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Metagenomic profile of the bacterial communities associated with Ixodes ricinus ticks.

ABSTRACT: Assessment of the microbial diversity residing in arthropod vectors of medical importance is crucial for monitoring endemic infections, for surveillance of newly emerging zoonotic pathogens, and for unraveling the associated bacteria within its host. The tick Ixodes ricinus is recognized as the primary European vector of disease-causing bacteria in humans. Despite I. ricinus being of great public health relevance, its microbial communities remain largely unexplored to date. Here we evaluate the pathogen-load and the microbiome in single adult I. ricinus by using 454- and Illumina-based metagenomic approaches. Genomic DNA-derived sequences were taxonomically profiled using a computational approach based on the BWA algorithm, allowing for the identification of known tick-borne pathogens at the strain level and the putative tick core microbiome. Additionally, we assessed and compared the bacterial taxonomic profile in nymphal and adult I. ricinus pools collected from two distinct geographic regions in Northern Italy by means of V6-16S rRNA amplicon pyrosequencing and community based ecological analysis. A total of 108 genera belonging to representatives of all bacterial phyla were detected and a rapid qualitative assessment for pathogenic bacteria, such as Borrelia, Rickettsia and Candidatus Neoehrlichia, and for other bacteria with mutualistic relationship or undetermined function, such as Wolbachia and Rickettsiella, was possible. Interestingly, the ecological analysis revealed that the bacterial community structure differed between the examined geographic regions and tick life stages. This finding suggests that the environmental context (abiotic and biotic factors) and host-selection behaviors affect their microbiome.Our data provide the most complete picture to date of the bacterial communities present within I. ricinus under natural conditions by using high-throughput sequencing technologies. This study further demonstrates a novel detection strategy for the microbiomes of arthropod vectors in the context of epidemiological and ecological studies.

SUBMITTER: Carpi G

PROVIDER: S-EPMC3192763 | biostudies-literature | 2011

REPOSITORIES: biostudies-literature

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Metagenomic profile of the bacterial communities associated with Ixodes ricinus ticks.

Carpi Giovanna G Cagnacci Francesca F Wittekindt Nicola E NE Zhao Fangqing F Qi Ji J Tomsho Lynn P LP Drautz Daniela I DI Rizzoli Annapaola A Schuster Stephan C SC

PloS one 20111013 10

Assessment of the microbial diversity residing in arthropod vectors of medical importance is crucial for monitoring endemic infections, for surveillance of newly emerging zoonotic pathogens, and for unraveling the associated bacteria within its host. The tick Ixodes ricinus is recognized as the primary European vector of disease-causing bacteria in humans. Despite I. ricinus being of great public health relevance, its microbial communities remain largely unexplored to date. Here we evaluate the ...[more]

PMID: 22022422

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Project description:Ixodes persulcatus, Ixodes pavlovskyi, and Dermacentor reticulatus ticks inhabiting Western Siberia are responsible for the transmission of a number of etiological agents that cause human and animal tick-borne diseases. Because these ticks are abundant in the suburbs of large cities, agricultural areas, and popular tourist sites and frequently attack people and livestock, data regarding the microbiomes of these organisms are required. Using metagenomic 16S profiling, we evaluate bacterial communities associated with I. persulcatus, I. pavlovskyi, and D. reticulatus ticks collected from the Novosibirsk region of Russia. A total of 1214 ticks were used for this study. DNA extracted from the ticks was pooled according to tick species and sex. Sequencing of the V3-V5 domains of 16S rRNA genes was performed using the Illumina Miseq platform. The following bacterial genera were prevalent in the examined communities: Acinetobacter (all three tick species), Rickettsia (I. persulcatus and D. reticulatus) and Francisella (D. reticulatus). B. burgdorferi sensu lato and B. miyamotoi sequences were detected in I. persulcatus and I. pavlovskyi but not in D. reticulatus ticks. The pooled samples of all tick species studied contained bacteria from the Anaplasmataceae family, although their occurrence was low. DNA from A. phagocytophilum and Candidatus Neoehrlichia mikurensis was first observed in I. pavlovskyi ticks. Significant inter-species differences in the number of bacterial taxa as well as intra-species diversity related to tick sex were observed. The bacterial communities associated with the I. pavlovskyi ticks displayed a higher biodiversity compared with those of the I. persulcatus and D. reticulatus ticks. Bacterial community structure was also diverse across the studied tick species, as shown by permutational analysis of variance using the Bray-Curtis dissimilarity metric (p = 0.002). Between-sex variation was confirmed by PERMANOVA testing in I. persulcatus (p = 0.042) and I. pavlovskyi (p = 0.042) ticks. Our study indicated that 16S metagenomic profiling could be used for rapid assessment of the occurrence of medically important bacteria in tick populations inhabiting different natural biotopes and therefore the epidemic danger of studied foci.

Project description:Background:Ticks can survive long periods without feeding but, when feeding, ingest large quantities of blood, resulting in a more than 100-fold increase of body volume. We study morphological adaptations to changes in opisthosoma volume during feeding in the castor bean tick, Ixodes ricinus. We aim to understand the functional morphological features that accommodate enormous changes in volume changes. Methods:Using light and electron microscopy, we compare the cuticle and epidermis of the alloscutum, the epithelium of the midgut diverticula, and the tracheae of adult female ticks when fasting, semi-engorged, and fully engorged. Results:Our results add to an existing body of knowledge that the area of the epidermis increases by cellular differentiation, cellular hypertrophy, and changes in the shape of epithelial cells from pseudostratified to single layered prismatic in semi-engorged ticks, and to thin squamous epithelium in fully engorged ticks. We did not find evidence for cell proliferation. The midgut diverticula accommodate the volume increase by cellular hypertrophy and changes in cell shape. In fully engorged ticks, the epithelial cells of the midgut diverticula are stretched to an extremely thin, squamous epithelium. Changes in size and shape (and cell divisions) contribute to the accommodation of volume changes. Tracheae do not increase in size, but extend in length, thus following the volume changes of the opisthosoma in feeding ticks to secure oxygen supply to the internal organs. Conclusions:Changes of epithelial tissue configuration in the epidermis and the midgut diverticula are described as important components of the morphological response to feeding in ticks. We provide evidence for a previously unknown mechanism hosted in the endocuticle of the tracheae that allows the tracheae of castor bean ticks to expand when the body volume increases and the distance between the respiratory spiracle and the oxygen demanding tissue enlarges. This is the first report of expandable tracheae in arthropods.

Dataset Information

Metagenomic profile of the bacterial communities associated with Ixodes ricinus ticks.

Publications

Metagenomic profile of the bacterial communities associated with Ixodes ricinus ticks.

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