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

Author
item MAVRODI, DMITRI - Washington State University
item MAVRODI, OLGA - Washington State University
item PAREJKO, JAMES - Washington State University
item BONSALL, ROBERT - Washington State University
item KWAK, YOUN-SIG - Washington State University
item Paulitz, Timothy
item Thomashow, Linda
item Weller, David

Submitted to: Applied and Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/2/2011
Publication Date: 2/1/2012
Citation: Mavrodi, D.V., Mavrodi, O.V., Parejko, J.A., Bonsall, R.F., Kwak, Y., Paulitz, T.C., Thomashow, L.S., Weller, D.M. 2012. Accumulation of the Antibiotic Phenazine-1-Carboxylic Acid in the Rhizosphere of Dryland Cereals. Applied and Environmental Microbiology. 78:804-812.

Interpretive Summary: Many microorganisms produce natural antibiotics in the environment. Considerable evidence has accumulated that these substances have diverse roles in microbial fitness, competitiveness, and interactions in microbial habitats. Much less is known about the amounts of antibiotics produced and the area over which they are distributed in nature. In this study we mapped the distribution of bacteria producing the natural antibiotic phenazine-1-carboxylic acid (PCA) on roots of wheat growing throughout dryland areas (less than 13.8 inches of annual precipitation) of Inland Washington State, USA. We found PCA-producing bacteria on the roots of plants collected from all of 61 commercial wheat fields distributed over an area of 8,500 square miles. Population sizes of the bacteria varied from as few as a thousand to over ten million per gram of fresh roots, and greater numbers of root systems were colonized by the bacteria in drier areas as compared to areas with greater annual precipitation. We also recovered small quantities of PCA directly from the roots of wheat grown in 26 of 29 fields that we sampled and showed that greater numbers of bacteria on the roots resulted in larger amounts of PCA recovered. This is the first demonstration of the accumulation of significant quantities of a natural antibiotic across a large area of land. Our results strongly suggest that natural antibiotics can accumulate on the roots of plants in amounts sufficient not only for communication among microorganisms, but also for the direct inhibition of sensitive organisms.

Technical Abstract: Natural antibiotics are thought to function in the defense, fitness, competitiveness, biocontrol activity, communication and gene regulation of microorganisms. However, the scale and quantitative aspects of antibiotic production in natural settings are poorly understood. We addressed these fundamental questions by assessing the geographic distribution of indigenous phenazine-producing (Phz+) Pseudomonas spp. and accumulation of the broad-spectrum antibiotic phenazine-1-carboxylic acid (PCA) in the rhizosphere of wheat grown in the low-precipitation zone (<350 mm) of the Columbia Plateau, USA, and in adjacent higher precipitation areas. Plants were collected from 61 commercial wheat fields located within an area of about 22,000 km2. Phz+ Pseudomonas spp. were detected in all sampled fields, with mean population sizes ranging from log 3.2 to log 7.1 g-1 fresh weight of root. Linear regression analysis demonstrated a significant inverse relationship between annual precipitation and the proportion of plants colonized by Phz+ Pseudomonas spp. (r2=0.36, P =0.0001). PCA was detected in as much as nanomolar amounts in the rhizosphere of plants from 26 of 29 fields that were selected for antibiotic quantitation. There was a direct relationship between the amount of PCA extracted from the rhizosphere and population density of Phz+ pseudomonads (r2=0.46, P =0.0006). This is the first demonstration of accumulation of significant quantities of a natural antibiotic across a terrestrial ecosystem. Our results strongly suggest that natural antibiotics can transiently accumulate in the plant rhizosphere in amounts sufficient not only for inter- and intraspecies signaling, but also for the direct inhibition of sensitive organisms.