Tick-Pathogen Ensembles: Do Molecular Interactions Lead Ecological Innovation?

Cabezas-Cruz, Alejandro; Estrada-Peña, Agustı́n; Rego, Ryan O. M.; Fuente, José de la

doi:10.3389/fcimb.2017.00074

Cited by 25 publications

(28 citation statements)

References 44 publications

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“…Several lines of evidence suggest that tick-pathogen associations evolved to form “ intimate epigenetic relationships ” that have the potential to increase tick fitness (Cabezas-Cruz et al, 2017). At the tick-pathogen interface, A. phagocytophilum induces an antifreeze glycoprotein (IAFGP) and heat shock proteins (HSPs) to increase tick survival and feeding fitness (Neelakanta et al, 2010; Busby et al, 2012).…”

Section: Biological Processes Involved In Tick-pathogen Interactionsmentioning

confidence: 99%

Tick-Pathogen Interactions and Vector Competence: Identification of Molecular Drivers for Tick-Borne Diseases

Fuente

Antunes

Bonnet

et al. 2017

Front. Cell. Infect. Microbiol.

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Ticks and the pathogens they transmit constitute a growing burden for human and animal health worldwide. Vector competence is a component of vectorial capacity and depends on genetic determinants affecting the ability of a vector to transmit a pathogen. These determinants affect traits such as tick-host-pathogen and susceptibility to pathogen infection. Therefore, the elucidation of the mechanisms involved in tick-pathogen interactions that affect vector competence is essential for the identification of molecular drivers for tick-borne diseases. In this review, we provide a comprehensive overview of tick-pathogen molecular interactions for bacteria, viruses, and protozoa affecting human and animal health. Additionally, the impact of tick microbiome on these interactions was considered. Results show that different pathogens evolved similar strategies such as manipulation of the immune response to infect vectors and facilitate multiplication and transmission. Furthermore, some of these strategies may be used by pathogens to infect both tick and mammalian hosts. Identification of interactions that promote tick survival, spread, and pathogen transmission provides the opportunity to disrupt these interactions and lead to a reduction in tick burden and the prevalence of tick-borne diseases. Targeting some of the similar mechanisms used by the pathogens for infection and transmission by ticks may assist in development of preventative strategies against multiple tick-borne diseases.

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Section: Biological Processes Involved In Tick-pathogen Interactionsmentioning

confidence: 99%

Tick-Pathogen Interactions and Vector Competence: Identification of Molecular Drivers for Tick-Borne Diseases

Fuente

Antunes

Bonnet

et al. 2017

Front. Cell. Infect. Microbiol.

Self Cite

353

272

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“…While the majority of metagenomic studies of disease vectors focus on bacterial communities, rather than eukaryotic microbes or viruses, there is still much to learn about the factors that affect bacterial community composition in arthropod vectors and how these microbial communities might impact pathogen transmission [7]. In addition to the obvious importance of pathogen occurrence, abundance, and genotypic diversity in disease vectors, there is increasing recognition that non-pathogenic microbes might affect acquisition and transmission of vector-borne pathogens [8,9]. For example, the presence of specific bacterial genera may inhibit the growth of pathogens, and some non-pathogenic bacteria may facilitate colonization by pathogens or affect vector behavior in ways that impact transmission dynamics [10,11].…”

Section: Introductionmentioning

confidence: 99%

“…For example, the presence of specific bacterial genera may inhibit the growth of pathogens, and some non-pathogenic bacteria may facilitate colonization by pathogens or affect vector behavior in ways that impact transmission dynamics [10,11]. In other cases, pathogen occurrence may enhance vector survival [12,13] and thus affect range expansion and abundance of such vectors in the environment [9,14,15].…”

