Ralstonia pseudosolanacearum LOV domain protein regulates environmental stress tolerance, iron homeostasis and bacterial wilt virulence

Bacteria use diverse sensors to integrate environmental stimuli into physiological responses that ensure fitness and survival. Ralstonia pseudosolanacearum (Rps), a soil-borne plant pathogen that causes bacterial wilt disease, encodes a conserved LOV (light-oxygen-voltage) protein known to mediate photoreception across the tree of life. However, Rps had a minimal LOV-dependent transcriptional response to light. Using clues from functional domains, the lov genomic neighborhood, and in planta transcriptional analyses, we tested the hypothesis that LOV shapes Rps biology in response to stress. We discovered lov modulates Rps stress response and virulence independently of light cues, but in a plant-dependent fashion. A ?lov mutant had reduced heat tolerance that required a conserved flavin mononucleotide-binding cysteine residue. Deleting lov caused broad metabolic dysregulation, leading to growth defects on several carbon sources. In contrast ?lov grew better in ex vivo tomato xylem sap and in high-iron medium, a possible consequence of its increased siderophore production. However, LOV is essential for full virulence in the host, mediating attachment to the root surface, stem colonization, and overall symptom development. Together these findings reveal that LOV, which is highly conserved among plant pathogenic Ralstonia, regulates a myriad of functions required for plant fitness independently of light. Overall design: RNAseq data of Ralstonia pseudosolanacearum strain GMI1000 wild-type compared to ?lov both in vitro and in planta conditions. In vitro cells were subjected to blue light and dark conditions.