Grappling with the tick microbiome

Abstract Background : Ixodes scapularis ticks harbor microbial communities including pathogenic and non-pathogenic microbes. Pathogen infection increases the expression of several tick gut proteins which disturb the tick gut microbiota and impact bacterial biofilm formation. Anaplasma phagocytophilum induces ticks to express I. scapularis IAFGP, a protein with antimicrobial activity while Borrelia burgdorferi induces the expression of PIXR. Here, we tested the resistance of I. scapularis microbiome to A. phagocytophilum infection, antimicrobial peptide IAFGP, and anti-tick immunity specific to PIXR. Results : We demonstrate that A. phagocytophilum infection and IAFGP affect the taxonomic composition and taxa co-occurrence networks but had no effect on the functional traits of tick microbiome. In contrast, anti-tick immunity disturbed the taxonomic composition and the functional profile of tick microbiome, by increasing both taxonomic and pathways diversity. Mechanistically, we show that anti-tick immunity increases the representation and importance of polysaccharide biosynthesis pathways involved in biofilm formation while these pathways are under-represented in the microbiome of ticks infected by A. phagocytophilum or exposed to IAFGP. Conclusions : These analyses revealed that tick microbiota is highly sensitive to anti-tick immunity, while it is less sensitive to pathogen infection and antimicrobial peptides. Results suggest that biofilm formation is a defensive response of tick microbiome to anti-tick immunity.

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Resistance of Tick Gut Microbiome to Anti-Tick Vaccines, Pathogen Infection and Antimicrobial Peptides

Pathogens ◽

10.3390/pathogens9040309 ◽

2020 ◽

Vol 9 (4) ◽

pp. 309 ◽

Cited By ~ 4

Author(s):

Agustín Estrada-Peña ◽

Alejandro Cabezas-Cruz ◽

Dasiel Obregón

Keyword(s):

Antimicrobial Peptides ◽

Biofilm Formation ◽

Ixodes Scapularis ◽

Taxonomic Composition ◽

Bacterial Biofilm ◽

Pathogen Infection ◽

Polysaccharide Biosynthesis ◽

Antifreeze Glycoprotein ◽

Highly Sensitive ◽

Tick Microbiome

Ixodes scapularis ticks harbor microbial communities including pathogenic and non-pathogenic microbes. Pathogen infection increases the expression of several tick gut proteins, which disturb the tick gut microbiota and impact bacterial biofilm formation. Anaplasma phagocytophilum induces ticks to express I. scapularis antifreeze glycoprotein (IAFGP), a protein with antimicrobial activity, while Borrelia burgdorferi induces the expression of PIXR. Here, we tested the resistance of I. scapularis microbiome to A. phagocytophilum infection, antimicrobial peptide IAFGP, and anti-tick immunity specific to PIXR. We demonstrate that A. phagocytophilum infection and IAFGP affect the taxonomic composition and taxa co-occurrence networks, but had limited impact on the functional traits of tick microbiome. In contrast, anti-tick immunity disturbed the taxonomic composition and the functional profile of tick microbiome, by increasing both the taxonomic and pathways diversity. Mechanistically, we show that anti-tick immunity increases the representation and importance of the polysaccharide biosynthesis pathways involved in biofilm formation, while these pathways are under-represented in the microbiome of ticks infected by A. phagocytophilum or exposed to IAFGP. These analyses revealed that tick microbiota is highly sensitive to anti-tick immunity, while it is less sensitive to pathogen infection and antimicrobial peptides. Results suggest that biofilm formation may be a defensive response of tick microbiome to anti-tick immunity.

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

10.1101/2021.03.15.435198 ◽

2021 ◽

Author(s):

Phineas T. Hamilton ◽

Elodie Maluenda ◽

Anouk Sarr ◽

Alessandro Belli ◽

Georgia Hurry ◽

...

Keyword(s):

Large Scale ◽

Vector Competence ◽

Bacterial Community Composition ◽

Blood Feeding ◽

Rodent Host ◽

Vector Borne Diseases ◽

Bacterial Microbiome ◽

Vector Borne ◽

Scale Experiment ◽

Tick Microbiome

AbstractBackgroundVector-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.

