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Biosurfactants Produced by Phyllosphere-Colonizing Pseudomonads Impact Diesel Degradation but Not Colonization of Leaves of Gnotobiotic Arabidopsis thaliana.

ABSTRACT: Biosurfactant production is a common trait in leaf surface-colonizing bacteria that has been associated with increased survival and movement on leaves. At the same time, the ability to degrade aliphatics is common in biosurfactant-producing leaf colonizers. Pseudomonads are common leaf colonizers and have been recognized for their ability to produce biosurfactants and degrade aliphatic compounds. In this study, we investigated the role of biosurfactants in four non-plant-pathogenic Pseudomonas strains by performing a series of experiments to characterize their surfactant properties and their role during leaf colonization and diesel degradation. The biosurfactants produced were identified using mass spectrometry. Two strains produced viscosin-like biosurfactants, and the other two produced massetolide A-like biosurfactants, which aligned with the phylogenetic relatedness between the strains. To further investigate the role of surfactant production, random Tn5 transposon mutagenesis was performed to generate knockout mutants. The knockout mutants were compared to their respective wild types with regard to their ability to colonize gnotobiotic Arabidopsis thaliana and to degrade diesel or dodecane. It was not possible to detect negative effects during plant colonization in direct competition or individual colonization experiments. When grown on diesel, knockout mutants grew significantly slower than their respective wild types. When grown on dodecane, knockout mutants were less impacted than during growth on diesel. By adding isolated wild-type biosurfactants, it was possible to complement the growth of the knockout mutants.IMPORTANCE Many leaf-colonizing bacteria produce surfactants and are able to degrade aliphatic compounds; however, whether surfactant production provides a competitive advantage during leaf colonization is unclear. Furthermore, it is unclear if leaf colonizers take advantage of the aliphatic compounds that constitute the leaf cuticle and cuticular waxes. Here, we tested the effect of surfactant production on leaf colonization, and we demonstrate that the lack of surfactant production decreases the ability to degrade aliphatic compounds. This indicates that leaf surface-dwelling, surfactant-producing bacteria contribute to degradation of environmental hydrocarbons and may be able to utilize leaf surface waxes. This has implications for plant-microbe interactions and future studies.

SUBMITTER: Oso S

PROVIDER: S-EPMC8091026 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Natural control of phytopathogenic microorganisms is assumed as a priority function of the commensal plant microbiota. In this study, the suitability of fluorescent pseudomonads in the phyllosphere of crop plants as natural control agents was evaluated. Under field conditions, ears of winter wheat were found to be colonized with high consistency and at a high density by pseudomonads at the late milk dough stage. Isolates of these bacteria were evaluated for their potential to protect the plants from phytopathogenic Alternaria and Fusarium fungi. More Pseudomonas isolates were antagonistically active against alternaria than against fusaria in the dual culture test. The alternaria responded species-specifically and more sensitively to bacterial antagonism than the strain-specific reacting fusaria. A total of 110 randomly selected Pseudomonas isolates were screened for genes involved in the biosynthesis of the antibiotics 2,4-diacetylphloroglucinol, phenazine-1-carboxylic acid, pyoluteorin, and pyrrolnitrin. The key gene for production of the phloroglucinol was found in none of these isolates. At least one of the genes, encoding the biosynthesis of the other antibiotics was detected in 81% of the isolates tested. However, the antagonistic effect found in the dual culture assay was not necessarily associated with the presence of these antibiotic genes. Wheat grains as natural substrate were inoculated with selected antagonistic Pseudomonas isolates and Alternaria and Fusarium strains, respectively. The fungal growth was only slightly delayed, but the mycotoxin production was significantly reduced in most of these approaches. In conclusion, the distribution of phytopathogenic fungi of the genera Alternaria and Fusarium in the field is unlikely to be inhibited by naturally occurring pseudomonads, also because the bacterial antagonists were not evenly distributed in the field. However, pseudomonads can reduce the production of Alternaria and Fusarium mycotoxins in wheat grains and thus have the potential to improve the crop quality.

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Biosurfactants Produced by Phyllosphere-Colonizing Pseudomonads Impact Diesel Degradation but Not Colonization of Leaves of Gnotobiotic Arabidopsis thaliana.

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