Diversity and Evolution of the Phenazine Biosynthesis Pathway

Authors: MAVRODI, DMITRI - Washington State University; PEEVER, TOBIN - Washington State University; MAVRODI, OLGA - Washington State University; PAREJKO, JAMES - Washington State University; RAAIJMAKERS, JOS - Wageningen University; LEMANCEAU, PHILIPPE - Institut National De La Recherche Agronomique (INRA); MAZURIER, SYLVIE - Institut National De La Recherche Agronomique (INRA); HEIDE, LUTZ - Eberhard-Karls University; BLANKENFELDT, WULF - Max Planck Society; Thomashow, Linda; Weller, David

Submitted to: Applied and Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/1/2009
Publication Date: 2/20/2010
Citation: Mavrodi, D.V., Peever, T.L., Mavrodi, O.V., Parejko, J.A., Raaijmakers, J.M., Lemanceau, P., Mazurier, S., Heide, L., Blankenfeldt, W., Thomashow, L.S., Weller, D.M. 2010. Diversity and Evolution of the Phenazine Biosynthesis Pathway. Applied and Environmental Microbiology. Feb, 2010, p. 866-879.

Interpretive Summary: The ability to produce phenazine antibiotics is a specialized property of certain bacterial strains isolated from soils and clinical settings. In soils, these antibiotics contribute to the competitiveness of the strains that produce them, whereas they are a factor in the pathogenicity of bacteria infecting immunocompromised individuals. Here, we used DNA sequence analysis to study the distribution and evolution of phenazine biosynthesis genes among 94 different phenazine-producing bacteria of various origins. Our results indicate that the phenazine genes are highly conserved among some bacteria, many of which are plant-associated, but that the genes can be transferred horizontally among certain other bacterial groups. Several different variants of phenazine genes were detected in DNA extracted directly from soils in central Washington State in which wheat had been grown, providing the first example of a soil enriched in populations of phenazine-producing bacteria.

Technical Abstract: Phenazines are versatile secondary metabolites of bacterial origin that function in biological control of plant pathogens and contribute to the ecological fitness and pathogenicity of the producing strains. In this study, we employed a collection of 94 strains of various geographic, environmental and clinical origins to study the distribution and evolution of phenazine genes in economically important groups of bacteria. Our results confirmed the extensive diversity of phenazine producers and revealed that most of them appear to be soil-dwelling and/or plant-associated species. Genome analyses and comparisons of phylogenies inferred from sequences of the key phenazine biosynthesis phzF and housekeeping genes (16S, recA, rpoB, atpD, and gyrB) revealed that the evolution and dispersal of phenazine genes is driven by mechanisms ranging from conservation in Pseudomonas spp. to horizontal gene transfer in Burkholderia spp. and members of Enterobacteriaceae. DNA extracted from cereal crop rhizospheres and screened for the presence of phzF contained sequences consistent with a diverse population of phenazine-producers in commercial farm fields located in central Washington State, thus providing the first example of U.S. soils enriched in indigenous phenazine-producing bacteria.