Dataset Information

Sequencing the Obligate Intracellular Rhabdochlamydia helvetica within Its Tick Host Ixodes ricinus to Investigate Their Symbiotic Relationship.

ABSTRACT: The Rhabdochlamydiaceae family is one of the most widely distributed within the phylum Chlamydiae, but most of its members remain uncultivable. Rhabdochlamydia 16S rRNA was recently reported in more than 2% of 8,534 pools of ticks from Switzerland. Shotgun metagenomics was performed on a pool of five female Ixodes ricinus ticks presenting a high concentration of chlamydial DNA, allowing the assembly of a high-quality draft genome. About 60% of sequence reads originated from a single bacterial population that was named "Candidatus Rhabdochlamydia helvetica" whereas only few thousand reads mapped to the genome of "Candidatus Midichloria mitochondrii," a symbiont normally observed in all I. ricinus females. The 1.8 Mbp genome of R. helvetica is smaller than other Chlamydia-related bacteria. Comparative analyses with other chlamydial genomes identified transposases of the PD-(D/E)XK nuclease family that are unique to this new genome. These transposases show evidence of interphylum horizontal gene transfers between multiple arthropod endosymbionts, including Cardinium spp. (Bacteroidetes) and diverse proteobacteria such as Wolbachia, Rickettsia spp. (Rickettsiales), and Caedimonas varicaedens (Holosporales). Bacterial symbionts were previously suggested to provide B-vitamins to hematophagous hosts. However, incomplete metabolic capacities including for B-vitamin biosynthesis, high bacterial density and limited prevalence suggest that R. helvetica is parasitic rather than symbiotic to its host. The identification of novel Rhabdochlamydia strains in different hosts and their sequencing will help understanding if members of this genus have become highly specialized parasites with reduced genomes, like the Chlamydiaceae, or if they could be pathogenic to humans using ticks as a transmission vector.

SUBMITTER: Pillonel T

PROVIDER: S-EPMC6490308 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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Sequencing the Obligate Intracellular Rhabdochlamydia helvetica within Its Tick Host Ixodes ricinus to Investigate Their Symbiotic Relationship.

Pillonel Trestan T Bertelli Claire C Aeby Sébastien S de Barsy Marie M Jacquier Nicolas N Kebbi-Beghdadi Carole C Mueller Linda L Vouga Manon M Greub Gilbert G

Genome biology and evolution 20190401 4

The Rhabdochlamydiaceae family is one of the most widely distributed within the phylum Chlamydiae, but most of its members remain uncultivable. Rhabdochlamydia 16S rRNA was recently reported in more than 2% of 8,534 pools of ticks from Switzerland. Shotgun metagenomics was performed on a pool of five female Ixodes ricinus ticks presenting a high concentration of chlamydial DNA, allowing the assembly of a high-quality draft genome. About 60% of sequence reads originated from a single bacterial po ...[more]

PMID: 30949677

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Project description:Rickettsia helvetica is an emerging pathogen of the Spotted Fever Group Rickettsia (SFGR) causing spotted fever diseases in various European countries. This tick-borne pathogen replicates in tick tissues such as the midgut and salivary gland, but its potential interactions with the vector microbiota is poorly characterized. The vector microbiome plays a pivotal role in tick-pathogen interactions, and some microbiota members facilitate or impede tick-borne pathogen infection. Manipulations of the tick microbiome have led to reduction in pathogen colonization in the tick vector. However, translating these findings into disease control applications requires a thorough characterization of vector microbiota response to different pathogens. In this study, we analyzed and compared the microbiota of Ixodes ricinus ticks attached on humans and collected in Serbia. Ticks were either infected with R. helvetica, or uninfected with major tick-borne pathogens (referred hereafter as 'pathogen-free'). We used microbial co-occurrence network analysis to determine keystone taxa of each set of samples, and to study the interaction patterns of the microbial communities in response to pathogen infection. The inferred functional profiles of the tick microbiome in R. helvetica-positive and pathogen-free samples were also compared. Our results show that R. helvetica infection reduces significantly the diversity of the microbiota and the connectivity of the co-occurrence network. In addition, using co-occurrence network we identified bacterial taxa (i.e., Enterobacteriaceae, Comamonadaceae, and Bacillus) that were negatively associated with 'Rickettsia' in R. helvetica-infected ticks, suggesting competition between R. helvetica and some members of the tick microbiota. The reconstruction of microbial metabolic pathways shows that the presence of R. helvetica might have a major impact on the metabolic functions of the tick microbiome. These results can inform novel interventions for the prevention of R. helvetica, or other SFGR infections in humans.

