Microbes can establish mutualistic interactions with plants and insects. Here we track the movement of an endophytic strain of Streptomyces bacteria throughout a managed strawberry ecosystem. We show that a Streptomyces isolate found in the rhizosphere and on flowers protects both the plant and pollinating honeybees from pathogens (phytopathogenic fungus Botrytis cinerea and pathogenic bacteria, respectively). The pollinators can transfer the Streptomyces bacteria among flowers and plants, and Streptomyces can move into the plant vascular bundle from the flowers and from the rhizosphere. Our results present a tripartite mutualism between Streptomyces, plant and pollinator partners.

Background Plants in nature interact with other species, among which are mutualistic microorganisms that affect plant health. The co-existence of microbial symbionts with the host contributes to host fitness in a natural context. In turn, the composition of the plant microbiota responds to the environment and the state of the host, raising the possibility that it can be engineered to benefit the plant. However, technology for engineering the structure of the plant microbiome is not yet available. Results The loss of diversity and reduction in population density of Streptomyces globisporus SP6C4, a core microbe, was observed coincident with the aging of strawberry plants. Here, we show that glutamic acid reshapes the plant microbial community and enriches populations of Streptomyces, a functional core microbe in the strawberry anthosphere. Similarly, in the tomato rhizosphere, treatment with glutamic acid increased the population sizes of Streptomyces as well as those of Bacillaceae and Burkholderiaceae. At the same time, diseases caused by species of Botrytis and Fusarium were significantly reduced in both habitats. We suggest that glutamic acid directly modulates the composition of the microbiome community. Conclusions Much is known about the structure of plant-associated microbial communities, but less is understood about how the community composition and complexity are controlled. Our results demonstrate that the intrinsic level of glutamic acid in planta is associated with the composition of the microbiota, which can be modulated by an external supply of a biostimulant.

Streptomyces griseus S4-7 is representative of strains responsible for the specific soil suppressiveness of Fusarium wilt of strawberry caused by Fusarium oxysporum f. sp. fragariae. Members of the genus Streptomyces secrete diverse secondary metabolites including lantipeptides, heat-stable lanthionine-containing compounds that can exhibit antibiotic activity. In this study, a class II lantipeptide provisionally named grisin, of previously unknown biological function, was shown to inhibit F. oxysporum. The inhibitory activity of grisin distinguishes it from other class II lantipeptides from Streptomyces spp. Results of quantitative reverse transcription-polymerase chain reaction with lanM-specific primers showed that the density of grisin-producing Streptomyces spp. in the rhizosphere of strawberry was positively correlated with the number of years of monoculture and a minimum of seven years was required for development of specific soil suppressiveness to Fusarium wilt disease. We suggest that lanM can be used as a diagnostic marker of whether a soil is conducive or suppressive to the disease.

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