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Recently evolved Francisella-like endosymbiont outcompetes an ancient and evolutionarily associated Coxiella-like endosymbiont in the lone star tick (Amblyomma americanum) linked to the Alpha-Gal Syndrome

10.21203/rs.3.rs-856007/v1 ◽

2021 ◽

Author(s):

Deepak Kumar ◽

Surendra Raj Sharma ◽

Abdulsalam Adegoke ◽

Ashley Kennedy ◽

Holly C. Tuten ◽

...

Keyword(s):

Microbial Communities ◽

Developmental Stages ◽

The United States ◽

Amblyomma Americanum ◽

Strong Positive Correlation ◽

Metagenomic Sequencing ◽

Lone Star Tick ◽

Positive Correlation ◽

The Usa ◽

Tick Microbiome

Abstract BackgroundTicks are hematophagous arthropods that transmit various bacterial, viral, and protozoan pathogens of public health significance. The lone star tick (Amblyomma americanum) is an aggressive human-biting tick that transmits bacterial and viral pathogens, and its bites are suspected of eliciting the Alpha-Gal Syndrome, a newly emerged delayed hypersensitivity following consumption of red meat in the United States. While ongoing studies have attempted to investigate the contribution of different tick-inherent factors to the induction of Alpha-Gal syndrome, an otherwise understudied aspect is the contribution of the tick microbiome and specifically obligate endosymbionts to the establishment of the Alpha-Gal syndrome in humans.MethodsHere we utilized a high throughput metagenomic sequencing approach to cataloging the entire microbial communities residing within different developmental stages and tissues of unfed and blood-fed ticks from laboratory-maintained ticks and three new geographical locations in the USA. The quantitative insights into microbial ecology (QIIME2) pipeline were used to perform data analysis and taxonomic classification. Moreover, using a SparCC network construction model, we investigated potential interactions between members of the microbial communities from lab-maintained and field-collected ticks. ResultsOverall, Francisellaceae was the most dominant bacteria identified in the microbiome of both lab-raised and field-collected Am. americanum across all tissues and developmental stages. Likewise, microbial diversity was seen to be significantly higher in field-collected ticks compared to lab-maintained ticks as seen with a higher number of both OTUs and measures of species richness. Several potential positive and negative correlations were identified from our network analysis. We observed a strong positive correlation between Francisellaceae, Rickettsiaceae, and Midichloriaceae in both developmental stages and tissues from lab-maintained ticks, while ovarian tissues had a strong positive correlation of bacteria in the family Xanthobacteraceae and Rhizobiaceae. A negative interaction was observed between Coxiellaceae and Francisellaceae in Illinois, and all the bacteria detected from ticks from Delaware were negatively correlated.ConclusionThis study is the first to catalog the microbiome of Am. americanum throughout its developmental stages and different tissue niches and report the potential replacement of Coxiellaceae by Francisellaceae across developmental stages and tissues tested except in ovarian tissues. These unique and significant findings advance our knowledge and open a new avenue of research to further understand the role of tick microbiome in tick-borne diseases and develop a holistic strategy to control Alpha-Gal syndrome.

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Behind Taxonomic Variability: The Functional Redundancy in the Tick Microbiome

Microorganisms ◽

10.3390/microorganisms8111829 ◽

2020 ◽

Vol 8 (11) ◽

pp. 1829

Author(s):

Agustín Estrada-Peña ◽

Alejandro Cabezas-Cruz ◽

Dasiel Obregón

Keyword(s):

Metabolic Pathways ◽

Developmental Stages ◽

Sequence Data ◽

Ixodes Scapularis ◽

Functional Redundancy ◽

Taxonomic Composition ◽

Functional Similarity ◽

Data Set ◽

Taxonomic Profiling ◽

Tick Microbiome

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.

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Applications of Blocker Nucleic Acids and Non-Metazoan PCR Improves the Discovery of the Eukaryotic Microbiome in Ticks

Microorganisms ◽

10.3390/microorganisms9051051 ◽

2021 ◽

Vol 9 (5) ◽

pp. 1051

Author(s):

Yurie Taya ◽

Gohta Kinoshita ◽

Wessam Mohamed Ahmed Mohamed ◽

Mohamed Abdallah Mohamed Moustafa ◽

Shohei Ogata ◽

...

