Anti-Microbiota Vaccines Modulate the Tick Microbiome in a Taxon-Specific Manner
The lack of tools for the precise manipulation of the tick microbiome is currently a major limitation to achieve mechanistic insights into the tick microbiome. Anti-tick microbiota vaccines targeting keystone bacteria of the tick microbiota alter tick feeding, but their impact on the taxonomic and f...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2021-07-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2021.704621/full |
| _version_ | 1818619859973439488 |
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| author | Lourdes Mateos-Hernández Dasiel Obregón Alejandra Wu-Chuang Jennifer Maye Jeremie Bornères Nicolas Versillé José de la Fuente José de la Fuente Sandra Díaz-Sánchez Luis G. Bermúdez-Humarán Edgar Torres-Maravilla Agustín Estrada-Peña Adnan Hodžić Ladislav Šimo Alejandro Cabezas-Cruz |
| author_facet | Lourdes Mateos-Hernández Dasiel Obregón Alejandra Wu-Chuang Jennifer Maye Jeremie Bornères Nicolas Versillé José de la Fuente José de la Fuente Sandra Díaz-Sánchez Luis G. Bermúdez-Humarán Edgar Torres-Maravilla Agustín Estrada-Peña Adnan Hodžić Ladislav Šimo Alejandro Cabezas-Cruz |
| author_sort | Lourdes Mateos-Hernández |
| collection | DOAJ |
| description | The lack of tools for the precise manipulation of the tick microbiome is currently a major limitation to achieve mechanistic insights into the tick microbiome. Anti-tick microbiota vaccines targeting keystone bacteria of the tick microbiota alter tick feeding, but their impact on the taxonomic and functional profiles of the tick microbiome has not been tested. In this study, we immunized a vertebrate host model (Mus musculus) with live bacteria vaccines targeting keystone (i.e., Escherichia-Shigella) or non-keystone (i.e., Leuconostoc) taxa of tick microbiota and tested the impact of bacterial-specific antibodies (Abs) on the structure and function of tick microbiota. We also investigated the effect of these anti-microbiota vaccines on mice gut microbiota composition. Our results showed that the tick microbiota of ticks fed on Escherichia coli-immunized mice had reduced Escherichia-Shigella abundance and lower species diversity compared to ticks fed on control mice immunized with a mock vaccine. Immunization against keystone bacteria restructured the hierarchy of nodes in co-occurrence networks and reduced the resistance of the bacterial network to taxa removal. High levels of E. coli-specific IgM and IgG were negatively correlated with the abundance of Escherichia-Shigella in tick microbiota. These effects were not observed when Leuconostoc was targeted with vaccination against Leuconostoc mesenteroides. Prediction of functional pathways in the tick microbiome using PICRUSt2 revealed that E. coli vaccination reduced the abundance of lysine degradation pathway in tick microbiome, a result validated by qPCR. In contrast, the gut microbiome of immunized mice showed no significant alterations in the diversity, composition and abundance of bacterial taxa. Our results demonstrated that anti-tick microbiota vaccines are a safe, specific and an easy-to-use tool for manipulation of vector microbiome. These results guide interventions for the control of tick infestations and pathogen infection/transmission. |
| first_indexed | 2024-12-16T17:44:11Z |
| format | Article |
| id | doaj.art-70df5b4b3ac941a489832559d5607e71 |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-12-16T17:44:11Z |
| publishDate | 2021-07-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-70df5b4b3ac941a489832559d5607e712022-12-21T22:22:31ZengFrontiers Media S.A.Frontiers in Immunology1664-32242021-07-011210.3389/fimmu.2021.704621704621Anti-Microbiota Vaccines Modulate the Tick Microbiome in a Taxon-Specific MannerLourdes Mateos-Hernández0Dasiel Obregón1Alejandra Wu-Chuang2Jennifer Maye3Jeremie Bornères4Nicolas Versillé5José de la Fuente6José de la Fuente7Sandra Díaz-Sánchez8Luis G. Bermúdez-Humarán9Edgar Torres-Maravilla10Agustín Estrada-Peña11Adnan Hodžić12Ladislav Šimo13Alejandro Cabezas-Cruz14Anses, INRAE, Ecole Nationale Vétérinaire d’Alfort, UMR BIPAR, Laboratoire de Santé Animale, Maisons-Alfort, F-94700, FranceSchool of Environmental Sciences University of Guelph, Guelph, ON, CanadaAnses, INRAE, Ecole Nationale Vétérinaire d’Alfort, UMR BIPAR, Laboratoire de Santé Animale, Maisons-Alfort, F-94700, FranceSEPPIC Paris La Défense, La Garenne Colombes, 92250, FranceSEPPIC Paris La Défense, La Garenne Colombes, 