The plant growth-promoting Burkholderia vietnamiensis produces acyl-homoserine lactones and modulates the quorum-sensing signaling in the rhizosphere

The genus <i>Burkholderia</i>, comprising over 60 species, represents a highly diverse group of bacteria known for their exceptional metabolic versatility. Quorum sensing (QS), a mechanism of cell-density-dependent gene regulation, plays a critical role in host colonization, environmental adaptation, and, in many cases, pathogenesis. Due to the established link between QS and virulence, most QS studies in <i>Burkholderia cepacia</i> complex (Bcc) species have focused on pathogenic strains. In contrast, comparatively little attention has been given to QS in plant growth-promoting (PGP) <i>Burkholderia</i> strains. In this study, we investigated the QS systems of <i>Burkholderia vietnamiensis</i> strains with plant growth-promoting potential. We identified two functional QS circuits, CepI/R and BviI/R, responsible for the synthesis of distinct AHL molecules with <i>N</i>-decanoyl homoserine lactone (C₁₀-HSL) as the dominant molecule. In <i>B. vietnamiensis</i> CBMB40, both synthases contributed to the production of N-hexanoyl (C₆-) and <i>N</i>-Octanoyl (C₈-) homoserine lactones, while <i>bviI</i> synthase contributed to the production of C₁₀-HSL and <i>N</i>-Dodecanoyl (C₁₂-) homoserine lactones. The AHLs produced by CBMB40 could be detected in plant tissues, and they served as interpopulation signaling molecules within the rhizosphere. A random transposon mutagenesis approach was employed to generate an AHL-deficient mutant (ΔCBMB40). The mutant exhibited an extended log phase, reduced protease activity, and loss of antagonism against <i>Erwinia carotovora</i> subsp. <i>carotovora</i>, as well as diminished activity against multiple fungal pathogens. Notably, the addition of AHL extracts from the wild-type strain restored antagonistic activity in the mutant. Furthermore, <i>in vitro</i> potato tuber assays and pot culture experiments in red pepper confirmed that AHL-mediated QS is essential for the biocontrol potential of CBMB40. Together, these findings enhance our understanding of QS-regulated functions in PGP <i>B. vietnamiensis</i> CBMB40 and support its potential application as a sustainable biocontrol agent in agriculture. Importantly, this study underscores the potential of using PGP bacteria (PGPB) to prime plant defenses, offering a biologically meaningful and ecologically sustainable alternative to genetically modified plants engineered with AHL synthase genes. AHL-mediated cross-communication in the rhizosphere may further disrupt pathogenic signaling, opening new avenues for microbiome-based crop protection strategies.