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Plantard, O.

Publications and source records attributed to Plantard, O..

10 recordsLinked to original sources

The Bacterial Kinase AnmK Integrates into Tick Genome and Biology

Horizontal Gene Transfer (HGT) contributes to eukaryotic evolution, potentially bringing phenotypic novelties to the recipient organisms. Ticks pose a severe threat to human health as vectors of various pathogens, including viruses, bacteria and protozoa, while stably hosting endosymbiotic bacteria. As such, these obligate blood-feeding parasites have been and continue to be exposed to HGT from a broad range of donors. To determine whether bacterial-to-tick HGT has contributed to important tick traits, we surveyed Ixodes tick genomes for HGT events. We revealed duplications of the known bacteria-derived gene dae2 and discovered two novel cases of bacterial HGT, the most remarkable of which involves a bacterial peptidoglycan metabolic gene (anmK) acquired by the common ancestor of ticks. The acquisition of an intron demonstrates "eukaryotization" of anmK within tick genomes. Transcript profiling revealed that anmK expression is upregulated during blood feeding, peaking in female ovaries, a niche occupied by horizontally acquired endosymbionts. Biochemical analysis confirmed that, to some extent, recombinant AnmK retains kinase activity on its cognate substrate - the bacterial cell wall component 1,6-anhydro-N-acetylmuramic acid. Immunolocalization showed that the enzyme is predominantly localized towards outer layers of the vitellogenic oocytes. Silencing of anmK in different tick species compromised blood-feeding and reproduction, demonstrating that this domesticated bacterial enzyme underpins reproductive fitness across tick species. Our findings exemplify the ability of horizontally acquired genes to integrate into the host biology and thereby shape host life history.

evolutionary biology↗

Phenology of questing Ixodes frontalis nymphs reveals a late-winter to early-spring activity peak

Although Ixodes frontalis is widespread across Europe, including urban and peri-urban habitats, several aspects of its biology remain undescribed. One such aspect is the population dynamics of its nymphal stage, which has so far been reported from limited sample sizes, preventing the identification of its peak abundance. To fill this knowledge gap, we conducted a year-long monthly survey at four locations in France representing three distinct climates. The sampling protocol--based on the flagging method performed under bamboo bushes where larvae of this species had previously been found--was designed to maximize the likelihood of capturing the nymphal stage. Based on the 400 nymphs collected during this survey, a clear peak of I. frontalis nymphs was observed around March (February to April) across all four sites, with an additional peak in August at one site. The population dynamics of the larval stage--based on semi-quantitative counts--showed the same previously described pattern, with a peak in late autumn. Twenty adults (11 females and 9 males) were also collected from March to December, but these data did not allow a clear identification of a peak abundance. Because several bird species--such as blackbirds, song thrushes, European robins, and Eurasian blackcaps--serve as feeding hosts for both I. ricinus and I. frontalis, and are also reservoirs for pathogens transmitted by these ticks, the implications of our findings for the eco-epidemiology of tick-borne diseases are discussed. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=84 SRC="FIGDIR/small/696149v1_ufig1.gif" ALT="Figure 1000"> View larger version (34K): org.highwire.dtl.DTLVardef@170abeforg.highwire.dtl.DTLVardef@2802b5org.highwire.dtl.DTLVardef@c9be48org.highwire.dtl.DTLVardef@eb8e4d_HPS_FORMAT_FIGEXP M_FIG C_FIG HighlightsA sampling method for Ixodes frontalis nymphs was developed Four hundred nymphs were collected across four different sites in France through a monthly survey A clear peak was observed around March, with an additional peak in August at one site

ecology↗

Whole genome sequencing of four Ixodes species expands understanding of tick evolution

Ticks, hematophagous acari, pose a significant threat by transmitting various pathogens to their vertebrate hosts during feeding. Despite advances in tick genomics, high-quality genomes were lacking until recently, particularly in the genus Ixodes, which includes the main vectors of Lyme disease. Here, we present the complete genome sequences of four tick species, derived from a single female individual, with a particular focus on the European species Ixodes ricinus, achieving a chromosome-level assembly. Additionally, draft assemblies were generated for the three other Ixodes species, I. persulcatus, I. pacificus and I. hexagonus. The quality of the four genomes and extensive annotation of several important gene families have allowed us to study the evolution of gene repertoires at the level of the genus Ixodes and of the tick group. We have determined gene families that have undergone major amplifications during the evolution of ticks, while an expression atlas obtained for I. ricinus reveals striking patterns of specialization both between and within gene families. Notably, several gene family amplifications are associated with a proliferation of single-exon genes. The integration of our data with existing genomes establishes a solid framework for the study of gene evolution, improving our understanding of tick biology. In addition, our work lays the foundations for applied research and innovative control targeting these organisms.

genomics↗

Seasonality of host-seeking Ixodes ricinus nymph abundance in relation to climate

