Ana Laura Cano-Argüelles, Elianne Piloto-Sardiñas, Apolline Maitre, Lourdes Mateos-Hernández, Jennifer Maye, Alejandra Wu-Chuang, Lianet Abuin-Denis, Dasiel Obregón, Timothy Bamgbose, Ana Oleaga, Alejandro Cabezas-Cruz, Ricardo Pérez-Sánchez
{"title":"Microbiota-driven vaccination in soft ticks: Implications for survival, fitness and reproductive capabilities in Ornithodoros moubata","authors":"Ana Laura Cano-Argüelles, Elianne Piloto-Sardiñas, Apolline Maitre, Lourdes Mateos-Hernández, Jennifer Maye, Alejandra Wu-Chuang, Lianet Abuin-Denis, Dasiel Obregón, Timothy Bamgbose, Ana Oleaga, Alejandro Cabezas-Cruz, Ricardo Pérez-Sánchez","doi":"10.1111/mec.17506","DOIUrl":null,"url":null,"abstract":"<p>The <i>Ornithodoros moubata</i> (Om) soft tick, a vector for diseases like tick-borne human relapsing fever and African swine fever, poses challenges to conventional control methods. With diminishing insecticide efficacy, harnessing the tick's microbiota through innovative approaches like microbiota-driven vaccination emerges as a promising strategy for sustainable and targeted disease control. This study investigated the intricate relationship between <i>Pseudomonas</i>, a keystone taxon in the Om microbiome, and its impact on tick fitness, microbiome structure and network dynamics. Utilizing in silico analyses and empirical vaccination experiments, the role of <i>Pseudomonas</i> within microbial networks in the tick midguts (MG) and salivary glands (SG) of Om was studied. Additionally, the consequences of anti-microbiota vaccines targeting <i>Pseudomonas</i> and <i>Lactobacillus</i> on tick fitness, microbiome diversity and community assembly were explored. The result of the study shows that in Om, <i>Pseudomonas</i> plays a central role in microbial networks, influencing keystone species despite being categorized as peripheral (interacting with 47 different taxa, 13 of which are keystone species). Anti-microbiota vaccination targeting <i>Pseudomonas</i> and <i>Lactobacillus</i> yields distinct effects on tick fitness, with <i>Pseudomonas</i> vaccination significantly impacting female tick survival, while <i>Lactobacillus</i> significantly reduced oviposition and fertility. Microbiome changes post-vaccination reveal diversity alterations, emphasizing the impact of vaccine choice. Community assembly dynamics and network robustness analyses highlight <i>Pseudomonas</i>' pivotal role, in influencing topological features and network resilience. The findings of the study provide comprehensive insights into the intricate dynamics of Om microbial networks and the potential of targeted microbiota-driven vaccines for tick control.</p>","PeriodicalId":210,"journal":{"name":"Molecular Ecology","volume":null,"pages":null},"PeriodicalIF":4.5000,"publicationDate":"2024-08-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/mec.17506","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Molecular Ecology","FirstCategoryId":"99","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1111/mec.17506","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
The Ornithodoros moubata (Om) soft tick, a vector for diseases like tick-borne human relapsing fever and African swine fever, poses challenges to conventional control methods. With diminishing insecticide efficacy, harnessing the tick's microbiota through innovative approaches like microbiota-driven vaccination emerges as a promising strategy for sustainable and targeted disease control. This study investigated the intricate relationship between Pseudomonas, a keystone taxon in the Om microbiome, and its impact on tick fitness, microbiome structure and network dynamics. Utilizing in silico analyses and empirical vaccination experiments, the role of Pseudomonas within microbial networks in the tick midguts (MG) and salivary glands (SG) of Om was studied. Additionally, the consequences of anti-microbiota vaccines targeting Pseudomonas and Lactobacillus on tick fitness, microbiome diversity and community assembly were explored. The result of the study shows that in Om, Pseudomonas plays a central role in microbial networks, influencing keystone species despite being categorized as peripheral (interacting with 47 different taxa, 13 of which are keystone species). Anti-microbiota vaccination targeting Pseudomonas and Lactobacillus yields distinct effects on tick fitness, with Pseudomonas vaccination significantly impacting female tick survival, while Lactobacillus significantly reduced oviposition and fertility. Microbiome changes post-vaccination reveal diversity alterations, emphasizing the impact of vaccine choice. Community assembly dynamics and network robustness analyses highlight Pseudomonas' pivotal role, in influencing topological features and network resilience. The findings of the study provide comprehensive insights into the intricate dynamics of Om microbial networks and the potential of targeted microbiota-driven vaccines for tick control.
Ornithodoros moubata(Om)软蜱是蜱传人类复发性热病和非洲猪瘟等疾病的病媒,它对传统的控制方法构成了挑战。随着杀虫剂效力的降低,通过微生物群驱动疫苗接种等创新方法来利用蜱的微生物群,成为一种可持续和有针对性的疾病控制策略。本研究调查了假单胞菌(Om 微生物组中的一个关键类群)之间错综复杂的关系及其对蜱的适应性、微生物组结构和网络动力学的影响。利用硅学分析和经验疫苗接种实验,研究了假单胞菌在 Om 的蜱中肠(MG)和唾液腺(SG)微生物网络中的作用。此外,还探讨了针对假单胞菌和乳酸杆菌的抗微生物群疫苗对蜱的适应性、微生物群多样性和群落组合的影响。研究结果表明,在 Om 中,假单胞菌在微生物网络中发挥着核心作用,尽管它被归类为边缘物种(与 47 个不同类群相互作用,其中 13 个是关键物种),但却影响着关键物种。针对假单胞菌和乳酸杆菌的抗微生物群疫苗接种对蜱的适应性产生了不同的影响,假单胞菌疫苗接种会显著影响雌蜱的存活率,而乳酸杆菌则会显著降低雌蜱的产卵率和繁殖力。接种疫苗后微生物组的变化揭示了多样性的改变,强调了疫苗选择的影响。群落组装动力学和网络鲁棒性分析突出了假单胞菌在影响拓扑特征和网络弹性方面的关键作用。这项研究的结果提供了对 Om 微生物网络复杂动态的全面见解,以及有针对性的微生物群驱动疫苗在蜱虫控制方面的潜力。
期刊介绍:
Molecular Ecology publishes papers that utilize molecular genetic techniques to address consequential questions in ecology, evolution, behaviour and conservation. Studies may employ neutral markers for inference about ecological and evolutionary processes or examine ecologically important genes and their products directly. We discourage papers that are primarily descriptive and are relevant only to the taxon being studied. Papers reporting on molecular marker development, molecular diagnostics, barcoding, or DNA taxonomy, or technical methods should be re-directed to our sister journal, Molecular Ecology Resources. Likewise, papers with a strongly applied focus should be submitted to Evolutionary Applications. Research areas of interest to Molecular Ecology include:
* population structure and phylogeography
* reproductive strategies
* relatedness and kin selection
* sex allocation
* population genetic theory
* analytical methods development
* conservation genetics
* speciation genetics
* microbial biodiversity
* evolutionary dynamics of QTLs
* ecological interactions
* molecular adaptation and environmental genomics
* impact of genetically modified organisms