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

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 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 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.

Authors:
 [1]; ORCiD logo [2];  [3];  [4];  [3]; ORCiD logo [5];  [6];  [5];  [1];  [7]; ORCiD logo [7]
  1. Department of Crop & Soil Sciences, Washington State University, Pullman WA 99164-6420 USA
  2. Earth & Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland WA 99352 USA
  3. Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland WA 99352 USA
  4. Department of Plant Pathology, Washington State University, Pullman WA 99164-6420 USA
  5. Department of Biological Sciences, University of Southern Mississippi, Hattiesburg MS 39406-0001 USA
  6. Institute of Bioresources and Sustainable Development, Takyelpat Manipur Imphal 795001 India
  7. United States Department of Agriculture - Agricultural Research Service, Wheat Health, Genetics, and Quality Research Unit, Pullman WA 99164-6430 USA
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1468485
Report Number(s):
PNNL-SA-134049
Journal ID: ISSN 1462-2912
DOE Contract Number:  
AC05-76RL01830
Resource Type:
Journal Article
Journal Name:
Environmental Microbiology
Additional Journal Information:
Journal Volume: 20; Journal Issue: 6; Journal ID: ISSN 1462-2912
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
Phenazine, biofilm, wheat

Citation Formats

LeTourneau, Melissa K., Marshall, Matthew J., Cliff, John B., Bonsall, Robert F., Dohnalkova, Alice C., Mavrodi, Dmitri V., Devi, S. Indira, Mavrodi, Olga V., Harsh, James B., Weller, David M., and Thomashow, Linda S. Phenazine-1-carboxylic acid and soil moisture influence biofilm development and turnover of rhizobacterial biomass on wheat root surfaces: PCA and soil moisture impact biofilm development. United States: N. p., 2018. Web. doi:10.1111/1462-2920.14244.
LeTourneau, Melissa K., Marshall, Matthew J., Cliff, John B., Bonsall, Robert F., Dohnalkova, Alice C., Mavrodi, Dmitri V., Devi, S. Indira, Mavrodi, Olga V., Harsh, James B., Weller, David M., & Thomashow, Linda S. Phenazine-1-carboxylic acid and soil moisture influence biofilm development and turnover of rhizobacterial biomass on wheat root surfaces: PCA and soil moisture impact biofilm development. United States. doi:10.1111/1462-2920.14244.
LeTourneau, Melissa K., Marshall, Matthew J., Cliff, John B., Bonsall, Robert F., Dohnalkova, Alice C., Mavrodi, Dmitri V., Devi, S. Indira, Mavrodi, Olga V., Harsh, James B., Weller, David M., and Thomashow, Linda S. Fri . "Phenazine-1-carboxylic acid and soil moisture influence biofilm development and turnover of rhizobacterial biomass on wheat root surfaces: PCA and soil moisture impact biofilm development". United States. doi:10.1111/1462-2920.14244.
@article{osti_1468485,
title = {Phenazine-1-carboxylic acid and soil moisture influence biofilm development and turnover of rhizobacterial biomass on wheat root surfaces: PCA and soil moisture impact biofilm development},
author = {LeTourneau, Melissa K. and Marshall, Matthew J. and Cliff, John B. and Bonsall, Robert F. and Dohnalkova, Alice C. and Mavrodi, Dmitri V. and Devi, S. Indira and Mavrodi, Olga V. and Harsh, James B. and Weller, David M. and Thomashow, Linda S.},
abstractNote = {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 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 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.},
doi = {10.1111/1462-2920.14244},
journal = {Environmental Microbiology},
issn = {1462-2912},
number = 6,
volume = 20,
place = {United States},
year = {2018},
month = {6}
}

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