title: Convergent patterns in the evolution of mealybug symbioses involving different intrabacterial symbionts.
abstract: Mealybugs (Insecta: Hemiptera: Pseudococcidae) maintain obligatory relationships with bacterial symbionts, which provide essential nutrients to their insect hosts. Most pseudococcinae mealybugs harbor a unique symbiosis setup with enlarged betaproteobacterial symbionts ('Candidatus Tremblaya princeps'), which themselves contain gammaproteobacterial symbionts. Here we investigated the symbiosis of the manna mealybug, Trabutina mannipara, using a metagenomic approach. Phylogenetic analyses revealed that the intrabacterial symbiont of T. mannipara represents a novel lineage within the Gammaproteobacteria, for which we propose the tentative name 'Candidatus Trabutinella endobia'. Combining our results with previous data available for the nested symbiosis of the citrus mealybug Planococcus citri, we show that synthesis of essential amino acids and vitamins and translation-related functions partition between the symbiotic partners in a highly similar manner in the two systems, despite the distinct evolutionary origin of the intrabacterial symbionts. Bacterial genes found in both mealybug genomes and complementing missing functions in both symbioses were likely integrated in ancestral mealybugs before T. mannipara and P. citri diversified. The high level of correspondence between the two mealybug systems and their highly intertwined metabolic pathways are unprecedented. Our work contributes to a better understanding of the only known intracellular symbiosis between two bacteria and suggests that the evolution of this unique symbiosis included the replacement of intrabacterial symbionts in ancestral mealybugs.
authors.affiliation: Division of Microbial Ecology, Department of Microbiology and Ecosystem Science, University of Vienna, Vienna, Austria.
authors.forename: Gitta
authors.initials: G
authors.lastname: Szabó
authors.affiliation: Division of Microbial Ecology, Department of Microbiology and Ecosystem Science, University of Vienna, Vienna, Austria.
authors.forename: Frederik
authors.initials: F
authors.lastname: Schulz
authors.affiliation: Division of Microbial Ecology, Department of Microbiology and Ecosystem Science, University of Vienna, Vienna, Austria.
authors.forename: Elena R
authors.initials: ER
authors.lastname: Toenshoff
authors.affiliation: Department of Limnology and Bio-Oceanography, University of Vienna, Vienna, Austria.
authors.forename: Jean-Marie
authors.initials: JM
authors.lastname: Volland
authors.affiliation: Department of Plant and Environmental Sciences, The Alexander Silberman Institute of Life Sciences, Hebrew University of Jerusalem, Jerusalem, Israel.
authors.forename: Omri M
authors.initials: OM
authors.lastname: Finkel
authors.affiliation: Department of Plant and Environmental Sciences, The Alexander Silberman Institute of Life Sciences, Hebrew University of Jerusalem, Jerusalem, Israel.
authors.forename: Shimshon
authors.initials: S
authors.lastname: Belkin
authors.affiliation: Division of Microbial Ecology, Department of Microbiology and Ecosystem Science, University of Vienna, Vienna, Austria.
authors.forename: Matthias
authors.initials: M
authors.lastname: Horn
mesh_terms: D000818:Animals; D001419:Bacteria / Q000235:genetics; D020562:Betaproteobacteria / Q000235:genetics* / Q000502:physiology; D005075:Biological Evolution; D020563:Gammaproteobacteria / Q000235:genetics* / Q000502:physiology; D006430:Hemiptera / Q000382:microbiology*; D013559:Symbiosis / Q000235:genetics* / Q000502:physiology