that the D. andersoni microbiome was distinct in different geographic populations and was tissue specific, differing between the midgut and the salivary gland, over multiple generations. Additionally, our study showed that the microbiomes of laboratory-reared populations were not necessarily representative of their respective field populations. Furthermore, we demonstrated that the microbiome of a few individual ticks does not represent the microbiome composition at the population level.ConclusionsWe demonstrated that the bacterial microbiome of D. andersoni was complex over three generations and specific to tick tissue (midgut vs. salivary glands) as well as geographic location (Burns, Oregon vs. Lake Como, Montana vs. laboratory setting). These results provide evidence that habitat of the tick population is a vital component of the complexity of the bacterial microbiome of ticks, and that the microbiome of lab colonies may not allow for comparative analyses with field populations. A broader understanding of microbiome variation will be required if we are to employ manipulation of the microbiome as a method for interfering with acquisition and transmission of tick-borne pathogens.

Dataset Information

The characterization and manipulation of the bacterial microbiome of the Rocky Mountain wood tick, Dermacentor andersoni.

Publications

The characterization and manipulation of the bacterial microbiome of the Rocky Mountain wood tick, Dermacentor andersoni.

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