Heritable beneficial bacterial endosymbionts have been crucial for the evolutionary success of numerous insects by enabling the exploitation of nutritionally limited food sources. Herein, we describe a previously unknown dual endosymbiosis in the psyllid genus Cacopsylla, consisting of the primary endosymbiont "Candidatus Carsonella ruddii" and a co-occurring Enterobacteriaceae bacterium for which we propose the name "Candidatus Psyllophila symbiotica." Its localization within the bacteriome and its small genome size confirm that Psyllophila is a co-primary endosymbiont widespread within the genus Cacopsylla. Despite its highly eroded genome, Psyllophila perfectly complements the tryptophan biosynthesis pathway that is incomplete in the co-occurring Carsonella. Moreover, the genome of Psyllophila is almost as small as Carsonella's, suggesting an ancient dual endosymbiosis that has now reached a precarious stage where any additional gene loss would make the system collapse. Hence, our results shed light on the dynamic interactions of psyllids and their endosymbionts over evolutionary time.

Competence Centre for Plant Health Free University of Bozen Bolzano Bolzano Italy

Department of Developmental Biology and Morphology of Invertebrates Institute of Zoology and Biomedical Research Faculty of Biology Jagiellonian University Krakow Poland

Faculty of Agricultural Environmental and Food Sciences Free University of Bozen Bolzano Bolzano Italy

Faculty of Science University of South Bohemia České Budějovice Czech Republic

UMR 1345 Université d'Angers Institut Agro INRAE IRHS SFR Quasav Beaucouzé France

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Seasonal wild dance of dual endosymbionts in the pear psyllid Cacopsylla pyricola (Hemiptera: Psylloidea)