Keyword(s):

Nucleic Acids ◽

Alpha Diversity ◽

Illumina Miseq ◽

18S Rrna Gene ◽

Rrna Gene ◽

Miseq Platform ◽

Pcr Method ◽

Almost All ◽

Tick Microbiome ◽

Generation Sequencing

Ticks serve as important vectors of a variety of pathogens. Recently, the viral and prokaryotic microbiomes in ticks have been explored using next-generation sequencing to understand the physiology of ticks and their interactions with pathogens. However, analyses of eukaryotic communities in ticks are limited, owing to the lack of suitable methods. In this study, we developed new methods to selectively amplify microeukaryote genes in tick-derived DNA by blocking the amplification of the 18S rRNA gene of ticks using artificial nucleic acids: peptide nucleic acids (PNAs) and locked nucleic acids (LNAs). In addition, another PCR using non-metazoan primers, referred to as UNonMet-PCR, was performed for comparison. We performed each PCR using tick-derived DNA and sequenced the amplicons using the Illumina MiSeq platform. Almost all sequences obtained by conventional PCR were derived from ticks, whereas the proportion of microeukaryotic reads and alpha diversity increased upon using the newly developed method. Additionally, the PNA- or LNA-based methods were suitable for paneukaryotic analyses, whereas the UNonMet-PCR method was particularly sensitive to fungi. The newly described methods enable analyses of the eukaryotic microbiome in ticks. We expect the application of these methods to improve our understanding of the tick microbiome.

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Presence of Human Pathogens of the Borrelia burgdorferi sensu lato Complex Shifts the Sequence Read Abundances of Tick Microbiomes in Two German Locations

Microorganisms ◽

10.3390/microorganisms9091814 ◽

2021 ◽

Vol 9 (9) ◽

pp. 1814

Author(s):

Angeline Hoffmann ◽

Thomas Müller ◽

Volker Fingerle ◽

Matthias Noll

Keyword(s):

Nucleic Acid ◽

16S Rrna ◽

Borrelia Burgdorferi ◽

16S Rrna Gene ◽

Borrelia Burgdorferi Sensu Lato ◽

Rrna Gene ◽

Pathogenic Species ◽

Microbiome Composition ◽

Tick Microbiome ◽

Bacterial 16S Rrna Gene

The distribution of human Lyme borreliosis (LB) is assumed random in Germany, indicating that the human pathogenic species of the Borrelia burgdorferi sensu lato complex (Bb) are similarly distributed as part of the tick microbiome. The aim of this study was to differentiate if the presence of Bb occurs with a defined tick microbiome composition. Furthermore, the effect of location on tick microbiome composition was addressed for two German locations. Therefore, nucleic acid extracts from 82 Borrelia-positive and 118 Borrelia-negative Ixodes ricinus ticks sampled from human hosts in both districts were selected. Nucleic acid extracts were used for human pathogenic Bb species diagnostics based on qPCR and multilocus sequence typing (MLST) and bacterial 16S rRNA gene amplicon sequencing followed by network analyses. As a result, the presence of Bb shifted the sequence read abundances of Candidatus Midichloria, Rickettsia, Pseudomonas, Staphylococcus, and Candidatus Neoehrlichia and their topological roles in the tick microbiome. Moreover, the location was less important in the tick microbiome composition but shifted significantly sequence read abundances of Pseudomonas and Wolbachia as well as the topological role of microbial members. Since the presence of human pathogenic Bb species with other tick-associated pathogens varies regionally, we suggest that a bacterial 16S rRNA gene-based microbiome survey should be implemented in the routine diagnostics for both tick and host if human pathogenic species of Bb were detected. This diagnostic extension will help to optimize therapeutic approaches against Bb infection and co-occurring pathogens.

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Tick microbiome and pathogen acquisition altered by host blood meal

The ISME Journal ◽

10.1038/ismej.2016.152 ◽

2016 ◽

Vol 11 (3) ◽

pp. 813-816 ◽

Cited By ~ 55

Author(s):

Andrea Swei ◽

Jessica Y Kwan

Keyword(s):

Blood Meal ◽

Host Blood ◽

Tick Microbiome

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