A dual endosymbiosis supports nutritional adaptation to hematophagy in the invasive tick Hyalomma marginatum
Many animals are dependent on microbial partners that provide essential nutrients lacking from their diet. Ticks, whose diet consists exclusively on vertebrate blood, rely on maternally inherited bacterial symbionts to supply B vitamins. While previously studied tick species consistently harbor a si...
| Main Authors: | , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2021-12-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/72747 |
| _version_ | 1828195506728206336 |
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| author | Marie Buysse Anna Maria Floriano Yuval Gottlieb Tiago Nardi Francesco Comandatore Emanuela Olivieri Alessia Giannetto Ana M Palomar Benjamin L Makepeace Chiara Bazzocchi Alessandra Cafiso Davide Sassera Olivier Duron |
| author_facet | Marie Buysse Anna Maria Floriano Yuval Gottlieb Tiago Nardi Francesco Comandatore Emanuela Olivieri Alessia Giannetto Ana M Palomar Benjamin L Makepeace Chiara Bazzocchi Alessandra Cafiso Davide Sassera Olivier Duron |
| author_sort | Marie Buysse |
| collection | DOAJ |
| description | Many animals are dependent on microbial partners that provide essential nutrients lacking from their diet. Ticks, whose diet consists exclusively on vertebrate blood, rely on maternally inherited bacterial symbionts to supply B vitamins. While previously studied tick species consistently harbor a single lineage of those nutritional symbionts, we evidence here that the invasive tick Hyalomma marginatum harbors a unique dual-partner nutritional system between an ancestral symbiont, Francisella, and a more recently acquired symbiont, Midichloria. Using metagenomics, we show that Francisella exhibits extensive genome erosion that endangers the nutritional symbiotic interactions. Its genome includes folate and riboflavin biosynthesis pathways but deprived functional biotin biosynthesis on account of massive pseudogenization. Co-symbiosis compensates this deficiency since the Midichloria genome encompasses an intact biotin operon, which was primarily acquired via lateral gene transfer from unrelated intracellular bacteria commonly infecting arthropods. Thus, in H. marginatum, a mosaic of co-evolved symbionts incorporating gene combinations of distant phylogenetic origins emerged to prevent the collapse of an ancestral nutritional symbiosis. Such dual endosymbiosis was never reported in other blood feeders but was recently documented in agricultural pests feeding on plant sap, suggesting that it may be a key mechanism for advanced adaptation of arthropods to specialized diets. |
| first_indexed | 2024-04-12T09:44:47Z |
| format | Article |
| id | doaj.art-dbc644ec88b240d092dd6992f3b792aa |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T09:44:47Z |
| publishDate | 2021-12-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-dbc644ec88b240d092dd6992f3b792aa2022-12-22T03:37:59ZengeLife Sciences Publications LtdeLife2050-084X2021-12-011010.7554/eLife.72747A dual endosymbiosis supports nutritional adaptation to hematophagy in the invasive tick Hyalomma marginatumMarie Buysse0https://orcid.org/0000-0002-8160-2470Anna Maria Floriano1Yuval Gottlieb2Tiago Nardi3https://orcid.org/0000-0002-1248-9873Francesco Comandatore4Emanuela Olivieri5Alessia Giannetto6Ana M Palomar7https://orcid.org/0000-0002-5461-5874Benjamin L Makepeace8Chiara Bazzocchi9Alessandra Cafiso10Davide Sassera11Olivier Duron12MIVEGEC (Maladies Infectieuses et Vecteurs : Ecologie, Génétique, Evolution et Contrôle), Univ. Montpellier (UM) - Centre National de la Recherche Scientifique (CNRS) - Institut pour la Recherche et le Développement (IRD), Montpellier, France; Centre of Research in Ecology and Evolution of Diseases (CREES), Montpellier, France, Montpellier, FranceDepartment of Biology and Biotechnology “L. Spallanzani”, University of Pavia, Pavia, Italy; Faculty of Science, University of South Bohemia, České Budějovice, Czech RepublicKoret School of Veterinary Medicine, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, IsraelDepartment of Biology and Biotechnology “L. Spallanzani”, University of Pavia, Pavia, ItalyDepartment of Biomedical and Clinical Sciences L. Sacco and Pediatric Clinical Research Center, University of Milan, Milan, ItalyDepartment of Biology and Biotechnology “L. Spallanzani”, University of Pavia, Pavia, ItalyDepartment of Chemical, Biological, Pharmaceutical and Environmental Sciences, University of Messina, Messina, ItalyCenter of Rickettsiosis and Arthropod-Borne Diseases (CRETAV), San Pedro University Hospital- Center of Biomedical Research from La Rioja (CIBIR), Logroño, SpainInstitute of Infection, Veterinary & Ecological Sciences, University of Liverpool, Liverpool, United KingdomDepartment of Veterinary Medicine, University of Milan, Lodi, ItalyDepartment of Veterinary Medicine, University of Milan, Lodi, ItalyDepartment of Biology and Biotechnology “L. Spallanzani”, University of Pavia, Pavia, ItalyMIVEGEC (Maladies Infectieuses et Vecteurs : Ecologie, Génétique, Evolution et Contrôle), Univ. Montpellier (UM) - Centre National de la Recherche Scientifique (CNRS) - Institut pour la Recherche et le Développement (IRD), Montpellier, France; Centre of Research in Ecology and Evolution of Diseases (CREES), Montpellier, France, Montpellier, FranceMany animals are dependent on microbial partners that provide essential nutrients lacking from their diet. Ticks, whose diet consists exclusively on vertebrate blood, rely on maternally inherited bacterial symbionts to supply B vitamins. While previously studied tick species consistently harbor a single lineage of those nutritional symbionts, we evidence here that the invasive tick Hyalomma marginatum harbors a unique dual-partner nutritional system between an ancestral symbiont, Francisella, and a more recently acquired symbiont, Midichloria. Using metagenomics, we show that Francisella exhibits extensive genome erosion that endangers the nutritional symbiotic interactions. Its genome includes folate and riboflavin biosynthesis pathways but deprived functional biotin biosynthesis on account of massive pseudogenization. Co-symbiosis compensates this deficiency since the Midichloria genome encompasses an intact biotin operon, which was primarily acquired via lateral gene transfer from unrelated intracellular bacteria commonly infecting arthropods. Thus, in H. marginatum, a mosaic of co-evolved symbionts incorporating gene combinations of distant phylogenetic origins emerged to prevent the collapse of an ancestral nutritional symbiosis. Such dual endosymbiosis was never reported in other blood feeders but was recently documented in agricultural pests feeding on plant sap, suggesting that it may be a key mechanism for advanced adaptation of arthropods to specialized diets.https://elifesciences.org/articles/72747endosymbiosishematophagyFrancisellaMidichloriaHyalomma |
| spellingShingle | Marie Buysse Anna Maria Floriano Yuval Gottlieb Tiago Nardi Francesco Comandatore Emanuela Olivieri Alessia Giannetto Ana M Palomar Benjamin L Makepeace Chiara Bazzocchi Alessandra Cafiso Davide Sassera Olivier Duron A dual endosymbiosis supports nutritional adaptation to hematophagy in the invasive tick Hyalomma marginatum eLife endosymbiosis hematophagy Francisella Midichloria Hyalomma |
| title | A dual endosymbiosis supports nutritional adaptation to hematophagy in the invasive tick Hyalomma marginatum |
| title_full | A dual endosymbiosis supports nutritional adaptation to hematophagy in the invasive tick Hyalomma marginatum |
| title_fullStr | A dual endosymbiosis supports nutritional adaptation to hematophagy in the invasive tick Hyalomma marginatum |
| title_full_unstemmed | A dual endosymbiosis supports nutritional adaptation to hematophagy in the invasive tick Hyalomma marginatum |
| title_short | A dual endosymbiosis supports nutritional adaptation to hematophagy in the invasive tick Hyalomma marginatum |
| title_sort | dual endosymbiosis supports nutritional adaptation to hematophagy in the invasive tick hyalomma marginatum |
| topic | endosymbiosis hematophagy Francisella Midichloria Hyalomma |
| url | https://elifesciences.org/articles/72747 |
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