Dataset Information

Early Transcriptional Changes in the Midgut of Ornithodoros moubata after Feeding and Infection with Borrelia duttonii.

ABSTRACT: Studies on tick-pathogen-host interactions are helping to identify candidates for vaccines against ticks and tick-borne diseases and to discover potent bioactive tick molecules. The tick midgut is the main tissue involved in blood feeding and, moreover, the first organ to have contact with pathogens ingested through the blood meal. As little is known about the molecular biology of feeding and tick defence mechanisms against microorganisms, but important for understanding vector-pathogen interactions, we explored the early transcriptional changes in the midgut of Ornithodoros moubata after feeding and in response to challenge with the relapsing-fever spirochete Borrelia duttonii using the Ion S5XL platform. Besides transcripts with metabolic function and immune-related transcripts we discovered numerous putative and uncharacterized protein sequences. Overall, our analyses support previous studies and provides a valuable reference database for further functional proteomic analysis of midgut proteins of O. moubata.

SUBMITTER: Schafer M

PROVIDER: S-EPMC8948914 | biostudies-literature | 2022 Feb

REPOSITORIES: biostudies-literature

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Early Transcriptional Changes in the Midgut of <i>Ornithodoros moubata</i> after Feeding and Infection with <i>Borrelia duttonii</i>.

Schäfer Mandy M Pfaff Florian F Höper Dirk D Silaghi Cornelia C

Microorganisms 20220228 3

Studies on tick-pathogen-host interactions are helping to identify candidates for vaccines against ticks and tick-borne diseases and to discover potent bioactive tick molecules. The tick midgut is the main tissue involved in blood feeding and, moreover, the first organ to have contact with pathogens ingested through the blood meal. As little is known about the molecular biology of feeding and tick defence mechanisms against microorganisms, but important for understanding vector-pathogen interact ...[more]

PMID: 35336101

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Project description:IntroductionOrnithodoros erraticus and Ornithodoros moubata are the main vectors of African swine fever virus (ASFV) and the human relapsing fever spirochetes Borrelia hispanica and Borrelia crocidurae in the Mediterranean region and Borrelia duttoni in continental Africa. Manipulation of the tick microbiome has been shown to reduce vector fitness and competence in tick vectors, suggesting that the identification of key microbial players associated with tick tissues can inform interventions such as anti-microbiota vaccines to block pathogen development in the midgut and/or salivary glands.MethodsIn this study, we analyzed and compared the microbiome of the salivary glands and midgut of O. erraticus and O. moubata. For the taxonomic and functional characterization of the tissue-specific microbiome, we used 16S rRNA amplicon sequencing and prediction of metabolic profiles using PICRUSt2. Co-occurrence networks were built to characterize the community assembly and identify keystone taxa in each tick species.ResultsOur results revealed differences in the composition, diversity, and assembly of the bacterial microbiome of salivary glands and midgut within each tick species, but differences were more noticeable in O. moubata. Differences were also found in the microbiome of each tissue, salivary gland and midgut, between species. However, the 'Core Association Networks (CAN)' analysis revealed conserved patterns of interacting taxa in tissues within and between tick species. Different keystone taxa were identified in O. erraticus and O. moubata tissues, but Muribaculaceae and Alistipes were found as keystone taxa in the salivary glands of both tick species which justifies their use as anti-microbiota vaccine candidates to alter the microbiome and reduce tick fitness and/or block pathogen transmission. The high similarity of predicted metabolic pathways profiles between tissues of the two tick species suggests that taxonomic variability of the microbiome is not associated with significant changes in microbial functional profiles.ConclusionWe conclude that the taxonomic structure of the microbiome in O. erraticus and O. moubata is tissue-specific, suggesting niche partitioning of bacterial communities associated to these soft ticks. However, shared keystone taxa and conserved patterns of interacting taxa between tissues and tick species suggest the presence of key microbial players that could be used as anti-microbiota vaccine candidates to affect tick physiology and/or pathogen colonization.

Project description:BackgroundThe argasid tick Ornithodoros moubata is the main African vector of the human relapsing fever agent Borrelia duttoni and the African swine fever virus. Together with saliva, the tick midgut forms part of the host-tick-pathogen interface, and numerous midgut proteins play key functions in the blood digestion-related process and the infection and transmission of pathogens. This work explores the composition of the midgut proteome of unfed and fed O. moubata females with the aim to complete the biological information already obtained from the midgut transcriptome and provide a more robust and comprehensive perspective of this biological system.MethodsMidgut tissues taken from females before feeding and 48 h after feeding were subjected to LC/MS-MS analysis. After functional characterization and classification of the proteins identified, the differences in the proteome between unfed and fed females were analysed and discussed. Additionally, a detailed analysis of particular groups of proteins that are involved in the processes of nutrient digestion and responses to the oxidative stress was carried out.Results1491 non-redundant tick proteins were identified: 1132 of them in the midgut of unfed ticks, 1138 in the midgut of fed ticks, and up to 779 shared by both physiological conditions. Overall, the comparative analysis of the midgut proteomes of O. moubata females before and after feeding did not reveal great differences in the number or class of proteins expressed, enzymatic composition or functional classification.ConclusionsThe hemoglobinolytic system in ixodids and argasids is very similar in spite of the fact that they display very different feeding and reproductive strategies. Although the main source of nutrients in ticks are proteins, lipids and carbohydrates also constitute significant nutritional sources and play an important part in the process of blood digestion. The genes and proteins involved in intracellular transport mechanisms, defensive responses, detoxifying responses and stress responses seem to be closely regulated, highlighting the complexity and importance of these processes in tick biology, which in turn assigns them a great interest as targets for therapeutic and immunological interventions.

Dataset Information

Early Transcriptional Changes in the Midgut of Ornithodoros moubata after Feeding and Infection with Borrelia duttonii.

Publications

Early Transcriptional Changes in the Midgut of <i>Ornithodoros moubata</i> after Feeding and Infection with <i>Borrelia duttonii</i>.

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