1-Aminocyclopropane-1-Carboxylate and Its Chemoreceptor Drive Metabolic Reprogramming to Enhance Chemotactic Rhizocompetence in Pseudomonas sp. UW4

1-Aminocyclopropane-1-carboxylate (ACC) has been identified as the preferred chemoattractant driving rhizosphere colonization by the model plant growth-promoting rhizobacterium (PGPR) Pseudomonas sp. UW4. However, the regulatory mechanisms governing the expression of its ACC chemoreceptor WP116, as well as how changes in its abundance influence ACC chemotaxis and rhizosphere colonization, remain poorly understood. In this study, we found that the addition of ACC (3.0 mM) during the mid-logarithmic growth phase of UW4 rapidly induced the transcription of WP116 (up to 1.4-fold) and several other chemoreceptor genes, promoted bacterial growth by increasing the maximum specific growth rate by 21.1% (p < 0.05), yet did not significantly alter the protein abundance of chemoreceptors. At the proteome level, however, ACC drove a reprogramming of carbon, nitrogen, and energy metabolism, facilitating the transition of cells from a motile to a colonizing state. Furthermore, trans-overexpression of WP116 disrupted the homeostatic balance of receptor abundance, leading to a marked increase in its protein level (up to 32.3-fold) and enhancing both the ACC chemotactic response (up to 3–5-fold) and the rhizosphere colonization competitiveness (up to 9-fold) of UW4 (p < 0.05). These findings not only deepen our understanding of the molecular mechanisms underlying metabolism-dependent chemotaxis but also provide a novel technological avenue for rhizosphere microbiome engineering aimed at directionally enhancing the chemotactic rhizocompetence of PGPR.