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

SIMPLE SUMMARY: Leafhoppers depend on plant sap as their food source, which is inherently unbalanced in terms of nutrition. To compensate for this deficiency, leafhoppers rely on obligate symbiotic bacterial associations to acquire the amino acids that are lacking in their diet. In this study, we focused on Maiestas dorsalis to understand the distribution of two obligate symbiotic bacteria, Sulcia muelleri and Nasuia deltocephalinicola, within the insect and their vertical transmission pathways. Our findings revealed their spatial arrangement within specialized tissues and provide insights into their genomic characteristics. We discovered that these bacteria undergo significant genome reduction but still retain the ability to synthesize essential amino acids for the leafhopper. This study enhances our understanding of the coevolutionary processes and nutritional interactions in Auchenorrhyncha insects, contributing to our knowledge of the intricate symbiotic relationships in nature. 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.