Dataset Information

The transcriptome of the lone star tick, Amblyomma americanum, reveals molecular changes in response to infection with the pathogen, Ehrlichia chaffeensis.

ABSTRACT: The lone star tick, Amblyomma americanum, is an obligatory ectoparasite of many vertebrates and the primary vector of Ehrlichia chaffeensis, the causative agent of human monocytic ehrlichiosis. This study aimed to investigate the comparative transcriptomes of A. americanum underlying the processes of pathogen acquisition and of immunity towards the pathogen. Differential expression of the whole body transcripts in six different treatments were compared: females and males that were E. chaffeensis non-exposed, E. chaffeensis-exposed/uninfected, and E. chaffeensis-exposed/infected. The Trinity assembly pipeline produced 140,574 transcripts from trimmed and filtered total raw sequence reads (approximately 117M reads). The gold transcript set of the transcriptome data was established to minimize noise by retaining only transcripts homologous to official peptide sets of Ixodes scapularis and A. americanum ESTs and transcripts covered with high enough frequency from the raw data. Comparison of the gene ontology term enrichment analyses for the six groups tested here revealed an up-regulation of genes for defense responses against the pathogen and for the supply of intracellular Ca⁺⁺ for pathogen proliferation in the pathogen-exposed ticks. Analyses of differential expression, focused on functional subcategories including immune, sialome, neuropeptides, and G protein-coupled receptor, revealed that E. chaffeensis-exposed ticks exhibited an upregulation of transcripts involved in the immune deficiency (IMD) pathway, antimicrobial peptides, Kunitz, an insulin-like peptide, and bursicon receptor over unexposed ones, while transcripts for metalloprotease were down-regulated in general. This study found that ticks exhibit enhanced expression of genes responsible for defense against E. chaffeensis.

SUBMITTER: Kim D

PROVIDER: S-EPMC8312692 | biostudies-literature | 2018 Sep

REPOSITORIES: biostudies-literature

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The transcriptome of the lone star tick, Amblyomma americanum, reveals molecular changes in response to infection with the pathogen, Ehrlichia chaffeensis.

Kim Donghun D Jaworski Deborah C DC Cheng Chuanmin C Nair Arathy D S ADS Ganta Roman R RR Herndon Nic N Brown Susan S Park Yoonseong Y

Journal of Asia-Pacific entomology 20180522 3

The lone star tick, Amblyomma americanum, is an obligatory ectoparasite of many vertebrates and the primary vector of Ehrlichia chaffeensis, the causative agent of human monocytic ehrlichiosis. This study aimed to investigate the comparative transcriptomes of A. americanum underlying the processes of pathogen acquisition and of immunity towards the pathogen. Differential expression of the whole body transcripts in six different treatments were compared: females and males tha ...[more]

PMID: 34316264

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Project description:The Lone Star tick, Amblyomma americanum, transmits several bacterial pathogens including species of Anaplasma and Ehrlichia. Amblyomma americanum also hosts a number of non-pathogenic bacterial endosymbionts. Recent studies of other arthropod and insect vectors have documented that commensal microflora can influence transmission of vector-borne pathogens; however, little is known about tick microbiomes and their possible influence on tick-borne diseases. Our objective was to compare bacterial communities associated with A. americanum, comparing Anaplasma/Ehrlichia -infected and uninfected ticks. Field-collected questing specimens (n = 50) were used in the analyses, of which 17 were identified as Anaplasma/Ehrlichia infected based on PCR amplification and sequencing of groEL genes. Bacterial communities from each specimen were characterized using Illumina sequencing of 16S rRNA gene amplicon libraries. There was a broad range in diversity between samples, with inverse Simpson's Diversity indices ranging from 1.28-89.5. There were no statistical differences in the overall microbial community structure between PCR diagnosed Anaplasma/Ehrlichia-positive and negative ticks, but there were differences based on collection method (P < 0.05), collection site (P < 0.05), and sex (P < 0.1) suggesting that environmental factors may structure A. americanum microbiomes. Interestingly, there was not always agreement between Illumina sequencing and PCR diagnostics: Ehrlichia was identified in 16S rRNA gene libraries from three PCR-negative specimens; conversely, Ehrlichia was not found in libraries of six PCR-positive ticks. Illumina sequencing also helped identify co-infections, for example, one specimen had both Ehrlichia and Anaplasma. Other taxa of interest in these specimens included Coxiella, Borrelia, and Rickettsia. Identification of bacterial community differences between specimens of a single tick species from a single geographical site indicates that intra-species differences in microbiomes were not due solely to pathogen presence/absence, but may be also driven by vector life history factors, including environment, life stage, population structure, and host choice.

