Deciphering the antifungal and plant growth-stimulating traits of the stress-tolerant Streptomyces achromogenes subsp. achromogenes strain UMAF16, a bacterium isolated from soils affected by underground fires

Abstract

Crop plants are subjected to diverse abiotic and biotic stresses, which could affect their health and production. Therefore, searching for novel stress-resistant microbial agents with plant-beneficial activities is considered an urgent in agriculture. Here, we report the new stress tolerant bacterium Streptomyces achromogenes subsp. achromogenes UMAF16, isolated from a soil subjected to underground fires. Taxonomic and Genomic analysis derived from ANI (average nucleotide identity) species delimitation cut-off values, GGDC (genome-to-genome distance calculator), and phylogenetic analysis, corroborated the affiliation of UMAF16 to Streptomyces species. Genome mining of UMAF16 shows an excellent arsenal of stress tolerant genes (e.g. temperature, osmotic, and oxidative stress), as well as antifungal and plant growth-promoting mechanisms. Additionally, antiSMASH revealed multiple biosynthetic genes with antimicrobial (e.g. Achromosin, Livipeptin, Neocarazostatin A) and PGP activities (e.g. siderophores like Desferrioxamin B/Desferrioxamine E). To further confirmed previous predicted activities, it was biochemically evaluated the antifungal and plant growth-promoting mechanisms, including production of indole-3-acetic acid (IAA), proteases, siderophores, biofilm formation, and phosphate solubilization. Our results also show that strain UMAF16 grows well at temperature 50 °C, tolerates dehydration stress simulated by polyethylene glycol, and exert antifungal action against pathogens like Alternaria alternata, Mucor fragilis and Fusarium brachygibbosum. Strain UMAF16 also showed growth-stimulating activities when interacting with tomato plants, evaluated under three different plant-growth systems. Root and shoot dry weight, as well as chlorophyll content were increased in inoculated plants, compared to uninoculated controls. Finally, these results suggest a great potential of the strain UMAF16 as a bioinoculant candidate agent in stressful agriculture.