Dataset Information

Functional Redundancy and Ecological Innovation Shape the Circulation of Tick-Transmitted Pathogens.

ABSTRACT: Ticks are vectors of pathogens affecting human and animal health worldwide. Nevertheless, the ecological and evolutionary interactions between ticks, hosts, and pathogens are largely unknown. Here, we integrated a framework to evaluate the associations of the tick Ixodes ricinus with its hosts and environmental niches that impact pathogen circulation. The analysis of tick-hosts association suggested that mammals and lizards were the ancestral hosts of this tick species, and that a leap to Aves occurred around 120 M years ago. The signature of the environmental variables over the host's phylogeny revealed the existence of two clades of vertebrates diverging along a temperature and vegetation split. This is a robust proof that the tick probably experienced a colonization of new niches by adapting to a large set of new hosts, Aves. Interestingly, the colonization of Aves as hosts did not increase significantly the ecological niche of I. ricinus, but remarkably Aves are super-spreaders of pathogens. The disparate contribution of Aves to the tick-host-pathogen networks revealed that I. ricinus evolved to maximize habitat overlap with some hosts that are super-spreaders of pathogens. These results supported the hypothesis that large host networks are not a requirement of tick survival but pathogen circulation. The biological cost of tick adaptation to non-optimal environmental conditions might be balanced by molecular mechanisms triggered by the pathogens that we have only begun to understand.

SUBMITTER: Estrada-Pena A

PROVIDER: S-EPMC5450623 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Functional Redundancy and Ecological Innovation Shape the Circulation of Tick-Transmitted Pathogens.

Estrada-Peña Agustín A de la Fuente José J Cabezas-Cruz Alejandro A

Frontiers in cellular and infection microbiology 20170531

Ticks are vectors of pathogens affecting human and animal health worldwide. Nevertheless, the ecological and evolutionary interactions between ticks, hosts, and pathogens are largely unknown. Here, we integrated a framework to evaluate the associations of the tick <i>Ixodes ricinus</i> with its hosts and environmental niches that impact pathogen circulation. The analysis of tick-hosts association suggested that mammals and lizards were the ancestral hosts of this tick species, and that a leap to ...[more]

PMID: 28620590

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Project description:Ticks are blood-feeding arthropods and transmit a variety of medically important viral, bacterial, protozoan pathogens to animals and humans. Ticks also harbor a diverse community of microbes linked to their biological processes, such as hematophagy, and hence affect vector competence. The interactions between bacterial and/or protozoan pathogens and the tick microbiome is a black-box, and therefore we tested the hypothesis that the presence of a protozoan or bacterial pathogen will alter the microbial composition within a tick. Hence, this study was designed to define the microbial composition of two tick species, Hyalomma (H.) anatolicum and Rhipicephalus (R.) microplus. We used a combination of PCR based pathogen (Anaplasma marginale and Theileria species) and symbiont (Wolbachia species) identification followed by metagenomic sequencing and comparison of the microbial communities in PCR positive and negative ticks. A total of 1786 operational taxonomic units was identified representing 25 phyla, 50 classes, and 342 genera. The phylum Proteobacteria, Firmicutes, Actinobacteriota, and Bacteroidota were the most represented bacteria group. Alpha and beta diversity were not significantly affected in the presence or absence of Theileria sp. and A. marginale as see with H. anatolicum ticks. Interestingly, bacterial communities were significantly reduced in Theileria sp. infected R. microplus ticks, while also exhibiting a significant reduction in microbial richness and evenness. Putting these observations together, we referred to the effect the presence of Theileria sp. has on R. microplus a "pathogen-induced dysbiosis". We also identify the presence of Plasmodium falciparum, the causative agent of human malaria from the microbiome of both H. anatolicum and R. microplus ticks. These findings support the presence of a "pathogen-induced dysbiosis" within the tick and further validation experiments are required to investigate how they are important in the vector competence of ticks. Understanding the mechanism of "pathogen-induced dysbiosis" on tick microbial composition may aid the discovery of intervention strategies for the control of emerging tick-borne infections.

