Comparison of salivary gland and midgut microbiome in the soft ticks Ornithodoros erraticus and Ornithodoros moubata
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 m...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-05-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1173609/full |
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| author | Elianne Piloto-Sardiñas Elianne Piloto-Sardiñas Ana Laura Cano-Argüelles Apolline Maitre Apolline Maitre Apolline Maitre Alejandra Wu-Chuang Lourdes Mateos-Hernández Alexandra Corduneanu Alexandra Corduneanu Dasiel Obregón Ana Oleaga Ricardo Pérez-Sánchez Alejandro Cabezas-Cruz |
| author_facet | Elianne Piloto-Sardiñas Elianne Piloto-Sardiñas Ana Laura Cano-Argüelles Apolline Maitre Apolline Maitre Apolline Maitre Alejandra Wu-Chuang Lourdes Mateos-Hernández Alexandra Corduneanu Alexandra Corduneanu Dasiel Obregón Ana Oleaga Ricardo Pérez-Sánchez Alejandro Cabezas-Cruz |
| author_sort | Elianne Piloto-Sardiñas |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-04-09T13:46:11Z |
| format | Article |
| id | doaj.art-9d32b788cc234784b1cb712fb8a871b7 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-09T13:46:11Z |
| publishDate | 2023-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-9d32b788cc234784b1cb712fb8a871b72023-05-09T04:52:23ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-05-011410.3389/fmicb.2023.11736091173609Comparison of salivary gland and midgut microbiome in the soft ticks Ornithodoros erraticus and Ornithodoros moubataElianne Piloto-Sardiñas0Elianne Piloto-Sardiñas1Ana Laura Cano-Argüelles2Apolline Maitre3Apolline Maitre4Apolline Maitre5Alejandra Wu-Chuang6Lourdes Mateos-Hernández7Alexandra Corduneanu8Alexandra Corduneanu9Dasiel Obregón10Ana Oleaga11Ricardo Pérez-Sánchez12Alejandro Cabezas-Cruz13Direction of Animal Health, National Center for Animal and Plant Health, Carretera de Tapaste y Autopista Nacional, San José de las Lajas, Mayabeque, CubaANSES, INRAE, Ecole Nationale Vétérinaire d’Alfort, UMR BIPAR, Laboratoire de Santé Animale, Maisons-Alfort, FranceParasitology Laboratory, Institute of Natural Resources and Agrobiology (IRNASA, CSIC), Salamanca, SpainANSES, INRAE, Ecole Nationale Vétérinaire d’Alfort, UMR BIPAR, Laboratoire de Santé Animale, Maisons-Alfort, FranceUR 0045 Laboratoire de Recherches Sur Le Développement de L’Elevage (SELMET-LRDE), INRAE, Corte, FranceEA 7310, Laboratoire de Virologie, Université de Corse, Corte, FranceANSES, INRAE, Ecole Nationale Vétérinaire d’Alfort, UMR BIPAR, Laboratoire de Santé Animale, Maisons-Alfort, FranceANSES, INRAE, Ecole Nationale Vétérinaire d’Alfort, UMR BIPAR, Laboratoire de Santé Animale, Maisons-Alfort, FranceDepartment of Animal Breeding and Animal Production, University of Agricultural Sciences and Veterinary Medicine, Cluj-Napoca, RomaniaDepartment of Parasitology and Parasitic Diseases, University of Agricultural Sciences and Veterinary Medicine, Cluj-Napoca, RomaniaSchool of Environmental Sciences University of Guelph, Guelph, ON, CanadaParasitology Laboratory, Institute of Natural Resources and Agrobiology (IRNASA, CSIC), Salamanca, SpainParasitology Laboratory, Institute of Natural Resources and Agrobiology (IRNASA, CSIC), Salamanca, SpainANSES, INRAE, Ecole Nationale Vétérinaire d’Alfort, UMR BIPAR, Laboratoire de Santé Animale, Maisons-Alfort, FranceIntroductionOrnithodoros 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.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1173609/fullmicrobiomesalivary glandmidgutOrnithodoros erraticusOrnithodoros moubatanetworks |
| spellingShingle | Elianne Piloto-Sardiñas Elianne Piloto-Sardiñas Ana Laura Cano-Argüelles Apolline Maitre Apolline Maitre Apolline Maitre Alejandra Wu-Chuang Lourdes Mateos-Hernández Alexandra Corduneanu Alexandra Corduneanu Dasiel Obregón Ana Oleaga Ricardo Pérez-Sánchez Alejandro Cabezas-Cruz Comparison of salivary gland and midgut microbiome in the soft ticks Ornithodoros erraticus and Ornithodoros moubata Frontiers in Microbiology microbiome salivary gland midgut Ornithodoros erraticus Ornithodoros moubata networks |
| title | Comparison of salivary gland and midgut microbiome in the soft ticks Ornithodoros erraticus and Ornithodoros moubata |
| title_full | Comparison of salivary gland and midgut microbiome in the soft ticks Ornithodoros erraticus and Ornithodoros moubata |
| title_fullStr | Comparison of salivary gland and midgut microbiome in the soft ticks Ornithodoros erraticus and Ornithodoros moubata |
| title_full_unstemmed | Comparison of salivary gland and midgut microbiome in the soft ticks Ornithodoros erraticus and Ornithodoros moubata |
| title_short | Comparison of salivary gland and midgut microbiome in the soft ticks Ornithodoros erraticus and Ornithodoros moubata |
| title_sort | comparison of salivary gland and midgut microbiome in the soft ticks ornithodoros erraticus and ornithodoros moubata |
| topic | microbiome salivary gland midgut Ornithodoros erraticus Ornithodoros moubata networks |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1173609/full |
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