There is growing concern about climate change and its impact on human health. Specifically, global warming could increase the probability of emerging infectious diseases, notably because of changes in the geographical and seasonal distributions of disease vectors such as mosquitoes and ticks. For example, the range of Ixodes ricinus, the most common and widespread tick species in Europe, is currently expanding northward and at higher altitudes. However, little is known about the seasonal variation in tick abundance in different climates. Seasonality of I. ricinus is often based on expert opinions while field surveys are usually limited in time. Our objective was to describe seasonal variations in I. ricinus abundance under different climates. To this end, a seven-year longitudinal study, with monthly collections of I. ricinus host-seeking nymphs, was carried out in France, in six locations corresponding to different climates. Tick data were log-transformed and grouped between years so as to obtain seasonal variations for a typical year. Daily average temperature was measured during the study period. Seasonal patterns of nymph abundance were established for the six different locations using linear harmonic regression. Model parameters were estimated separately for each location. Seasonal patterns appeared different depending on the climate considered. Western temperate sites showed an early spring peak, a summer minimum and a moderate autumn and winter abundance. More continental sites showed a later peak in spring, and a minimum in winter. The peak occurred in summer for the mountainous site, with an absence of ticks in winter. In all cases except the mountainous site, the timing of the spring peak could be related to the sum of degree days since the beginning of the year. Winter abundance was positively correlated to the corresponding temperature. Our results highlight clear patterns in the different sites corresponding to different climates, which allow further forecast of tick seasonality under changing climate conditions.

ecology↗

The origin and evolution of mitochondrial tropism in Midichloria bacteria

Midichloria are intracellular bacterial symbionts of ticks. Some representatives of this genus have the unique capability to colonize mitochondria in the cells of their hosts. Hypotheses on the nature of this interaction have proven difficult to test, partly due to a lack of data. Indeed, until now, mitochondrial tropism information and genomes were available only for symbionts of three and two tick host species, respectively. Here we analyzed the mitochondrial tropism of three additional Midichloria and sequenced nine novel genomes, showing that the tropism is pnon-monophyletic, either due to losses of the trait or multiple parallel acquisitions. Comparative genome analyses support the first hypothesis, as the genomes of non-mitochondrial symbionts appear to be reduced subsets of those capable of colonizing the organelles. We detect genomic signatures of mitochondrial tropism, showing a set of candidate genes characteristic of the strains capable of mitochondrial colonization. These include the type IV secretion system and the flagellum, which could allow the secretion of unique effectors, direct interaction with, or invasion of the mitochondria. Other genes, including putative adhesion molecules, proteins possibly involved in actin polymerization, cell wall and outer membrane proteins, are only present in mitochondrial symbionts. The bacteria could use these to manipulate host structures, including mitochondrial membranes, in order to fuse with the organelles or manipulate the mitochondrial network.

evolutionary biology↗

Transcriptome of the synganglion and characterization of the cys-loop ligand-gated ion channel gene family in the tick Ixodes ricinus.

Ticks represent a major health issue for humans and domesticated animals. Assessing the expression patterns of the ticks central nervous system, known as the synganglion, is an important step in understanding tick physiology and in managing tick-borne diseases. Neuron-specific genes like the cys-loop ligand-gated ion channels (cys-loop LGICs) are important pharmacological targets of acaricides. Here, we carried out the sequencing of transcriptomes of the I. ricinus synganglion, for adult ticks in different conditions (unfed males, unfed females, and partially-fed females). The de novo assembly of these transcriptomes allowed us to obtain a large collection of cys-loop LGICs sequences. A reference meta-transcriptome based on synganglion and whole body transcriptomes was then produced, showing high completeness and allowing differential expression analyses between synganglion and whole body. Many of the genes upregulated in the synganglion were related to biological processes or functions associated with neurotransmission and located in neurones or the synaptic membrane, including most of the cys-loop LGICs. As a first step of a functional study of cysLGICs, we cloned the predicted sequence of the resistance to dieldrin (RDL) subunit homologue, and functionally reconstituted the first GABA-gated receptor of Ixodes ricinus using a hetrologous expression approach. A phylogenetic study was performed for the nicotinic acetylcholine receptors (nAChRs) and for other cys-loop LGICs respectively, showing tick-specific expansions of some types of receptors (Histamine-gated, GluCls).

evolutionary biology↗

Borrelia infection in rodent host has dramatic effects on the microbiome of ticks

BackgroundVector-borne diseases remain major causes of human morbidity and mortality. It is increasingly recognized that the community of microbes inhabiting arthropods can strongly affect their vector competence, but the role of the tick microbiome in Borrelia transmission - the cause of Lyme disease - remains unclear. ResultsHere, we use a large-scale experiment to clarify the reciprocal interactions between Borrelia afzelii and the microbiome of Ixodes ricinus, its primary vector. In contrast to other reports, we find that depletion of the bacterial microbiome in larval ticks has no effect on their subsequent acquisition of B. afzelii during blood feeding on infected mice. Rather, exposure to B. afzelii-infected hosts drives pervasive changes to the tick microbiome, decreasing overall bacterial abundance, shifting bacterial community composition, and increasing bacterial diversity. These effects appear to be independent of the acquisition of B. afzelii by ticks, suggesting they are mediated by physiological or immunological aspects of B. afzelii infection in the rodent host. ConclusionsManipulation of the microbiome of I. ricinus larvae had no effect on their ability to acquire B. afzelii. In contrast, B. afzelii infection in the mouse had dramatic effects on the composition of the gut microbiome in I. ricinus nymphs. Our study demonstrates that vector-borne infections in the vertebrate host shape the microbiome of the arthropod vector.

