Environmental determinants of phenazine- and 2,4-diacetylphloroglucinol-producing Pseudomonas in the wheat rhizosphere across a precipitation gradient

Abstract

ABSTRACT The Columbia Plateau of the Inland Pacific Northwest (IPNW) encompasses one of North America’s largest dryland wheat production regions, where soil moisture strongly influences plant growth, health, and rhizosphere microbial communities. Two ecologically and genetically distinct groups of the Pseudomonas fluorescens complex naturally suppress soilborne wheat pathogens in IPNW fields by producing either phenazine-1-carboxylic acid (Phz+) or 2,4-diacetylphloroglucinol (Phl+). To determine how precipitation and associated soil factors shape the abundance of these bacteria, we analyzed wheat root samples from commercial fields spanning a precipitation gradient across the Columbia Plateau. We quantified pairwise relationships among environmental variables using Spearman correlations and constructed a correlation network to visualize patterns of association. Network analysis revealed that precipitation influences soil properties indirectly, with organic matter, clay content, cation exchange capacity, and pH forming an interconnected cluster of correlated variables. Wheat rhizosphere colonization frequency by Phz+ pseudomonads was primarily associated with soil pH, which correlated with precipitation through its effects on weathering and organic matter accumulation, whereas colonization frequency of Phl+ pseudomonads showed weaker associations with abiotic variables. Phz+ pseudomonads were favored in neutral to alkaline, coarse soils typical of the low-precipitation zone, whereas Phl+ populations thrived in wetter, organic-rich soils with lower pH. These findings highlight soil pH as a key environmental filter mediating precipitation-driven differences in Pseudomonas populations and suggest that biotic interactions and plant selection further modulate root colonization. Understanding how these agriculturally important microbial functional groups respond to moisture regimes provides insight into the sustainability of disease-suppressive microbiomes in the IPNW. IMPORTANCE Dryland wheat-based production systems of the Inland Pacific Northwest are highly vulnerable to changing precipitation patterns that affect crop productivity, soilborne pathogens, and soil microbial ecology. This study reveals how long-term rainfall gradients influence the balance between two groups of beneficial Pseudomonas that protect wheat from root diseases. We show that soil pH, closely linked to rainfall, organic matter, and mineral weathering, is a key abiotic factor controlling the presence of phenazine-producing bacteria in dryland wheat grown in low-precipitation zone soils. In contrast, 2,4-diacetylphloroglucinol producers dominate in wetter, organic-rich environments. These insights help explain how beneficial microbiomes adapt to environmental constraints and identify soil conditions that promote natural disease suppression. Understanding these mechanisms will aid in predicting microbiome resilience and guiding management strategies to maintain wheat productivity under changing weather conditions.