The Endosymbiont Consortia of Two Cixiidae Planthoppers Reveal an Ancient Symbiosis With ‘ <i>Candidatus</i> Mirabilia Symbiotica’

Insects of the suborder Auchenorrhyncha harbour multiple ancient endosymbionts that jointly produce essential nutrients lacking from the host's diet. Compared to cicadas, leafhoppers, and spittlebugs, our understanding of the multipartite symbioses among planthoppers, an extremely diverse insect group, is still very limited. Herein, we assembled the genomes of the primary endosymbionts of two planthopper species from the Cixiidae family, Cixius wagneri and Pentastiridius leporinus, both vectors of phytopathogenic Arsenophonus in Europe. Each species harboured a different tripartite endosymbiont consortium: while P. leporinus carried the well-known combination 'Candidatus Karelsulcia muelleri', 'Ca. Vidania fulgoroideae', and 'Ca. Purcelliella pentastirinorum', C. wagneri harboured a yet unknown Gammaproteobacterium in addition to Karelsulcia and Vidania. This new endosymbiont 'Ca. Mirabilia symbiotica' is likely much older than Purcelliella, considering its extremely reduced genome. In both species, Karelsulcia and Vidania jointly produce the 10 essential amino acids, whereas Purcelliella and Mirabilia provide the non-essential amino acid cysteine and slightly different gene sets encoding B vitamins. Our findings confirm the functional stability of multipartite planthopper endosymbiont consortia despite changing partners over evolutionary time. In addition, we describe a new Rickettsia strain from the Meloidae group colonising P. leporinus, highlighting the diversity of bacterial endosymbionts associated with planthoppers.