Loss of the flagellar regulator FlhC changes the transcriptional response of plant-associated Acidovorax delafieldii strains to metabolites from Rhizophagus irregularis-colonized Lotus japonicus roots.

Acidovorax is a cosmopolitan bacterial genus comprising both beneficial and pathogenic plant-associated species. In plant-associated bacteria, flagella can facilitate colonization but also trigger plant immune responses driving mutation or loss of flagella in some strains. FlhC is an important transcriptional regulator of flagella assembly genes. Here, we investigated whether it modulates root colonization and the transcriptional response of plant-commensal Acidovorax strains to different plant cues. As model cues, we used root extracts from Lotus japonicus that forms symbioses with arbuscular mycorrhiza fungi (AMF), which strongly change root metabolism and add their own metabolites. To offer different stimuli to Acidovorax bacteria, we used extracts from L. japonicus roots colonized or not with the AMF Rhizophagus irregularis. We investigated two Acidovorax delafieldii strains with almost identical genomes but differences in the presence or absence of flhC. Overall, loss of flhC resulted in distinct expression profiles and a more modular transcriptional network. Pathway analysis linked flhC to genes associated with stress tolerance, nutrient mobilization, biofilm formation, secretion, surface attachment, and quorum sensing. Root extracts from mycorrhizal roots induced increased expression of genes associated with substrate preference and downregulation of genes involved in biofilm formation and secretion. flhC-deficient strains also responded with increased expression of genes related to surface attachment and vitamin biosynthesis. The absence of flhC correlated with increased root colonization and influenced the response of Acidovorax to R. irregularis in planta. Our findings highlight that a flagellar regulator in root-associated bacteria influences root colonization and transcriptional responses to host cues.