Section: Introductionmentioning

confidence: 99%

Factors affecting the microbiome of Ixodes scapularis and Amblyomma americanum

et al. 2020

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The microbial community composition of disease vectors can impact pathogen establishment and transmission as well as on vector behavior and fitness. While data on vector microbiota are accumulating quickly, determinants of the variation in disease vector microbial communities are incompletely understood. We explored the microbiome of two humanbiting tick species abundant in eastern North America (Amblyomma americanum and Ixodes scapularis) to identify the relative contribution of tick species, tick life stage, tick sex, environmental context and vertical transmission to the richness, diversity, and species composition of the tick microbiome. We sampled 89 adult and nymphal Ixodes scapularis (N = 49) and Amblyomma americanum (N = 40) from two field sites and characterized the microbiome of each individual using the v3-v4 hypervariable region of the 16S rRNA gene. We identified significant variation in microbial community composition due to tick species and life stage with lesser impact of sampling site. Compared to unfed nymphs and males, the microbiome of engorged adult female I. scapularis, as well as the egg masses they produced, were low in bacterial richness and diversity and were dominated by Rickettsia, suggesting strong vertical transmission of this genus. Likewise, microbiota of A. americanum nymphs and males were more diverse than those of adult females. Among bacteria of public health importance, we detected several different Rickettsia sequence types, several of which were distinct from known species. Borrelia was relatively common in I. scapularis but did not show the same level of sequence variation as Rickettsia. Several bacterial genera were significantly over-represented in Borrelia-infected I. scapularis, suggesting a potential interaction of facilitative relationship between these taxa; no OTUs were under-represented in Borrelia-infected ticks. The systematic sampling we conducted for this study allowed us to partition the variation in tick microbial composition as a function of tick-and environmentallyrelated factors. Upon more complete understanding of the forces that shape the tick microbiome it will be possible to design targeted experimental studies to test the impacts of individual taxa and suites of microbes on vector-borne pathogen transmission and on vector biology.

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“…In the case of vector-borne bacteria, such as A. phagocytophilum , a solely-competition-based mechanism does not explain how this vector-pathogen ensemble is kept during evolution. Therefore, alternative models of vector-pathogen interaction, where both partners benefit from the association, should be explored (de la Fuente et al, 2016b ; Cabezas-Cruz et al, 2017c ).…”

Section: Introductionmentioning

confidence: 99%

Ixodes scapularis Tick Cells Control Anaplasma phagocytophilum Infection by Increasing the Synthesis of Phosphoenolpyruvate from Tyrosine

Cabezas-Cruz

Espinosa

Obregón

et al. 2017

Front. Cell. Infect. Microbiol.

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The obligate intracellular pathogen, Anaplasma phagocytophilum, is the causative agent of life-threatening diseases in humans and animals. A. phagocytophilum is an emerging tick-borne pathogen in the United States, Europe, Africa and Asia, with increasing numbers of infected people and animals every year. It is increasingly recognized that intracellular pathogens modify host cell metabolic pathways to increase infection and transmission in both vertebrate and invertebrate hosts. Recent reports have shown that amino acids are central to the host–pathogen metabolic interaction. In this study, a genome-wide search for components of amino acid metabolic pathways was performed in Ixodes scapularis, the main tick vector of A. phagocytophilum in the United States, for which the genome was recently published. The enzymes involved in the synthesis and degradation pathways of the twenty amino acids were identified. Then, the available transcriptomics and proteomics data was used to characterize the mRNA and protein levels of I. scapularis amino acid metabolic pathway components in response to A. phagocytophilum infection of tick tissues and ISE6 tick cells. Our analysis was focused on the interplay between carbohydrate and amino acid metabolism during A. phagocytophilum infection in ISE6 cells. The results showed that tick cells increase the synthesis of phosphoenolpyruvate (PEP) from tyrosine to control A. phagocytophilum infection. Metabolic pathway analysis suggested that this is achieved by (i) increasing the transcript and protein levels of mitochondrial phosphoenolpyruvate carboxykinase (PEPCK-M), (ii) shunting tyrosine into the tricarboxylic acid (TCA) cycle to increase fumarate and oxaloacetate which will be converted into PEP by PEPCK-M, and (iii) blocking all the pathways that use PEP downstream gluconeogenesis (i.e., de novo serine synthesis pathway (SSP), glyceroneogenesis and gluconeogenesis). While sequestering host PEP may be critical for this bacterium because it cannot actively carry out glycolysis to produce PEP, excess of this metabolite may be toxic for A. phagocytophilum. The present work provides a more comprehensive view of the major amino acid metabolic pathways involved in the response to pathogen infection in ticks, and provides the basis for further studies to develop novel strategies for the control of granulocytic anaplasmosis.

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Tick-Pathogen Ensembles: Do Molecular Interactions Lead Ecological Innovation?

Cited by 25 publications

References 44 publications

Tick-Pathogen Interactions and Vector Competence: Identification of Molecular Drivers for Tick-Borne Diseases

Tick-Pathogen Interactions and Vector Competence: Identification of Molecular Drivers for Tick-Borne Diseases

Factors affecting the microbiome of Ixodes scapularis and Amblyomma americanum

Ixodes scapularis Tick Cells Control Anaplasma phagocytophilum Infection by Increasing the Synthesis of Phosphoenolpyruvate from Tyrosine

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