Phenazine antibiotics produced by fluorescent pseudomonads contribute to natural soil suppressiveness to Fusarium wilt

Abstract

Natural disease-suppressive soils provide an untapped resource for the discovery of novel beneficial microorganisms and traits. For most suppressive soils, however, the consortia of microorganisms and mechanisms involved in pathogen control are unknown. To date, soil suppressiveness to Fusarium wilt disease has been ascribed to carbon and iron competition between pathogenic Fusarium oxysporum and resident non-pathogenic F. oxysporum and fluorescent pseudomonads. In this study, the role of bacterial antibiosis in Fusarium wilt suppressiveness was assessed by comparing the densities, diversity and activity of fluorescent Pseudomonas species producing 2,4-diacetylphloroglucinol (DAPG) (phlD+) or phenazine (phzC+) antibiotics. The frequencies of phlD+ populations were similar in the suppressive and conducive soils but their genotypic diversity differed significantly. However, phlD genotypes from the two soils were equally effective in suppressing Fusarium wilt, either alone or in combination with non-pathogenic F. oxysporum strain Fo47. A mutant deficient in DAPG production provided a similar level of control as its parental strain, suggesting that this antibiotic does not play a major role. In contrast, phzC+ pseudomonads were only detected in the suppressive soil. Representative phzC+ isolates of five distinct genotypes did not suppress Fusarium wilt on their own, but acted synergistically in combination with strain Fo47. This increased level of disease suppression was ascribed to phenazine production as the phenazine-deficient mutant was not effective. These results suggest, for the first time, that redox-active phenazines produced by fluorescent pseudomonads contribute to the natural soil suppressiveness to Fusarium wilt disease and may act in synergy with carbon competition by resident non-pathogenic F. oxysporum.

Irrigation Differentially Impacts Populations of Indigenous Antibiotic-Producing Pseudomonas spp. in the Rhizosphere of Wheat

“…These two groups of Pseudomonas spp. are of special interest because they are wellstudied, highly effective biological control agents (19,35) and contribute to the natural suppressiveness of soils to certain soilborne diseases (22,35,36). This study was prompted by the recent report of Mavrodi et al (20), who found that Phz ϩ Pseudomonas spp.…”

“…have especially important roles in the promotion of plant growth and the suppression of soilborne diseases of wheat and other crops (12,13,33). For example, isolates of Pseudomonas fluorescens that produce the broad-spectrum polyketide antibiotic 2,4-diacetylphloroglucinol (2,4-DAPG) are responsible for the natural suppression of take-all in the Pacific Northwest (35), and phenazine-producing pseudomonads contribute to the natural suppression of Fusarium wilt in soils of the Châteaurenard region of France (22).…”

Accumulation of the Antibiotic Phenazine-1-Carboxylic Acid in the Rhizosphere of Dryland Cereals

“…tritici, the take-all pathogen of wheat. In the Châteaurenard region of Dijon, France, indigenous phenazine-producing bacteria working in concert with nonpathogenic Fusarium oxysporum form the basis of natural disease suppression in these Fusarium wiltsuppressive soils (26,43). In the inland Pacific Northwest, root and crown rots caused by Fusarium culmorum, Fusarium pseudograminearum, Rhizoctonia solani AG-8, and Rhizoctonia oryzae are common soilborne diseases of dryland wheat for which commercial varieties lack resistance (6,31).…”

An Interspecies Signaling System Mediated by Fusaric Acid Has Parallel Effects on Antifungal Metabolite Production by Pseudomonas protegens Strain Pf-5 and Antibiosis of Fusarium spp

“…Pseudomonas spp. are prominent members of the suppressive soil microflora, as components of Fusarium-suppressive soils (23)(24)(25) or as strains applied to seeds, soil, or plant growth media to achieve biological control (23,(26)(27)(28)(29). Among the strains of Pseudomonas spp.…”