92250, FranceSEPPIC Paris La Défense, La Garenne Colombes, 92250, FranceSaBio, Instituto de Investigación en Recursos Cinegéticos (IREC-CSIC-UCLM-JCCM), Ciudad Real, SpainDepartment of Veterinary Pathobiology, Center for Veterinary Health Sciences, Oklahoma State University, Stillwater, OK, United StatesSaBio, Instituto de Investigación en Recursos Cinegéticos (IREC-CSIC-UCLM-JCCM), Ciudad Real, SpainUniversité Paris-Saclay, INRAE, AgroParisTech, Micalis Institute, 78350, Jouy-en-Josas, FranceUniversité Paris-Saclay, INRAE, AgroParisTech, Micalis Institute, 78350, Jouy-en-Josas, FranceFaculty of Veterinary Medicine, University of Zaragoza, Zaragoza, SpainInstitute of Parasitology, Department of Pathobiology, University of Veterinary Medicine Vienna, Vienna, AustriaAnses, INRAE, Ecole Nationale Vétérinaire d’Alfort, UMR BIPAR, Laboratoire de Santé Animale, Maisons-Alfort, F-94700, FranceAnses, INRAE, Ecole Nationale Vétérinaire d’Alfort, UMR BIPAR, Laboratoire de Santé Animale, Maisons-Alfort, F-94700, FranceThe lack of tools for the precise manipulation of the tick microbiome is currently a major limitation to achieve mechanistic insights into the tick microbiome. Anti-tick microbiota vaccines targeting keystone bacteria of the tick microbiota alter tick feeding, but their impact on the taxonomic and functional profiles of the tick microbiome has not been tested. In this study, we immunized a vertebrate host model (Mus musculus) with live bacteria vaccines targeting keystone (i.e., Escherichia-Shigella) or non-keystone (i.e., Leuconostoc) taxa of tick microbiota and tested the impact of bacterial-specific antibodies (Abs) on the structure and function of tick microbiota. We also investigated the effect of these anti-microbiota vaccines on mice gut microbiota composition. Our results showed that the tick microbiota of ticks fed on Escherichia coli-immunized mice had reduced Escherichia-Shigella abundance and lower species diversity compared to ticks fed on control mice immunized with a mock vaccine. Immunization against keystone bacteria restructured the hierarchy of nodes in co-occurrence networks and reduced the resistance of the bacterial network to taxa removal. High levels of E. coli-specific IgM and IgG were negatively correlated with the abundance of Escherichia-Shigella in tick microbiota. These effects were not observed when Leuconostoc was targeted with vaccination against Leuconostoc mesenteroides. Prediction of functional pathways in the tick microbiome using PICRUSt2 revealed that E. coli vaccination reduced the abundance of lysine degradation pathway in tick microbiome, a result validated by qPCR. In contrast, the gut microbiome of immunized mice showed no significant alterations in the diversity, composition and abundance of bacterial taxa. Our results demonstrated that anti-tick microbiota vaccines are a safe, specific and an easy-to-use tool for manipulation of vector microbiome. These results guide interventions for the control of tick infestations and pathogen infection/transmission.https://www.frontiersin.org/articles/10.3389/fimmu.2021.704621/fullanti-microbiota vaccinestickmicrobiome modulationkeystone bacterianetworks analysis |
| spellingShingle | Lourdes Mateos-Hernández Dasiel Obregón Alejandra Wu-Chuang Jennifer Maye Jeremie Bornères Nicolas Versillé José de la Fuente José de la Fuente Sandra Díaz-Sánchez Luis G. Bermúdez-Humarán Edgar Torres-Maravilla Agustín Estrada-Peña Adnan Hodžić Ladislav Šimo Alejandro Cabezas-Cruz Anti-Microbiota Vaccines Modulate the Tick Microbiome in a Taxon-Specific Manner Frontiers in Immunology anti-microbiota vaccines tick microbiome modulation keystone bacteria networks analysis |
| title | Anti-Microbiota Vaccines Modulate the Tick Microbiome in a Taxon-Specific Manner |
| title_full | Anti-Microbiota Vaccines Modulate the Tick Microbiome in a Taxon-Specific Manner |
| title_fullStr | Anti-Microbiota Vaccines Modulate the Tick Microbiome in a Taxon-Specific Manner |
| title_full_unstemmed | Anti-Microbiota Vaccines Modulate the Tick Microbiome in a Taxon-Specific Manner |
| title_short | Anti-Microbiota Vaccines Modulate the Tick Microbiome in a Taxon-Specific Manner |
| title_sort | anti microbiota vaccines modulate the tick microbiome in a taxon specific manner |
| topic | anti-microbiota vaccines tick microbiome modulation keystone bacteria networks analysis |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2021.704621/full |
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