Submitted to: Applied and Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/27/2003
Publication Date: 3/1/2004
Citation: Brodhagen, M., Henkels, M.D., Loper, J.E. 2004. Positive autoregulation of the antibiotic pyoluteorin in the biological control organism Pseudomonas fluorescens Pf-5. Applied and Environmental Microbiology. 70:1758-1766. Interpretive Summary: Pseudomonas fluorescens strain Pf-5 is a naturally-occuring bacterium that inhabits the surfaces of plant roots and functions as a biological control agent, protecting roots from infection by pathogens that live in the soil. Pf-5 produces many antibiotics that are toxic to plant pathogens. Because these antibiotics are critical to the success of biological control, we study factors that influence antibiotic production by Pf-5. This paper describes a recent discovery that very small concentrations of one of the antibiotics, called pyoluteorin or PLT, induced its own production by Pf-5. This induction occured in bacteria grown in culture, and also in bacteria inhabiting root surfaces. The discovery that PLT functions as a signal molecule in a natural environment is important because it provides insight into an age-old question about the role of antibiotics in microbial ecology and because PLT signaling was identified as a factor influencing the success of Pf-5 in the biological control of plant diseases.
Technical Abstract: Pseudomonas fluorescens Pf-5, a rhizosphere bacterium, produces a suite of secondary metabolites that are toxic to seed- and-root-rotting plant pathogens. Among these are the polyketide compounds pyoluteorin (PLT) and 2,4-diacetylphloroglucinol (2,4,DAPG). We provide evidence that PLT production is influenced by positive autoregulation. Addition of PLT to liquid cultures of Pf-5 enhanced PLT production. In addition, PLT and 2,4-DAPG mutually inhibit one another's production in Pf-5. For PLT, both positive autoregulation and negative influences on production by 2,4-DAPG were demonstrated at the transcriptional level, by measuring activity from transcriptional fusions of an ice nucleation reporter gene to three separate PLT biosynthetic genes. The occurrence of PLT autoregulation in the rhizosphere was assessed on cucumber seedlings in pasteurized soil, using cross-feeding experiments. In the rhizosphere, a Plt-minus derivative of Pf-5 carrying a reporter gene fusion to a PLT biosynthetic gene responded positively to PLT produced by coinoculated cells of Pf-5 or a derivative. These data establish that PLT is an autoregulatory compound and functions as a signal molecule influencing the spectrum of secondary metabolites produced by the bacterial cell.