microbiology↗

Sequence diversity and evolution of an iflavirus family associated with ticks

We studied a family of iflaviruses, a group of RNA viruses frequently found in arthropods, focusing on viruses associated with ticks. Our aim was to bring insight on the evolutionary dynamics of this group of viruses, which may interact with the biology of ticks. We explored systematically de novo RNA-Seq assemblies available for species of ticks which allowed to identify nine new genomes of iflaviruses. The phylogeny of virus sequences was not congruent with that of the tick hosts, suggesting recurrent host changes across tick genera along evolution. We identified five different variants with a complete or near-complete genome in Ixodes ricinus. These sequences were closely related, which allowed a fine-scale estimation of patterns of substitutions: we detected a strong excess of synonymous mutations suggesting evolution under strong positive selection. ISIV, a sequence found in the ISE6 cell line of Ixodes scapularis, was unexpectedly nearidentical with I. ricinus variants, suggesting a contamination of this cell line by I. ricinus material. Overall, our work constitutes a step in the understanding of the interactions between this family of viruses and ticks.

evolutionary biology↗

Relationships between landscape structure and the prevalence of two tick-borne infectious agents, Anaplasma phagocytophilum and Borrelia burgdorferi sensu lato, in small mammal communities

ContextBy modifying ecosystems, land cover changes influence the emergence, the spread and the incidence of vector-borne diseases. ObjectiveThis study aimed at identifying associations between landscape structure and the prevalence of two tick-borne infectious agents, Anaplasma phagocytophilum and Borrelia burgdorferi s.l., in small mammal communities. MethodsSmall mammals were sampled in 24 sites along a gradient of woodland fragmentation and hedgerow network density, and screened for infectious agents with real-time PCR techniques. For each site, structural variables (composition and configuration) of the surrounding landscape at various scales (0-500 m) and variables of wooded habitats connectivity based on graph theory and least cost path distances for the two dominant species, bank voles (Myodes glareolus) and wood mice (Apodemus sylvaticus), were computed. ResultsThe A. phagocytophilum prevalence increased with wooded habitats cover (0-500 m), likely through host population size, and increased slightly with bank vole abundance, which has a higher reservoir competence than wood mouse. The B. burgdorferi s.l. prevalence increased with wooded ecotones only at local scales (50-100 m). Wooded habitats connectivity measures did not improve models built with simple land cover variables. A more marked spatial pattern was observed for the prevalence of A. phagocytophilum than B. burgdorferi s.l.. ConclusionsThis study highlights the interest of considering together the ecology of infectious agents (e.g. host specificity) and the host species community ecology to better understand the influence of the landscape structure on the spatial distribution of vector-borne infectious agents.

ecology↗

Whole body transcriptomes and new insights into the biology of the tick Ixodes ricinus

BackgroundIxodes ricinus is the most important vector of tick-borne-diseases in Europe. A better knowledge of its genome and transcriptome is important for developing control strategies. Previous transcriptomic studies of I. ricinus have focused on gene expression during the blood meal in specific tissues. To obtain a broader picture of changes in gene expression during the blood meal, our study analysed the transcriptome at the level of the whole body for both nymphal and adult ticks. I. ricinus ticks from a highly inbred colony at the University of Neuchatel were used. We also analysed previously published RNAseq studies to compare the genetic variation between three wild strains and three lab strains, including the strain from Neuchatel.\n\nResultsRNA was extracted from whole tick bodies and the cDNA was sequenced, producing 162,872,698 paired-end reads. Our reference transcriptome contained 179,682 contigs, of which 31% were annotated using Trinotate. Gene expression was compared between ticks that differed with respect to stage (nymph, adult), sex (female, male), and feeding status (unfed, partially fed). We found that blood feeding in nymphs and female adult ticks increased the expression of cuticle-associated genes. Using a set of 5,422 single nucleotide polymorphisms to calculate the heterozygosity, we found that the wild tick populations of I. ricinus had much higher levels of heterozygosity than the three lab populations.\n\nConclusionUsing high throughput strand-oriented sequencing for whole ticks in different stages and feeding conditions, we obtained a de novo assembly that significantly increased the genomic resources available for I. ricinus. Our study illustrates the importance of analysing the transcriptome at the level of the whole body to gain additional insights into how gene expression changes over the life cycle of an organism. Our comparison of several RNAseq datasets shows the power of transcriptomic data to accurately characterize genetic polymorphism and for comparing different populations or sources of sequencing material.

genomics↗