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

Melissa K. LeTourneau, Matthew J. Marshall, John B. Cliff, Robert F. Bonsall, Alice C. Dohnalkova, Dmitri V. Mavrodi, S. Indira Devi, Olga V. Mavrodi, James B. Harsh, David M. Weller, Linda S. Thomashow

Research output: Contribution to journalArticlepeer-review

34 Scopus citations

Abstract

Phenazine-1-carboxylic acid (PCA) is produced by rhizobacteria in dryland but not in irrigated wheat fields of the Pacific Northwest, 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, where biofilms influence terrestrial carbon and nitrogen cycles with ramifications for crop and soil health. Furthermore, the relationships between soil moisture and the rates of PCA biosynthesis and degradation have not been established. In this study, expression of PCA biosynthesis genes was upregulated 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 those in rhizospheres inoculated with an isogenic PCA-deficient (PCA-) mutant strain. This trend was reversed in irrigated rhizospheres. In dryland PCA+ rhizospheres, the turnover of 15N-labelled rhizobacterial biomass was slower than in the PCA- and irrigated PCA+ 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.

Original languageEnglish
Pages (from-to)2178-2194
Number of pages17
JournalEnvironmental Microbiology
Volume20
Issue number6
DOIs
StatePublished - Jun 2018

Funding

We thank Daryl Stacks, Jacob Mullins and Karen Hansen for their assistance with the experimental procedures; Dr. Markus Flury for consultation regarding soil moisture monitoring and control; Dr. James Moran for providing the NanoSIMS yeast standard; and Drs. Valerie Lynch-Holm, Vaithiyalingam Shutthanandan, Bruce Arey, Christine Davitt and Daniel Mullendore for training and assistance with SEM, HIM and TEM sample preparation and imaging. This work was funded by the Harry E. Goldsworthy Wheat Research Fund and the Otto and Doris Amen Dryland Research Endowment administered by Washington State University (WSU); Agriculture and Food Research Initiative Competitive Grant No. 2090-22000-016-07 from the USDA National Institute of Food and Agriculture; the Office of Science Graduate Student Research (SCGSR) program administered by the Oak Ridge Institute for Science and Education for the U.S. Department of Energy (DOE), Office of Science, Office of Workforce Development for Teachers and Scientists under contract number DE-SC0014664; and a DOE Office of Science Early Career Research Award (Project No. 60385). A portion of this work was conducted at the Franceschi Microscopy & Imaging Center at WSU, and at the Environmental Molecular Sciences Laboratory (EMSL), a DOE Office of Science User Facility sponsored by the Office of Biological and Environmental Research and located at Pacific Northwest National Laboratory (PNNL), a multiprogram national laboratory operated by Batelle for the U.S. Department of Energy under Contract DE-AC05-76RL01830. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture. USDA is an equal opportunity provider and employer. We thank Daryl Stacks, Jacob Mullins and Karen Hansen for their assistance with the experimental procedures; Dr. Markus Flury for consultation regarding soil moisture monitoring and control; Dr. James Moran for providing the NanoSIMS yeast standard; and Drs. Valerie Lynch-Holm, Vaithiyalingam Shut-thanandan, Bruce Arey, Christine Davitt and Daniel Mullen-dore for training and assistance with SEM, HIM and TEM sample preparation and imaging. This work was funded by the Harry E. Goldsworthy Wheat Research Fund and the Otto and Doris Amen Dryland Research Endowment administered by Washington State University (WSU); Agriculture and Food Research Initiative Competitive Grant No. 2090-22000-016-07 from the USDA National Institute of Food and Agriculture; the Office of Science Graduate Student Research (SCGSR) program administered by the Oak Ridge Institute for Science and Education for the U.S. Department of Energy (DOE), Office of Science, Office of Workforce Development for Teachers and Scientists under contract number DE-SC0014664; and a DOE Office of Science Early Career Research Award (Project No. 60385). A portion of this work was conducted at the Franceschi Microscopy & Imaging Center at WSU, and at the Environmental Molecular Sciences Laboratory (EMSL), a DOE Office of Science User Facility sponsored by the Office of Biological and Environmental Research and located at Pacific Northwest National Laboratory (PNNL), a multiprogram national laboratory operated by Batelle for the U.S. Department of Energy under Contract DE-AC05-76RL01830. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture. USDA is an equal opportunity provider and employer.

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