Metagenomics of the planthopper Pentastiridius leporinus

The plant hopper Pentastiridius leporinus has emerged as a severe crop pest, rapidly expanding both its host plant range and the infested areas in central Europe. Originating from a monophagous herbivore on aboveground parts of reed grass (Phragmites australis), P. leporinus recently adopted a polyphagous feeding habit, and is now a pest of sugar beet (Beta vulgaris), potato (Solanum tuberosum), carrot and onion, implicating a dynamic ecological niche expansion. P. leporinus vectors the bacterial plant pathogens ?-proteobacterium 'Candidatus Arsenophonus phytopathogenicus' and the stolbur phytoplasma 'Candidatus Phytoplasma solani' causing the disease syndrome basses richesses (SBR) in sugar beet and potato fields. Here, we used long read metagenomic sequencing to identify the vectored plant pathogens and P. leporinus primary symbionts belonging to the genera Purcelliella, Sulcia and Vidania as well as the facultative symbionts Rickettsia and Wolbachia. High-resolution bacterial fluorescent in situ hybridization (BAC-FISH) revealed tissue distribution, cellular localization, relative abundances and potential transmission patterns of the identified bacteria. The determined intracellular presence of all primary symbionts in specialized bacteriomes and the distribution of Wolbachia and Rickettsia suggest vertical transmission of these symbionts. Phytoplasma was found to be restricted to salivary glands, suggesting a strict horizontal, plant-mediated transmission, while Arsenophonus occurred across all tissue types, allowing both horizontal and vertical transmission. Our data suggest that P. leporinus is host to an exceptionally broad range of symbionts, and includes mutualistic, commensal and potential pathogenic interactions with the bacteria housed in specialized organs, restricted to a single tissue, localized to insect nuclei or widely distributed across all tissues.