Impact of phenazine-1-carboxylic acid upon the dynamics and wheat uptake of soil iron and manganese under dryland and irrigated conditions

Authors: LE TOURNEAU, MELISSA - Washington State University; MARSHALL, MATTHEW - Pacific Northwest National Laboratory; GRANT, MICHAEL - Washington State University; FREEZE, PATRICK - Washington State University; STRAWN, DANIEL - University Of Idaho; LAI, BARRY - Argonne National Laboratory; DOHNALKOVA, ALICE - Pacific Northwest National Laboratory; Weller, David; Thomashow, Linda; HARSH, JAMES - Washington State University

Submitted to: Environmental Science and Technology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/21/2019
Publication Date: 11/21/2019
Citation: Le Tourneau, M.K., Marshall, M.J., Grant, M.R., Freeze, P., Strawn, D., Lai, B., Dohnalkova, A.C., Weller, D.M., Thomashow, L.S., Harsh, J.B. 2019. Impact of phenazine-1-carboxylic acid upon the dynamics and wheat uptake of soil iron and manganese under dryland and irrigated conditions. Environmental Science and Technology. 2019,53,24,14273-14284. https://doi.org/10.1021/acs.est.9b03962.
DOI: https://doi.org/10.1021/acs.est.9b03962

Interpretive Summary: Bacteria associated with non-irrigated wheat roots produce the organic compound phenazine-1-carboxylic acid (PCA) in concentrations exceeding 1 microgram per gram of root in dry and semi-dry regions of the Columbia Plateau of Washington State, USA. PCA and other phenazines can dissolve iron (Fe) and manganese (Mn) (hydr)oxides in culture systems, but their impact upon these minerals in soil is unknown. Soil Fe and Mn cycles influence plant nutrition and the turnover of soil organic matter associated with high surface-area Fe and Mn (hydr)oxides. To optimize sustainable management practices in agro-ecosystems of the Columbia Plateau, which are susceptible to soil organic matter losses and wind erosion, it is necessary to clarify the impact of PCA upon soil Fe and Mn cycles. This study therefore addressed the impact of PCA upon soil Fe and Mn mineralogy and uptake by wheat. Concentrations of poorly-crystalline Fe were increased in soil associated with wheat roots that had been inoculated with the PCA-producing (PCA+) strain Pseudomonas synxantha 2-79 relative to roots inoculated with a PCA non-producing (PCA-) mutant derivative. Moreover, PCA--inoculated root zones exhibited an iron deficit relative to the bulk soil and the deficit was roughly equal to the uptake of Fe into wheat biomass, whereas it was smaller than the biomass-Fe in PCA+-inoculated root zones. Differences in plant uptake among the treatments were not large enough to account for the differences in soil Fe. These results indicate that PCA facilitated the conversion of soil Fe to poorly-crystalline forms, which were the primary Fe forms accessed by the wheat plants. X-ray spectroscopy revealed that Fe-bearing illite was the major Fe mineral in root-zone soil, but micro-scale Fe-bearing features attached to the roots were mixtures of Fe (hydr)oxides and clays. Significant differences in concentrations of iron and manganese in root-zone soil also were not observed. These results indicate that PCA promotes the formation of reactive, plant-avialable Fe phases, but any PCA-mediated transformations of Fe and Mn are transient, or are masked by competing processes. Furthermore PCA either does not produce a unique Fe mineral assemblage in Columbia Basin soils, or such assemblages are too transient, or are too limited in abundance to detect with the small sample size and methods employed in this study. However, the results of the study indicate that is likely that PCA+ bacteria influence Fe and Mn cycles with ramifications for soil health and crop nutrition in non-irrigated fields of the Columbia Plateau.

Technical Abstract: Bacteria associated with non-irrigated wheat roots produce phenazine-1-carboxylic acid (PCA) in concentrations exceeding 1 µg g-1 root in arid and semi-arid regions of the Columbia Plateau. PCA and other phenazines are potent redox-active antibiotics that reductively dissolve iron and manganese (hydr)oxides in culture systems, but their impact upon Fe and Mn cycling in soil is unknown. Soil Fe and Mn cycles influence plant nutrition and the turnover of soil organic matter associated with high surface-area Fe and Mn (hydr)oxides. To optimize sustainable management practices in agro-ecosystems of the Columbia Plateau, which are susceptible to soil organic matter losses and wind erosion, it is necessary to clarify the impact of PCA upon soil Fe and Mn cycles. This study therefore addresses the impact of PCA upon soil Fe and Mn mineralogy and uptake by wheat. Concentrations of poorly-crystalline Fe were increased in soil associated with wheat roots that had been inoculated with the PCA-producing (PCA+) strain Pseudomonas synxantha 2-79 relative to roots inoculated with a PCA non-producing (PCA-) mutant derivative. Moreover, PCA--inoculated root zones exhibited a poorly-crystalline Fe deficit relative to the bulk soil that was roughly equal to the uptake of Fe into wheat biomass, whereas the deficit was smaller than the biomass-Fe in PCA+-inoculated root zones. Differences in plant uptake among the treatments were insufficient to account for the differences in soil Fe. These results indicate that PCA facilitated the conversion of soil Fe to poorly-crystalline forms, which were the primary Fe forms accessed by the wheat plants. Multi-scale Fe K-edge X-ray absorption near edge spectroscopy (XANES) revealed that Fe-bearing illite was the major Fe phase in root-zone soil, but micro-scale Fe-bearing features attached to the roots were mixtures of Fe (hydr)oxides and clays. Consistent differences in Fe mineralogy and redox status were not observed among the small number of root-zone samples measured with XANES. Significant differences in concentrations of Fe(II) and Mn in root-zone soil also were not observed. These results indicate that PCA promotes the formation of reactive, plant-avialable Fe phases, but any PCA-mediated redox transformations of Fe and Mn are transient, or are masked by competing processes. Furthermore PCA either does not produce a unique Fe mineral assemblage in Columbia Basin soils, or such assemblages are too transient, or are too limited in abundance to detect with the small sample size and methods employed in this study. It is likely that PCA+ bacteria influence Fe and Mn cycles with ramifications for soil health and crop nutrition in non-irrigated fields of the Columbia Plateau.