Effects of Phosphonate Herbicides on the Secretions of Plant-Beneficial Compounds by Two Plant Growth-Promoting Soil Bacteria: A Metabolomics Investigation

Abstract

Plant growth-promoting rhizobacteria (PGPR) that colonize plant roots produce a variety of plant-beneficial compounds, including plant-growth regulators, metal-scavenging compounds, and antibiotics against plant pathogens. Adverse effects of phosphonate herbicides, the most extensively used herbicides, on the growth and metabolism of PGPR species have been widely reported. However, the potential consequence of these effects on the biosynthesis and secretion of PGPR-derived beneficial compounds still remains to be investigated. Here, using high-resolution mass spectrometry and a metabolomics approach, we investigated both the intracellular metabolome and the extracellular secretions of biomass-normalized metabolite levels in two PGPR species (Pseudomonas protegens Pf-5, a Gram-negative bacterium; Priestia megaterium QM B1551, a Grampositive bacterium) exposed to three common phosphonate herbicides (glyphosate, glufosinate, and fosamine; 0.1−1 mM) in either iron (Fe)-replete or Fe-deficient nutrient media. We quantified secreted auxin-type plant hormone compounds (phenylacetic acid and indole-3-acetic acid), iron-scavenging compounds or siderophores (pyoverdine and schizokinen), and antibiotics (2,4diacetylphloroglucinol and pyoluteorin) produced by these PGPR species. The Fe-replete cells exposed to the phosphonate herbicides yielded up to a 25-fold increase in the production of both auxin and antibiotic compounds, indicating that herbicide exposure under Fe-replete conditions triggered metabolite secretions. However, the herbicide-exposed Fe-deficient cells exhibited a near 2-fold depletion in the secretion of these auxin and antibiotic compounds as well as a 77% decrease in siderophore production. Intracellular metabolomics analysis of the Fe-deficient cells further revealed metabolic perturbations in biosynthetic pathways consistent with the impaired production of the plant-beneficial compounds. Our findings implied that compromised cellular metabolism during nutrient deficiency may exacerbate the adverse effects of phosphonate herbicides on PGPR species.

Degradation kinetics and physiological studies of organophosphates degrading microorganisms for soil bioremediation

“…Explicitly, isolates S36 and S37 showed the highest sequence similarity with P. megaterium and P. arybhattia respectively. In correspondence, a number of studies have showed that, bacterial strains in the genus Pristia are versatile in degrading pesticides including atrazine (Abd Rani et al 2022 ), chlorpyrifos (Varghese et al 2022 ) and benzoate (Esikova et al 2021 ) using diverse metabolic pathways in mineralizing toxins and pesticides (Li et al 2022 ). Moreover, Pailan et al ( 2015 ) reported that B. arybhattia SanPS1 could tolerate chlorpyrifos and parathion at concentrations of 500 μg mL −1 .…”