Streptomyces Endophytes Promote Host Health and Enhance Growth across Plant Species

• Published in: Applied and environmental microbiology Vol. 86; no. 16; p. 1
• Main Authors: Worsley, Sarah F., Newitt, Jake, Rassbach, Johannes, Batey, Sibyl F. D., Holmes, Neil A., Murrell, J. Colin, Wilkinson, Barrie, Hutchings, Matthew I.
• Format: Journal Article
• Language: English
• Published: United States American Society for Microbiology 03.08.2020
• Subjects: Acetic acid; Antifungal activity; Antifungal agents; Antimicrobial activity; Antimicrobial agents; Arabidopsis - growth & development; Arabidopsis - microbiology; Arabidopsis - physiology; Arabidopsis thaliana; Bacteria; Endophytes; Endophytes - physiology; Environmental Microbiology; Fungi; Fungicides; Gaeumannomyces graminis tritici; Gene sequencing; Genomes; Host Microbial Interactions; Indoleacetic acid; Metabolites; Natural products; Phytosterols; Plant biomass; Plant growth; Plant roots; Plant species; Polyenes; Probiotics; Rhizosphere; Roots; Secondary metabolites; Seedlings; Seedlings - growth & development; Seedlings - microbiology; Seeds; Soil bacteria; Soil Microbiology; Spores; Streptomyces; Streptomyces - physiology; Streptomycetes; Take-all disease; Triticum - growth & development; Triticum - microbiology; Triticum - physiology; Wheat; Streptomyces; wheat; plant-microbe interactions; Arabidopsis
• ISSN: 0099-2240; 1098-5336; 1098-5336
• DOI: 10.1128/AEM.01053-20

We must reduce reliance on agrochemicals, and there is increasing interest in using bacterial strains to promote plant growth and protect against disease. Our study follows up reports that Arabidopsis thaliana specifically recruits Streptomyces bacteria to its roots. We test the hypotheses that they offer benefits to their A. thaliana hosts and that strains isolated from these plants might be used as probiotics. We isolated Streptomyces strains from A. thaliana roots and genome sequenced five phylogenetically distinct strains. Genome mining and bioassays indicated that all five have plant growth-promoting properties, including production of indole-3-acetic acid (IAA), siderophores, and aminocyclopropane-1-carboxylate (ACC) deaminase. Three strains significantly increased A. thaliana growth in vitro and in combination in soil. Another produces potent filipin-like antifungals and protected germinating wheat seeds against the fungal pathogen Gaeumannomyces graminis var. tritici (wheat take-all fungus). We conclude that introducing Streptomyces strains into the root microbiome provides significant benefits to plants. Streptomyces bacteria are ubiquitous in soils and are well known for producing secondary metabolites, including antimicrobials. Increasingly, they are being isolated from plant roots, and several studies have shown they are specifically recruited to the rhizosphere and the endosphere of the model plant Arabidopsis thaliana . Here, we test the hypothesis that Streptomyces bacteria have a beneficial effect on A. thaliana growth and could potentially be used as plant probiotics. To do this, we selectively isolated streptomycetes from surface-washed A. thaliana roots and generated high-quality genome sequences for five strains, which we named L2, M2, M3, N1, and N2. Reinfection of A. thaliana plants with L2, M2, and M3 significantly increased plant biomass individually and in combination, whereas N1 and N2 had a negative effect on plant growth, likely due to their production of polyene natural products which can bind to phytosterols and reduce plant growth. N2 exhibits broad-spectrum antimicrobial activity and makes filipin-like polyenes, including 14-hydroxyisochainin which inhibits the take-all fungus, Gaeumannomyces graminis var. tritici . N2 antifungal activity as a whole was upregulated ∼2-fold in response to indole-3-acetic acid (IAA), suggesting a possible role during competition in the rhizosphere. Furthermore, coating wheat seeds with N2 spores protected wheat seedlings against take-all disease. We conclude that at least some soil-dwelling streptomycetes confer growth-promoting benefits on A. thaliana , while others might be exploited to protect crops against disease. IMPORTANCE We must reduce reliance on agrochemicals, and there is increasing interest in using bacterial strains to promote plant growth and protect against disease. Our study follows up reports that Arabidopsis thaliana specifically recruits Streptomyces bacteria to its roots. We test the hypotheses that they offer benefits to their A. thaliana hosts and that strains isolated from these plants might be used as probiotics. We isolated Streptomyces strains from A. thaliana roots and genome sequenced five phylogenetically distinct strains. Genome mining and bioassays indicated that all five have plant growth-promoting properties, including production of indole-3-acetic acid (IAA), siderophores, and aminocyclopropane-1-carboxylate (ACC) deaminase. Three strains significantly increased A. thaliana growth in vitro and in combination in soil. Another produces potent filipin-like antifungals and protected germinating wheat seeds against the fungal pathogen Gaeumannomyces graminis var. tritici (wheat take-all fungus). We conclude that introducing Streptomyces strains into the root microbiome provides significant benefits to plants.