Phenazine-1-carboxylic acid and soil moisture influence biofilm development and turnover of rhizobacterial biomass on wheat root surfaces

Authors: LETOURNEAU, MELISSA - Washington State University; MARSHALL, MATTHEW - Pacific Northwest National Laboratory; CLIFF, JOHN - Pacific Northwest National Laboratory; BONSALL, ROBERT - Washington State University; MAVRODI, DMITIR - University Of Southern Mississippi; DEVI, S - Washington State University; MAVRODI, OLGA - University Of Southern Mississippi; HARSH, JAMES - Washington State University; Weller, David; Thomashow, Linda

Submitted to: Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/15/2018
Publication Date: 6/20/2018
Citation: Letourneau, M.K., Marshall, M.J., Cliff, J.B., Bonsall, R.F., Mavrodi, D.V., Devi, S.I., Mavrodi, O.V., Harsh, J.B., Weller, D.M., Thomashow, L.S. 2018. Phenazine-1-carboxylic acid and soil moisture influence biofilm development and turnover of rhizobacterial biomass on wheat root surfaces. Environmental Microbiology. https://doi.org/10.1111/1462-2920.14244.
DOI: https://doi.org/10.1111/1462-2920.14244

Interpretive Summary: Dryland wheat fields grown throughout the Columbia Plateau of the Inland Pacific Northwest (PNW) of the USA harbor large populations of Pseudomonas bacteria that produce phenazine-1-carboxylic acid (PCA) on the roots. This antibiotic has an important role in plant defense against fungal root pathogens and is known to promote the formation of biofilms that surround and protect bacterial colonies grown in culture. We used powerful microscopy techniques to demonstrate (1) that bacteria producing PCA form more extensive biofilms on wheat roots than do bacteria that no longer have the ability to produce the antibiotic; (2) biofilm formation was more extensive on roots of wheat grown under dryland conditions than on roots of irrigated wheat; and (3) the presence of biofilms was correlated with enhanced preservation of soil organic matter and nutrient incorporation into root cells. We conclude from this work that PCA-producing bacteria present under dryland conditions are protected by biofilms that also influence crop nutrition and soil health in dryland wheat fields.

Technical Abstract: Rhizobacterial biofilm development influences terrestrial carbon and nitrogen cycles with ramifications for crop and soil health. Phenazine-1-carboxylic acid (PCA) is a redox-active metabolite produced by rhizobacteria in dryland wheat fields of Washington and Oregon, USA. PCA promotes biofilm development in bacterial cultures and bacterial colonization of wheat rhizospheres. However, its impact upon biofilm development has not been demonstrated in the rhizosphere, nor have the relationships between soil moisture and the rates of PCA biosynthesis and degradation been established. In this study, expression of PCA biosynthesis genes was up-regulated relative to background transcription, and persistence of PCA was slightly decreased in dryland relative to irrigated wheat rhizospheres. Biofilms in dryland rhizospheres inoculated with the PCA-producing (PCA+) strain Pseudomonas synxantha 2-79RN10 were more robust than in rhizospheres inoculated with an isogenic PCA-deficient (PCA ) mutant strain, and few biofilms were observed in irrigated rhizospheres. In dryland PCA+ rhizospheres, the turnover of some 15N-labelled rhizobacterial biomass was slower than in the other treatments, and incorporation of bacterial 15N into root cell walls was observed in multiple treatments. These results indicate that PCA promotes biofilm development in dryland rhizospheres, and likely influences crop nutrition and soil health in dryland wheat fields.