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SummaryThe evolutionary success of sap-feeding hemipteran insects in the suborder Auchenorrhyncha was enabled by nutritional contributions from their heritable endosymbiotic bacteria. However, the symbiont diversity, functions, and evolutionary origins in this large insect group have not been broadly characterized using genomic tools. In particular, the origins and relationships among ancient betaproteobacterial symbiontsVidania(in Fulgoromorpha) andNasuia/Zinderia(in Cicadomorpha) are uncertain. Here, we characterized the genomes ofVidaniaandSulciafrom threePyropsplanthoppers (family Fulgoridae) to understand their metabolic functions and evolutionary histories. Like in previously characterized planthoppers, these symbionts share nutritional responsibilities, withVidaniaproviding seven out of ten essential amino acids.Sulcialineages across the Auchenorrhyncha have a highly conserved genome but with multiple independent rearrangements occurring in an early ancestor of Cicadomorpha or Fulgoromorpha and in a few succeeding lineages. Genomic synteny was also observed within each of the betaproteobacterial symbiont generaNasuia,Zinderia, andVidania, but not across them, which challenges the expectation of a shared ancestry for these symbionts. The further comparison of other biological traits strongly suggests an independent origin ofVidaniaearly in the planthopper evolution and possibly ofNasuiaandZinderiain their respective host lineages.Originality-Significance StatementWe sequenced and characterized the genomes of two ancient nutritional symbionts,SulciaandVidania, in three species from the genusPyropsin the species- and symbiont-rich but understudied insect clade, Fulgoromorpha (planthoppers). We describe—for the first time—several independent genome rearrangements inSulcia, which is often cited as a premier example of extreme genome stability spanning hundreds of millions of years. We also show a global lack of synteny across the genomes of the Auchenorrhynchan betaproteobacterial symbionts (Vidania,Nasuia, andZinderia). This result is unexpected given previous hypotheses of a common origin for these symbionts >250 million years ago alongsideSulcia. Taken together, we suggest an independent origin ofVidaniaand possibly ofNasuiaandZinderiasymbiont lineages as well. This hypothesis further links the potential acquisition of novel nutritional endosymbiont lineages with the emergence of auchenorrhyncham superfamilies. |
