Oligomycin-producing Streptomyces sp. newly isolated from Swiss soils efficiently protect Arabidopsis thaliana against Botrytis cinerea.

Botrytis cinerea is a necrotrophic phytopathogen able to attack more than 200 different plant species causing strong yield losses worldwide. Many synthetic fungicides have been developed to control this disease, resulting in the rise of fungicide-resistance B. cinerea strains. The aim of this study was to identify Streptomyces strains showing antagonistic activity against B. cinerea to contribute to plant protection in an environmentally friendly way. We isolated 15 Actinomycete strains from 9 different Swiss soils. The culture filtrates of three isolates showing antifungal activity inhibited spore germination and delayed mycelial growth of B. cinerea. Infection experiments showed that Arabidopsis thaliana plants were more resistant to this pathogen after leaf treatment with the Streptomyces filtrates. Bioassay-guided isolation of the active compounds revealed the presence of germicidins A and B as well as of oligomycins A, B, and E. While germicidins were mostly inactive, oligomycin B reduced the mycelial growth of B. cinerea significantly. Moreover, all three oligomycins inhibited this fungus' spore germination, suggesting that these molecules might contribute to the Streptomyces's ability to protect plants against infection by the broad host-pathogen Botrytis cinerea. IMPORTANCE: This study reports the isolation of new Streptomyces strains with strong plant-protective potential mediated by their production of specialized metabolites. Using the broad host range pathogenic fungus Botrytis cinerea, we demonstrate that the cell-free filtrate of selected Streptomyces isolates efficiently inhibits different developmental stages of the fungus, including mycelial growth and the epidemiologically relevant spore germination. Beyond in vitro experiments, the strains and their metabolites also efficiently protected plants against the disease caused by this pathogen. This work further identifies oligomycins as active compounds involved in the observed antifungal activity of the strains. This work shows that we can harness the natural ability of soil-borne microbes and of their metabolites to efficiently fight other microbes responsible for significant crop losses. This opens the way to the development of environmentally friendly health protection measures for crops of agronomical relevance, based on these newly isolated strains or their metabolic extracts containing oligomycins.

Comparative genomic and metabolomic study of three Streptomyces sp. differing in biological activity.

The Streptomyces genus is known to produce many specialized metabolites of value for medicine, but the potential of these metabolites in agronomy remains largely unexplored. In this study, we investigated three phylogenetically closely related Streptomyces strains (B5, B91, and B135) isolated from three distinct soil samples in Sudan. Despite belonging to the same species, these strains exhibited different ranges of Phytophthora infestans inhibition. The objective of this work was to identify the active compound(s) responsible for the inhibition of P. infestans and of other plant pathogens by comparing the genomes and metabolomes of the three strains which showed distinct activity patterns: B5 was the strongest inhibitor of oomycetes, B5 and B91 both inhibited most fungi and B135 was the only strain showing antibacterial activity. Our comparative genomic and metabolomic analysis identified borrelidin as the bioactive compound underlying B5's strong anti-oomycete activity and highlighted a few other metabolites as putative candidates underlying the strains' antifungal and antibacterial activities. This study illustrates the power of comparative genomics and metabolomics on phylogenetically closely related strains of differing activities to highlight bioactive compounds that could contribute to new sustainable crop protection strategies.

Evaluating the Antagonistic Potential of Actinomycete Strains Isolated From Sudan's Soils Against Phytophthora infestans.

Soil microorganisms play crucial roles in soil fertility, e.g., through decomposing organic matter, cycling nutrients or through beneficial interactions with plants. Actinomycetes are a major component of soil inhabitants; they are prolific producers of specialized metabolites, among which many antibiotics. Here we report the isolation and characterization of 175 Actinomycetes from rhizosphere and bulk soil samples collected in 18 locations in Sudan. We evaluated the strains' metabolic potential for plant protection by testing their ability to inhibit the mycelial growth of the oomycete Phytophthora infestans, which is one of the most devastating plant pathogens worldwide. Most strains significantly reduced the oomycete's growth in direct confrontational in vitro assays. A significant proportion of the tested strains (15%) were able to inhibit P. infestans to more than 80%, 23% to 50%-80%, while the remaining 62% had inhibition percentages lesser than 50%. Different morphologies of P. infestans mycelial growth and sporangia formation were observed upon co-inoculation with some of the Actinomycetes isolates, such as the production of fewer, thinner hyphae without sporangia leading to a faint growth morphology, or on the contrary, of clusters of thick-walled hyphae leading to a bushy, or "frozen" morphology. These morphologies were caused by strains differing in activity levels but phylogenetically closely related with each other. To evaluate whether the isolated Actinomycetes could also inhibit the pathogen's growth in planta, the most active strains were tested for their ability to restrict disease progress in leaf disc and full plant assays. Five of the active strains showed highly significant protection of potato leaves against the pathogen in leaf disc assays, as well as substantial reduction of disease progress in full plants assays. Using cell-free filtrates instead of the bacterial spores also led to full protection against disease on leaf discs, which highlights the strong crop protective potential of the secreted metabolites that could be applied as leaf spray. This study demonstrates the strong anti-oomycete activity of soil- and rhizosphere-borne Actinomycetes and highlights their significant potential for the development of sustainable solutions based on either cell suspensions or cell-free filtrates to safeguard potatoes from their most damaging pathogen.