Phenazine-1-Carboxylic Acid-Producing Bacteria Enhance the Reactivity of Iron Minerals in Dryland and Irrigated Wheat Rhizospheres

LeTourneau, Melissa K.; Marshall, Matthew J.; Grant, Michael; Freeze, Patrick M.; Strawn, Daniel G.; Lai, Barry; Dohnalkova, Alice C.; Harsh, James B.; Weller, David M.; Thomashow, Linda S.

doi:10.1021/acs.est.9b03962

Title: Phenazine-1-Carboxylic Acid-Producing Bacteria Enhance the Reactivity of Iron Minerals in Dryland and Irrigated Wheat Rhizospheres

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Abstract

Phenazine-1-carboxylic acid (PCA) is a broad-spectrum antibiotic produced by rhizobacteria in the dryland wheat fields of the Columbia Plateau. PCA and other phenazines reductively dissolve Fe and Mn oxyhydroxides in bacterial culture systems, but the impact of PCA upon Fe and Mn cycling in the rhizosphere is unknown. Here, concentrations of dithionite-extractable and poorly crystalline Fe were approximately 10% and 30–40% higher, respectively, in dryland and irrigated rhizospheres inoculated with the PCA-producing (PCA⁺) strain Pseudomonas synxantha 2–79 than in rhizospheres inoculated with a PCA-deficient mutant. Yet, rhizosphere concentrations of Fe(II) and Mn did not differ significantly, indicating that PCA-mediated redox transformations of Fe and Mn were transient or were masked by competing processes. Total Fe and Mn uptake into wheat biomass also did not differ significantly, but the PCA⁺ strain significantly altered Fe translocation into shoots. X-ray absorption near edge spectroscopy revealed an abundance of Fe-bearing oxyhydroxides and phyllosilicates in all rhizospheres. These findings indicate that the PCA⁺ strain enhanced the reactivity and mobility of Fe derived from soil minerals without producing parallel changes in plant Fe uptake. This is the first report that directly links significant alterations of Fe-bearing minerals in the rhizosphere to a single bacterial trait.

Authors:

^[1]; Marshall, Matthew J. ^[2]; Grant, Michael ^[3]; Freeze, Patrick M. ^[3]; Strawn, Daniel G. ^[4]; Lai, Barry ^[5]; Dohnalkova, Alice C. ^[6]; Harsh, James B. ^[3]; Weller, David M. ^[7]; Thomashow, Linda S. ^[7]

Washington State Univ., Pullman, WA (United States); US Dept. of Agriculture (USDA), Pullman, WA (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Washington State Univ., Pullman, WA (United States)
Univ. of Idaho, Moscow, ID (United States)
Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
US Dept. of Agriculture (USDA), Pullman, WA (United States)

Publication Date:: Thu Nov 21 00:00:00 EST 2019

Research Org.:: Argonne National Lab. (ANL), Argonne, IL (United States); Oak Ridge Associated Univ., Oak Ridge, TN (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States); SLAC National Accelerator Lab., Menlo Park, CA (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Workforce Development for Teachers and Scientists (WDTS); National Institutes of Health (NIH)

OSTI Identifier:: 1617373

Grant/Contract Number:: AC02-06CH11357; SC0014664; AC05-76RL01830; AC02-76SF00515

Resource Type:: Accepted Manuscript

Journal Name:: Environmental Science and Technology

Additional Journal Information:: Journal Volume: 53; Journal Issue: 24; Journal ID: ISSN 0013-936X

Publisher:: American Chemical Society (ACS)

Country of Publication:: United States

Language:: English

Subject:: 54 ENVIRONMENTAL SCIENCES

Citation Formats


                    LeTourneau, Melissa K., Marshall, Matthew J., Grant, Michael, Freeze, Patrick M., Strawn, Daniel G., Lai, Barry, Dohnalkova, Alice C., Harsh, James B., Weller, David M., and Thomashow, Linda S. Phenazine-1-Carboxylic Acid-Producing Bacteria Enhance the Reactivity of Iron Minerals in Dryland and Irrigated Wheat Rhizospheres.  United States: N. p., 2019. 
Web.  doi:10.1021/acs.est.9b03962.

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                    LeTourneau, Melissa K., Marshall, Matthew J., Grant, Michael, Freeze, Patrick M., Strawn, Daniel G., Lai, Barry, Dohnalkova, Alice C., Harsh, James B., Weller, David M., & Thomashow, Linda S. Phenazine-1-Carboxylic Acid-Producing Bacteria Enhance the Reactivity of Iron Minerals in Dryland and Irrigated Wheat Rhizospheres.  United States.  https://doi.org/10.1021/acs.est.9b03962

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                    LeTourneau, Melissa K., Marshall, Matthew J., Grant, Michael, Freeze, Patrick M., Strawn, Daniel G., Lai, Barry, Dohnalkova, Alice C., Harsh, James B., Weller, David M., and Thomashow, Linda S. Thu .  
"Phenazine-1-Carboxylic Acid-Producing Bacteria Enhance the Reactivity of Iron Minerals in Dryland and Irrigated Wheat Rhizospheres".  United States.  https://doi.org/10.1021/acs.est.9b03962.  https://www.osti.gov/servlets/purl/1617373.

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@article{osti_1617373,

  title        = {Phenazine-1-Carboxylic Acid-Producing Bacteria Enhance the Reactivity of Iron Minerals in Dryland and Irrigated Wheat Rhizospheres},

  author       = {LeTourneau, Melissa K. and Marshall, Matthew J. and Grant, Michael and Freeze, Patrick M. and Strawn, Daniel G. and Lai, Barry and Dohnalkova, Alice C. and Harsh, James B. and Weller, David M. and Thomashow, Linda S.},

  abstractNote = {Phenazine-1-carboxylic acid (PCA) is a broad-spectrum antibiotic produced by rhizobacteria in the dryland wheat fields of the Columbia Plateau. PCA and other phenazines reductively dissolve Fe and Mn oxyhydroxides in bacterial culture systems, but the impact of PCA upon Fe and Mn cycling in the rhizosphere is unknown. Here, concentrations of dithionite-extractable and poorly crystalline Fe were approximately 10% and 30–40% higher, respectively, in dryland and irrigated rhizospheres inoculated with the PCA-producing (PCA+) strain Pseudomonas synxantha 2–79 than in rhizospheres inoculated with a PCA-deficient mutant. Yet, rhizosphere concentrations of Fe(II) and Mn did not differ significantly, indicating that PCA-mediated redox transformations of Fe and Mn were transient or were masked by competing processes. Total Fe and Mn uptake into wheat biomass also did not differ significantly, but the PCA+ strain significantly altered Fe translocation into shoots. X-ray absorption near edge spectroscopy revealed an abundance of Fe-bearing oxyhydroxides and phyllosilicates in all rhizospheres. These findings indicate that the PCA+ strain enhanced the reactivity and mobility of Fe derived from soil minerals without producing parallel changes in plant Fe uptake. This is the first report that directly links significant alterations of Fe-bearing minerals in the rhizosphere to a single bacterial trait.},

  doi          = {10.1021/acs.est.9b03962},

  journal      = {Environmental Science and Technology},

  number       = 24,

  volume       = 53,

  place        = {United States},

  year         = {Thu Nov 21 00:00:00 EST 2019},

  month        = {Thu Nov 21 00:00:00 EST 2019}

}

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