Project description:Ticks, pathogens, and vertebrates interact in a background of environmental features that regulate the densities of ticks and vertebrates, affecting their contact rates and thence the circulation of the pathogens. Regional scale studies are invaluable sources of information about the regulation of these interactions, but a large-scale analysis of the interaction of communities of ticks, hosts, and the environment has been never modeled. This study builds on network analysis, satellite-derived climate and vegetation, and environmental modeling, quantifying the interactions between the tick Ixodes ricinus and the transmitted bacteria of the complex Borrelia burgdorferi s.l. in the Western Palaearctic. We derived the rates of contact of the tick with 162 species of vertebrates recorded as hosts, and the relative importance of each vertebrate in the circulation of the pathogen. We compiled more than 11 millions of pairs of coordinates of the vertebrates, deriving distribution models of each species and the relative faunal composition in the target territory. The results of the modeling of the distribution of the tick and its hosts, weighted by their importance in the circulation of Borrelia captured the spatial patterns of interactions that allow the circulation of the pathogen. Results indicate that both I. ricinus and B. burgdorferi s.l. are supported in the Western Palaearctic by complex communities of vertebrates, which have large distribution ranges. This high functional redundancy results in the pervasiveness of B. burgdorferi s.l., which depends on the gradient of contributions of the large community of vertebrates, instead of relying on a few dominant vertebrates, which was the prevailing paradigm. Most prominent reservoirs of the pathogen are distributed in specific regions of the environmental niche. However, literally dozens of potential reservoirs can colonize many other environmental regions, marginally but efficiently contributing to the circulation of the pathogen. These results consistently point to the need of evaluating the beta-diversity of the community of vertebrates acting as reservoirs of the pathogen to better know the interactions with the vector. They also demonstrate why the pathogen is so resilient to perturbations in the composition of the reservoirs.

Project description:The taxonomic composition and diversity of tick midgut microbiota have been extensively studied in different species of the genera Rhipicephalus, Ixodes, Amblyomma, Haemaphysalis, Hyalomma, Dermacentor, Argas and Ornithodoros, while the functional significance of bacterial diversity has been proportionally less explored. In this study, we used previously published 16S amplicon sequence data sets from three Ixodes scapularis cohorts, two of uninfected nymphs, and one of larvae experimentally infected with Borrelia burgdorferi, to test the functional redundancy of the tick microbiome. We predicted the metabolic profiling of each sample using the state-of-the-art metagenomics tool PICRUSt2. The results showed that the microbiomes of all I. scapularis samples share only 80 taxa (24.6%, total 324), while out of the 342 metabolic pathways predicted, 82.7%, were shared by all the ticks. Borrelia-infected larvae lack 15.4% of pathways found in the microbiome of uninfected nymphs. Taxa contribution analysis showed that the functional microbiome of uninfected ticks was highly redundant, with, in some cases, up to 198 bacterial taxa contributing to a single pathway. However, Borrelia-infected larvae had a smaller redundancy with 6.7% of pathways provided by more than 100 genera, while 15.7-19.2% of pathways were provided by more than 100 genera in the two cohorts of uninfected ticks. In addition, we compared the functional profiles of three microbial communities from each data set, identified through a network-based approach, and we observed functional similarity between them. Based on the functional redundancy and functional similarity of the microbiome of ticks in different developmental stages and infection status, we concluded that the tick gut microbiota is a self-regulating community of very diverse bacteria contributing to a defined set of metabolic pathways and functions with yet unexplored relevance for tick fitness and/or bacterial community stability. We propose a change of focus in which the tick microbiome must be analyzed in all dimensions, highlighting their functional traits, instead of the conventional taxonomic profiling.

Project description:BACKGROUND: Canine babesiosis caused by Babesia rossi, transmitted by Haemaphysalis elliptica in South Africa, has also been reported from Nigeria. Although H. leachi (sensu lato) is widespread in sub-Saharan Africa, published literature on the occurrence of canine babesiosis is meagre. It has been postulated that the genotype of Babesia rossi Erythrocyte Membrane Antigen 1 (BrEMA1) may be linked to virulence of the specific isolate. The primary objective of this study was to detect and characterise tick-borne pathogens in dogs presented to a veterinary hospital using molecular techniques. In B. rossi-positive specimens, we aimed to determine whether the BrEMA1 gene occurred and to compare genotypes with those found in other isolates. Lastly, we wished to identify the tick species that were recovered from the sampled dogs. METHODS: Blood specimens (n = 100) were collected during January to March 2010 from domestic dogs presented at an animal hospital in Jos, Plateau State, Nigeria. They were screened for the presence of Babesia/Theileria and Ehrlichia/Anaplasma genomic DNA using PCR and Reverse Line Blot (RLB) assays. Positive B. rossi specimens were tested for the presence of the BrEMA1gene using an RT-PCR. In addition, ticks were collected from dogs found to be infested during sampling. RESULTS: On RLB, 72 (72%) of the specimens were positive for one or more haemoparasites. Of the positive specimens, 38 (53%) were infected with B. rossi; 9 (13%) with Theileria sp. (sable); 5 (7%) with either Ehrlichia canis or Anaplasma sp. Omatjenne, respectively; 3 (4%) with Theileria equi; and 1 (1%) with B. vogeli and E. ruminantium, respectively. Co-infections were detected in 13 (18%) of the specimens. Results of RT-PCR screening for the BrEMA1 gene were negative. A total of 146 ticks belonging to 8 species were collected and identified: Rhipicephalus sanguineus 107 (73%), Haemaphysalis leachi (sensu stricto) 27 (18%), R. turanicus 3 (2%), and Amblyomma variegatum, H. elliptica, R. lunulatus, R. muhsamae and R. senegalensis 1 (1%), respectively. CONCLUSIONS: Up to 8 tick-borne pathogens possibly occur in the dog population at Jos, with B. rossi being the most prevalent. The absence of the BrEMA1 gene suggests that B. rossi occurring in that area may be less virulent than South African isolates.

