A multi-partner symbiotic community inhabits the emerging insect pest Pentastiridius leporinus

The planthopper Pentastiridius leporinus has emerged as a severe crop pest, rapidly expanding both its host plant range and the affected areas in central Europe. Originating as a monophagous herbivore of reed grass, P. leporinus recently adopted polyphagous feeding and is now a pest of sugar beet, potato, carrot, and onion, suggesting rapid ecological niche expansion. P. leporinus vectors two bacterial pathogens: the γ-proteobacterium Candidatus Arsenophonus phytopathogenicus (CAP) and the stolbur phytoplasma Candidatus Phytoplasma solani (CPS), which are responsible for a range of disease syndromes, including syndrome basses richesses in sugar beet. We used long-read metagenomic sequencing to characterize the genomes of microbes associated with P. leporinus, resulting in the complete sequences of CAP and CPS, as well as obligate symbionts of the genera Purcelliella, Karelsulcia, and Vidania, and facultative symbionts Rickettsia and Wolbachia. The obligate symbionts are inferred to provide or contribute to the biosynthesis of 10 essential amino acids and to B vitamin. The genomes of CPS and CAP encode numerous pathogenicity factors, enabling the colonization of different hosts. Bacterial fluorescence in situ hybridization revealed the tissue distribution, cellular localization, relative abundance, and transmission patterns of these bacteria. The intracellular presence of all obligate symbionts in bacteriomes, the intracellular presence of Wolbachia, and the intranuclear localization of Rickettsia suggest vertical transmission. CPS was restricted to salivary glands, suggesting strict horizontal, plant-mediated transmission, whereas CAP colonized all tissue types, allowing for horizontal and vertical transmission. Our data suggest that P. leporinus hosts an exceptionally broad range of symbionts, encompassing mutualistic, commensal, and pathogenic interactions.IMPORTANCEThe planthopper Pentastiridius leporinus has recently expanded its host plant range and emerged as a severe pest of sugar beet and potato crops in central Europe, which is exacerbated by its capacity to vector bacterial pathogens to its host plants. Because microbial symbionts may play an important role for both the host plant shifts and the transmission of pathogens, we used metagenomic sequencing and fluorescence in situ hybridization to characterize the microbial community associated with P. leporinus. We detected three bacteriome-localized obligate symbionts that together provision all essential amino acids and several B-vitamins to the host, as well as two intracellular bacteria with a broader tissue distribution. In addition, we infer localization, transmission, and putative pathogenicity factors for the two major phytopathogens that are vectored by P. leporinus. Our results reveal a complex community of symbiotic bacteria that likely shapes the interaction of this emerging pest with its host plants.