5 Insect vectors efficiently convey complex endophytic communities across grapevine plants

Microbial endophytes colonize the inner tissues of plants. It is commonly held that most endophytes invade the host tissues through the roots or through discontinuities on the plant surface, including wounds and stomata. Microorganisms can also be transferred through root anastomoses, as it occurs for instance with some pathogenic mollicutes, such as the phytoplasmas. Some insects able to penetrate the plant surface are also vectors of phytoplasmas. Very little is known about the ability of such vectors to harbour and transfer other microorganisms. To unravel the ecological role of insects for endophytic microorganisms, we used freshly hatched nymphs of the sap-feeding leafhopper Scaphoideus titanus (vector) to transport microorganisms across grapevine plants. We used adult, greenhouse-grown (donor) plants with an established endophytic fauna, and micropropagated (acceptor) grapevines hosting no detectable bacteria. We used 454 pyrosequencing of the bacterial 16S rDNA gene to estimate the composition of bacterial endophytic communities in donor plants, vector insects and acceptor plants, and to track microbial communities along the insect-plant-microbe network. After contact with the vector, acceptor plants were colonized by a complex endophytic community dominated by Proteobacteria, highly similar to that present on donor plants. Interestingly, a similar bacterial community, but with a higher ratio of firmicutes, was found on S. titanus. Insects feeding only on acceptor plants transferred an entirely different bacterial community dominated by Actinobacteria, where the opportunistic human pathogen Mycobacterium abscessus played a major role. Despite the fact that insects dwelled mostly on plant stems, the bacterial communities in plant roots resembled more closely those inside and on insects, when compared with above-ground plants. We establish here for the first time the potential of insect vectors to transfer entire bacterial communities across plants. We also define the probiotic role of plants and microbial endophytes in establishing microbial communities in plant-feeding insects.