Project description:When facing environmental change and intensified anthropogenic impact on marine ecosystems, extensive knowledge of how these systems are functioning is required in order to manage them properly. However, in high-latitude ecosystems, where climate change is expected to have substantial ecological impact, the ecosystem functions of biological species have received little attention, partly due to the limited biological knowledge of Arctic species. Functional traits address the ecosystem functions of member species, allowing the functionality of communities to be characterised and the degree of functional redundancy to be assessed. Ecosystems with higher functional redundancy are expected to be less affected by species loss, and therefore less sensitive to disturbance. Here we highlight and compare typical functional characteristics of Arctic and boreal fish in the Barents Sea and address the consequences of a community-wide reorganization driven by climate warming on functional redundancy and characterization. Based on trait and fish community composition data, we assessed functional redundancy of the Barents Sea fish community for the period 2004-2012, a period during which this northern region was characterized by rapidly warming water masses and declining sea ice coverage. We identified six functional groups, with distinct spatial distributions, that collectively provide a functional characterization of Barents Sea fish. The functional groups displayed different prevalence in boreal and Arctic water masses. Some functional groups displayed a spatial expansion towards the northeast during the study period, whereas other groups showed a general decline in functional redundancy. Presently, the observed patterns of functional redundancy would seem to provide sufficient scope for buffering against local loss in functional diversity only for the more speciose functional groups. Furthermore, the observed functional reconfiguration may affect future ecosystem functioning in the area. In a period of rapid environmental change, monitoring programs integrating functional traits will help inform management on ecosystem functioning and vulnerability.

Project description:BackgroundTick-borne diseases (TBDs) constitute a major constraint for livestock development in sub-Saharan Africa, with East Coast fever (ECF) being the most devastating TBD of cattle. However, in Burundi, detailed information is lacking on the current prevalence of TBDs and on the associated economic losses from mortality and morbidity in cattle as well as the costs associated with TBD control and treatment. The aim of this study was, therefore, to assess the prevalence and spatial distribution of tick-borne pathogens (TBPs) in cattle across the major agro-ecological zones (AEZs) in Burundi.MethodsIn a cross-sectional study conducted in ten communes spanning the five main AEZs in Burundi, blood samples were taken from 828 cattle from 305 farms between October and December 2017. Evidence of Theileria parva infection was assessed by antibody level, measured using a polymorphic immunodominant molecule (PIM) antigen-based enzyme-linked immunosorbent assay (ELISA) and by a T. parva-specific p104 gene-based nested PCR. Antibodies against Theileria mutans infection were detected using the 32-kDa antigen-based indirect ELISA, while the 200-kDa antigen and the major surface protein 5 (MSP5)-based indirect ELISA were used to detect antibodies against Babesia bigemina and Anaplasma marginale, respectively.ResultsThe prevalence of T. parva across the ten communes sampled ranged from 77.5 to 93.1% and from 67.8 to 90.0% based on the ELISA and PCR analysis, respectively. A statistically significant difference in infection was observed between calves and adult cattle; however, T. parva infection levels were not significantly associated with sex and breed. The seroprevalence indicating exposure to T. mutans, B. bigemina and A. marginale ranged from 30 to 92.1%, 33.7 to 90% and 50 to 96.2%, respectively. Mixed infections of TBPs were detected in 82.91% of cattle sampled, with 11 different combinations of pathogen species detected .ConclusionsThe findings indicate that T. parva, A. marginale and B. bigemina infections are endemic in Burundi. Knowledge of the spatial distribution of TBPs will facilitate the design of effective targeted strategies to control these diseases. There is a need for further investigations of the distribution of tick vectors and the population structure of TBPs in order to identify the key epidemiological factors contributing to TBD outbreaks in Burundi.

Dataset Information

Functional Redundancy and Ecological Innovation Shape the Circulation of Tick-Transmitted Pathogens.

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Functional Redundancy and Ecological Innovation Shape the Circulation of Tick-Transmitted Pathogens.

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