A dual endosymbiosis supports nutritional adaptation to hematophagy in the invasive tick Hyalomma marginatum

eLife

Anna Maria Floriano¹  Tiago Nardi²  Chiara Bazzocchi³  Yuval Gottlieb⁴  Ana M Palomar⁴  Emanuela Olivieri⁴  Alessia Giannetto⁵  Benjamin L Makepeace⁶  Olivier Duron⁷  Davide Sassera⁷  Alessandra Cafiso⁸  Francesco Comandatore⁹  Marie Buysse^1,10 

[1] Centre of Research in Ecology and Evolution of Diseases (CREES), Montpellier, France, Montpellier, France;Faculty of Science, University of South Bohemia, České Budějovice, Czech Republic;Center of Rickettsiosis and Arthropod-Borne Diseases (CRETAV), San Pedro University Hospital- Center of Biomedical Research from La Rioja (CIBIR), Logroño, Spain;Department of Biology and Biotechnology “L. Spallanzani”, University of Pavia, Pavia, Italy;Department of Biomedical and Clinical Sciences L. Sacco and Pediatric Clinical Research Center, University of Milan, Milan, Italy;Department of Chemical, Biological, Pharmaceutical and Environmental Sciences, University of Messina, Messina, Italy;Department of Veterinary Medicine, University of Milan, Lodi, Italy;Institute of Infection, Veterinary & Ecological Sciences, University of Liverpool, Liverpool, United Kingdom;Koret School of Veterinary Medicine, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel;MIVEGEC (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;

关键词: endosymbiosis;    hematophagy;    Francisella;    Midichloria;    Hyalomma;   

DOI  :  10.7554/eLife.72747

来源: DOAJ

【 摘 要 】

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.

【 授权许可】

Unknown