Distribution, Vertical Transmission, and Cooperative Mechanisms of Obligate Symbiotic Bacteria in the Leafhopper Maiestas dorsalis (Hemiptera, Cicadellidea)

Abstract

Many insects rely on ancient symbiotic bacterial associations for essential nutrition. Auchenorrhyncha commonly harbor two obligate symbionts: Sulcia (Bacteroidetes) and a proteobacterial partner that supplies essential amino acids lacking in their plant-sap diets. In this study focusing on Maiestas dorsalis, we investigated the distribution and vertical transmission of two obligate symbiotic bacteria, Sulcia and Nasuia, within the leafhopper. Sulcia primarily inhabits the external region of the bacteriome, while Nasuia is restricted to the internal region. Both symbionts progressively infiltrate the ovary through the epithelial plug, ultimately reaching the developing primary oocyte. Furthermore, co-phylogenetic analysis suggests a close correlation between the evolution of Auchenorrhyncha insects and the presence of their obligate symbiotic bacteria. Genomic analysis further unveiled the extreme genome reduction of the obligate symbiotic bacteria, with Sulcia retaining genes involved in basic cellular processes and limited energy synthesis, while Nasuia exhibited further gene loss in replication, transcription, translation, and energy synthesis. However, both symbionts retained the genes for synthesizing the essential amino acids required by the host insect. Our study highlights the coevolutionary dynamics between Sulcia, proteobacterial partners, and their insect hosts, shedding light on the intricate nutritional interactions and evolutionary adaptations in Auchenorrhyncha insects.