Project description:BACKGROUND: During their blood meal, ticks secrete a wide variety of proteins that interfere with their host's defense mechanisms. Among these proteins, lipocalins play a major role in the modulation of the inflammatory response. METHODOLOGY/PRINCIPAL FINDINGS: Screening a cDNA library in association with RT-PCR and RACE methodologies allowed us to identify 14 new lipocalin genes in the salivary glands of the Ixodes ricinus hard tick. A computational in-depth structural analysis confirmed that LIRs belong to the lipocalin family. These proteins were called LIR for "Lipocalin from I. ricinus" and numbered from 1 to 14 (LIR1 to LIR14). According to their percentage identity/similarity, LIR proteins may be assigned to 6 distinct phylogenetic groups. The mature proteins have calculated pM and pI varying from 21.8 kDa to 37.2 kDa and from 4.45 to 9.57 respectively. In a western blot analysis, all recombinant LIRs appeared as a series of thin bands at 50-70 kDa, suggesting extensive glycosylation, which was experimentally confirmed by treatment with N-glycosidase F. In addition, the in vivo expression analysis of LIRs in I. ricinus, examined by RT-PCR, showed homogeneous expression profiles for certain phylogenetic groups and relatively heterogeneous profiles for other groups. Finally, we demonstrated that LIR6 codes for a protein that specifically binds leukotriene B4. CONCLUSIONS/SIGNIFICANCE: This work confirms that, regarding their biochemical properties, expression profile, and sequence signature, lipocalins in Ixodes hard tick genus, and more specifically in the Ixodes ricinus species, are segregated into distinct phylogenetic groups suggesting potential distinct function. This was particularly demonstrated by the ability of LIR6 to scavenge leukotriene B4. The other LIRs did not bind any of the ligands tested, such as 5-hydroxytryptamine, ADP, norepinephrine, platelet activating factor, prostaglandins D2 and E2, and finally leukotrienes B4 and C4.

Project description:BackgroundIxodid ticks are important vectors of a wide variety of viral, bacterial and protozoan pathogens of medical and veterinary importance. Although several studies have elucidated tick responses to bacteria, little is known about the tick response to viruses. To gain insight into the response of tick cells to flavivirus infection, the transcriptomes and proteomes of two Ixodes spp cell lines infected with the flavivirus tick-borne encephalitis virus (TBEV) were analysed.MethodsRNA and proteins were isolated from the Ixodes scapularis-derived cell line IDE8 and the Ixodes ricinus-derived cell line IRE/CTVM19, mock-infected or infected with TBEV, on day 2 post-infection (p.i.) when virus production was increasing, and on day 6 p.i. when virus production was decreasing. RNA-Seq and mass spectrometric technologies were used to identify changes in abundance of, respectively, transcripts and proteins. Functional analyses were conducted on selected transcripts using RNA interference (RNAi) for gene knockdown in tick cells infected with the closely-related but less pathogenic flavivirus Langat virus (LGTV).ResultsDifferential expression analysis using DESeq resulted in totals of 43 and 83 statistically significantly differentially-expressed transcripts in IDE8 and IRE/CTVM19 cells, respectively. Mass spectrometry detected 76 and 129 statistically significantly differentially-represented proteins in IDE8 and IRE/CTVM19 cells, respectively. Differentially-expressed transcripts and differentially-represented proteins included some that may be involved in innate immune and cell stress responses. Knockdown of the heat-shock proteins HSP90, HSP70 and gp96, the complement-associated protein Factor H and the protease trypsin resulted in increased LGTV replication and production in at least one tick cell line, indicating a possible antiviral role for these proteins. Knockdown of RNAi-associated proteins Argonaute and Dicer, which were included as positive controls, also resulted in increased LGTV replication and production in both cell lines, confirming their role in the antiviral RNAi pathway.ConclusionsThis systems biology approach identified several molecules that may be involved in the tick cell innate immune response against flaviviruses and highlighted that ticks, in common with other invertebrate species, have other antiviral responses in addition to RNAi.

Dataset Information

Sequencing the Obligate Intracellular Rhabdochlamydia helvetica within Its Tick Host Ixodes ricinus to Investigate Their Symbiotic Relationship.

Publications

Sequencing the Obligate Intracellular Rhabdochlamydia helvetica within Its Tick Host Ixodes ricinus to Investigate Their Symbiotic Relationship.

Similar Datasets

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