Project description:BackgroundGenomic resources within the phylum Arthropoda are largely limited to the true insects but are beginning to include unexplored subphyla, such as the Crustacea and Chelicerata. Investigations of these understudied taxa uncover high frequencies of orphan genes, which lack detectable sequence homology to genes in pre-existing databases. The ticks (Acari: Chelicerata) are one such understudied taxon for which genomic resources are urgently needed. Ticks are obligate blood-feeders that vector major diseases of humans, domesticated animals, and wildlife. In analyzing a transcriptome of the lone star tick Amblyomma americanum, one of the most abundant disease vectors in the United States, we find a high representation of unannotated sequences. We apply a general framework for quantifying the origin and true representation of unannotated sequences in a dataset and for evaluating the biological significance of orphan genes.ResultsExpressed sequence tags (ESTs) were derived from different life stages and populations of A. americanum and combined with ESTs available from GenBank to produce 14,310 ESTs, over twice the number previously available. The vast majority (71%) has no sequence homology to proteins archived in UniProtKB. We show that poor sequence or assembly quality is not a major contributor to this high representation by orphan genes. Moreover, most unannotated sequences are functional: a microarray experiment demonstrates that 59% of functional ESTs are unannotated. Lastly, we attempt to further annotate our EST dataset using genomic datasets from other members of the Acari, including Ixodes scapularis, four other tick species and the mite Tetranychus urticae. We find low homology with these species, consistent with significant divergence within this subclass.ConclusionsWe conclude that the abundance of orphan genes in A. americanum likely results from 1) taxonomic isolation stemming from divergence within the tick lineage and limited genomic resources for ticks and 2) lineage-specific genes needing functional genomic studies to evaluate their association with the unique biology of ticks. The EST sequences described here will contribute substantially to the development of tick genomics. Moreover, the framework provided for the evaluation of orphan genes can guide analyses of future transcriptome sequencing projects.

Project description:IntroductionThe lone star tick, Amblyomma americanum, is an important ectoparasite known for transmitting diseases to humans and animals. Ecdysis-related neuropeptides (ERNs) control behaviors crucial for arthropods to shed exoskeletons. However, ERN identification and characterization in A. americanum remain incomplete.MethodsWe investigated ERNs in A. americanum, assessing their evolutionary relationships, protein properties, and functions. Phylogeny, sequence alignment, and domain structures of ERNs were analyzed. ERN functionality was explored using enrichment analysis, and developmental and tissue-specific ERN expression profiles were examined using qPCR and RNAi experiments.Results and discussionThe study shows that ERN catalogs (i.e., eclosion hormone, corazonin, and bursicon) are found in most arachnids, and these ERNs in A. americanum have high evolutionary relatedness with other tick species. Protein modeling analysis indicates that ERNs primarily consist of secondary structures and protein stabilizing forces (i.e., hydrophobic clusters, hydrogen bond networks, and salt bridges). Gene functional analysis shows that ENRs are involved in many ecdysis-related functions, including ecdysis-triggering hormone activity, neuropeptide signaling pathway, and corazonin receptor binding. Bursicon proteins have functions in chitin binding and G protein-coupled receptor activity and strong interactions with leucine-rich repeat-containing G-protein coupled receptor 5. ERNs were expressed in higher levels in newly molted adults and synganglia. RNAi-mediated knockdown of burs α and burs β expression led to a significant decrease in the expression of an antimicrobial peptide, defensin, suggesting they might act in signaling or regulatory pathways that control the expression of immune-related genes. Arthropods are vulnerable immediately after molting because new cuticles are soft and susceptible to injury and pathogen infections. Bursicon homodimers act in prophylactic immunity during this vulnerable period by increasing the synthesis of transcripts encoding antimicrobial peptides to protect them from microbial invasion. Collectively, the expression pattern and characterization of ERNs in this study contribute to a deeper understanding of the physiological processes in A. americanum.

Dataset Information

The transcriptome of the lone star tick, Amblyomma americanum, reveals molecular changes in response to infection with the pathogen, Ehrlichia chaffeensis.

Publications

The transcriptome of the lone star tick, <i>Amblyomma americanum</i>, reveals molecular changes in response to infection with the pathogen, <i>Ehrlichia chaffeensis</i>.

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